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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus <italic>Laccaria bicolor</italic></title><author><name sortKey="Daguerre, Y" sort="Daguerre, Y" uniqKey="Daguerre Y" first="Y." last="Daguerre">Y. Daguerre</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8578 2742</institution-id><institution-id institution-id-type="GRID">grid.6341.0</institution-id><institution>Present address: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology,</institution><institution>Swedish University of Agricultural Sciences,</institution></institution-wrap>901 83, Umea, Sweden</nlm:aff></affiliation></author><author><name sortKey="Levati, E" sort="Levati, E" uniqKey="Levati E" first="E." last="Levati">E. Levati</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</nlm:aff></affiliation></author><author><name sortKey="Ruytinx, J" sort="Ruytinx, J" uniqKey="Ruytinx J" first="J." last="Ruytinx">J. Ruytinx</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff5">Present address: Hasselt University, Centre for Environmental Sciences, Agoralaan building D, 3590 Diepenbeek, Belgium</nlm:aff></affiliation></author><author><name sortKey="Tisserant, E" sort="Tisserant, E" uniqKey="Tisserant E" first="E." last="Tisserant">E. Tisserant</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Morin, E" sort="Morin, E" uniqKey="Morin E" first="E." last="Morin">E. Morin</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Kohler, A" sort="Kohler, A" uniqKey="Kohler A" first="A." last="Kohler">A. Kohler</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Montanini, B" sort="Montanini, B" uniqKey="Montanini B" first="B." last="Montanini">B. Montanini</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</nlm:aff></affiliation></author><author><name sortKey="Ottonello, S" sort="Ottonello, S" uniqKey="Ottonello S" first="S." last="Ottonello">S. Ottonello</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</nlm:aff></affiliation></author><author><name sortKey="Brun, A" sort="Brun, A" uniqKey="Brun A" first="A." last="Brun">A. Brun</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Veneault Fourrey, C" sort="Veneault Fourrey, C" uniqKey="Veneault Fourrey C" first="C." last="Veneault-Fourrey">C. Veneault-Fourrey</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Martin, F" sort="Martin, F" uniqKey="Martin F" first="F." last="Martin">F. Martin</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28923004</idno><idno type="pmc">5604158</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5604158</idno><idno type="RBID">PMC:5604158</idno><idno type="doi">10.1186/s12864-017-4114-7</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">000159</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000159</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus <italic>Laccaria bicolor</italic></title><author><name sortKey="Daguerre, Y" sort="Daguerre, Y" uniqKey="Daguerre Y" first="Y." last="Daguerre">Y. Daguerre</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8578 2742</institution-id><institution-id institution-id-type="GRID">grid.6341.0</institution-id><institution>Present address: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology,</institution><institution>Swedish University of Agricultural Sciences,</institution></institution-wrap>901 83, Umea, Sweden</nlm:aff></affiliation></author><author><name sortKey="Levati, E" sort="Levati, E" uniqKey="Levati E" first="E." last="Levati">E. Levati</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</nlm:aff></affiliation></author><author><name sortKey="Ruytinx, J" sort="Ruytinx, J" uniqKey="Ruytinx J" first="J." last="Ruytinx">J. Ruytinx</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff5">Present address: Hasselt University, Centre for Environmental Sciences, Agoralaan building D, 3590 Diepenbeek, Belgium</nlm:aff></affiliation></author><author><name sortKey="Tisserant, E" sort="Tisserant, E" uniqKey="Tisserant E" first="E." last="Tisserant">E. Tisserant</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Morin, E" sort="Morin, E" uniqKey="Morin E" first="E." last="Morin">E. Morin</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Kohler, A" sort="Kohler, A" uniqKey="Kohler A" first="A." last="Kohler">A. Kohler</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Montanini, B" sort="Montanini, B" uniqKey="Montanini B" first="B." last="Montanini">B. Montanini</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</nlm:aff></affiliation></author><author><name sortKey="Ottonello, S" sort="Ottonello, S" uniqKey="Ottonello S" first="S." last="Ottonello">S. Ottonello</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</nlm:aff></affiliation></author><author><name sortKey="Brun, A" sort="Brun, A" uniqKey="Brun A" first="A." last="Brun">A. Brun</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Veneault Fourrey, C" sort="Veneault Fourrey, C" uniqKey="Veneault Fourrey C" first="C." last="Veneault-Fourrey">C. Veneault-Fourrey</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author><author><name sortKey="Martin, F" sort="Martin, F" uniqKey="Martin F" first="F." last="Martin">F. Martin</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</nlm:aff></affiliation></author></analytic><series><title level="j">BMC Genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus <italic>Laccaria bicolor</italic>.</p></sec><sec><title>Results</title><p id="Par2">We curated the <italic>L. bicolor</italic> gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The <italic>L. bicolor</italic> core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of <italic>L. bicolor</italic> and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs).</p></sec><sec><title>Conclusions</title><p id="Par3">Transcriptional regulators required for ECM symbiosis development in <italic>L. bicolor</italic> have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (10.1186/s12864-017-4114-7) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Andrianopoulos, A" uniqKey="Andrianopoulos A">A Andrianopoulos</name></author><author><name sortKey="Timberlake, We" uniqKey="Timberlake W">WE Timberlake</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bibbins, M" uniqKey="Bibbins M">M Bibbins</name></author><author><name sortKey="Crepin, Vf" uniqKey="Crepin V">VF Crepin</name></author><author><name sortKey="Cummings, Nj" uniqKey="Cummings N">NJ Cummings</name></author><author><name sortKey="Mizote, T" uniqKey="Mizote T">T Mizote</name></author><author><name sortKey="Baker, K" uniqKey="Baker K">K Baker</name></author><author><name sortKey="Mellits, Kh" uniqKey="Mellits K">KH Mellits</name></author><author><name sortKey="Connerton, If" uniqKey="Connerton I">IF Connerton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bin Yusof, Mt" uniqKey="Bin Yusof M">MT Bin Yusof</name></author><author><name sortKey="Kershaw, Mj" uniqKey="Kershaw M">MJ Kershaw</name></author><author><name sortKey="Soanes, Dm" uniqKey="Soanes D">DM Soanes</name></author><author><name sortKey="Talbot, Nj" uniqKey="Talbot N">NJ Talbot</name></author><author><name sortKey="Zhang, Z" uniqKey="Zhang Z">Z Zhang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brown, Aj" uniqKey="Brown A">AJ Brown</name></author><author><name sortKey="Casselton, La" uniqKey="Casselton L">LA Casselton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brundrett, Mc" uniqKey="Brundrett M">MC Brundrett</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Burgess, T" uniqKey="Burgess T">T Burgess</name></author><author><name sortKey="Dell, B" uniqKey="Dell B">B Dell</name></author><author><name sortKey="Malajczuk, N" uniqKey="Malajczuk N">N Malajczuk</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chang, Yc" uniqKey="Chang Y">YC Chang</name></author><author><name sortKey="Wright, Lc" uniqKey="Wright L">LC Wright</name></author><author><name sortKey="Tscharke, Rl" uniqKey="Tscharke R">RL Tscharke</name></author><author><name sortKey="Sorrell, Tc" uniqKey="Sorrell T">TC Sorrell</name></author><author><name sortKey="Wilson, Cf" uniqKey="Wilson C">CF Wilson</name></author><author><name sortKey="Kwon Chung, Kj" uniqKey="Kwon Chung K">KJ Kwon-Chung</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cleary, Ia" uniqKey="Cleary I">IA Cleary</name></author><author><name sortKey="Mulabagal, P" uniqKey="Mulabagal P">P Mulabagal</name></author><author><name sortKey="Reinhard, Sm" uniqKey="Reinhard S">SM Reinhard</name></author><author><name sortKey="Yadev, Np" uniqKey="Yadev N">NP Yadev</name></author><author><name sortKey="Murdoch, C" uniqKey="Murdoch C">C Murdoch</name></author><author><name sortKey="Thornhill, Mh" uniqKey="Thornhill M">MH Thornhill</name></author><author><name sortKey="Lazzell, Al" uniqKey="Lazzell A">AL Lazzell</name></author><author><name sortKey="Monteagudo, C" uniqKey="Monteagudo C">C Monteagudo</name></author><author><name sortKey="Thomas, Dp" uniqKey="Thomas D">DP Thomas</name></author><author><name sortKey="Saville, Sp" uniqKey="Saville S">SP Saville</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="David, H" uniqKey="David H">H David</name></author><author><name sortKey="Krogh, Am" uniqKey="Krogh A">AM Krogh</name></author><author><name sortKey="Roca, C" uniqKey="Roca C">C Roca</name></author><author><name sortKey="Akesson, M" uniqKey="Akesson M">M Akesson</name></author><author><name sortKey="Nielsen, J" uniqKey="Nielsen J">J Nielsen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Delaunay, A" uniqKey="Delaunay A">A Delaunay</name></author><author><name sortKey="Isnard, Ad" uniqKey="Isnard A">AD Isnard</name></author><author><name sortKey="Toledano, Mb" uniqKey="Toledano M">MB Toledano</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Deveau, A" uniqKey="Deveau A">A Deveau</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Frey Klett, P" uniqKey="Frey Klett P">P Frey-Klett</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Duddridge, Ja" uniqKey="Duddridge J">JA Duddridge</name></author><author><name sortKey="Read, Dj" uniqKey="Read D">DJ Read</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Duplessis, S" uniqKey="Duplessis S">S Duplessis</name></author><author><name sortKey="Courty, Pe" uniqKey="Courty P">PE Courty</name></author><author><name sortKey="Tagu, D" uniqKey="Tagu D">D Tagu</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Felten, J" uniqKey="Felten J">J Felten</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Bhalerao, Rp" uniqKey="Bhalerao R">RP Bhalerao</name></author><author><name sortKey="Palme, K" uniqKey="Palme K">K Palme</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Ditengou, Fa" uniqKey="Ditengou F">FA Ditengou</name></author><author><name sortKey="Legue, V" uniqKey="Legue V">V Legué</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Felten, J" uniqKey="Felten J">J Felten</name></author><author><name sortKey="Legue, V" uniqKey="Legue V">V Legué</name></author><author><name sortKey="Ditengou, Fa" uniqKey="Ditengou F">FA Ditengou</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fujioka, T" uniqKey="Fujioka T">T Fujioka</name></author><author><name sortKey="Mizutani, O" uniqKey="Mizutani O">O Mizutani</name></author><author><name sortKey="Furukawa, K" uniqKey="Furukawa K">K Furukawa</name></author><author><name sortKey="Sato, N" uniqKey="Sato N">N Sato</name></author><author><name sortKey="Yoshimi, A" uniqKey="Yoshimi A">A Yoshimi</name></author><author><name sortKey="Yamagata, Y" uniqKey="Yamagata Y">Y Yamagata</name></author><author><name sortKey="Nakajima, T" uniqKey="Nakajima T">T Nakajima</name></author><author><name sortKey="Abe, K" uniqKey="Abe K">K Abe</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Goldar, Mm" uniqKey="Goldar M">MM Goldar</name></author><author><name sortKey="Jeong, Ht" uniqKey="Jeong H">HT Jeong</name></author><author><name sortKey="Tanaka, K" uniqKey="Tanaka K">K Tanaka</name></author><author><name sortKey="Matsuda, H" uniqKey="Matsuda H">H Matsuda</name></author><author><name sortKey="Kawamukai, M" uniqKey="Kawamukai M">M Kawamukai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hacquard, S" uniqKey="Hacquard S">S Hacquard</name></author><author><name sortKey="Delaruelle, C" uniqKey="Delaruelle C">C Delaruelle</name></author><author><name sortKey="Legue, V" uniqKey="Legue V">V Legué</name></author><author><name sortKey="Tisserant, E" uniqKey="Tisserant E">E Tisserant</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Frey, P" uniqKey="Frey P">P Frey</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Duplessis, S" uniqKey="Duplessis S">S Duplessis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hall, Da" uniqKey="Hall D">DA Hall</name></author><author><name sortKey="Zhu, H" uniqKey="Zhu H">H Zhu</name></author><author><name sortKey="Zhu, X" uniqKey="Zhu X">X Zhu</name></author><author><name sortKey="Royce, T" uniqKey="Royce T">T Royce</name></author><author><name sortKey="Gerstein, M" uniqKey="Gerstein M">M Gerstein</name></author><author><name sortKey="Snyder, M" uniqKey="Snyder M">M Snyder</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hartmann, Ha" uniqKey="Hartmann H">HA Hartmann</name></author><author><name sortKey="Kahmann, R" uniqKey="Kahmann R">R Kahmann</name></author><author><name sortKey="Bolker, M" uniqKey="Bolker M">M Bölker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hu, S" uniqKey="Hu S">S Hu</name></author><author><name sortKey="Xie, Z" uniqKey="Xie Z">Z Xie</name></author><author><name sortKey="Onishi, A" uniqKey="Onishi A">A Onishi</name></author><author><name sortKey="Yu, X" uniqKey="Yu X">X Yu</name></author><author><name sortKey="Jiang, L" uniqKey="Jiang L">L Jiang</name></author><author><name sortKey="Lin, J" uniqKey="Lin J">J Lin</name></author><author><name sortKey="Rho, Hs" uniqKey="Rho H">HS Rho</name></author><author><name sortKey="Woodard, C" uniqKey="Woodard C">C Woodard</name></author><author><name sortKey="Wang, H" uniqKey="Wang H">H Wang</name></author><author><name sortKey="Jeong, Js" uniqKey="Jeong J">JS Jeong</name></author><author><name sortKey="Long, S" uniqKey="Long S">S Long</name></author><author><name sortKey="He, X" uniqKey="He X">X He</name></author><author><name sortKey="Wade, H" uniqKey="Wade H">H Wade</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Johansson, T" uniqKey="Johansson T">T Johansson</name></author><author><name sortKey="Le Quere, A" uniqKey="Le Quere A">A Le Quéré</name></author><author><name sortKey="Ahren, D" uniqKey="Ahren D">D Ahren</name></author><author><name sortKey="Soderstrom, B" uniqKey="Soderstrom B">B Söderström</name></author><author><name sortKey="Erlandsson, R" uniqKey="Erlandsson R">R Erlandsson</name></author><author><name sortKey="Lundeberg, J" uniqKey="Lundeberg J">J Lundeberg</name></author><author><name sortKey="Uhlen, M" uniqKey="Uhlen M">M Uhlén</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jung, Us" uniqKey="Jung U">US Jung</name></author><author><name sortKey="Sobering, Ak" uniqKey="Sobering A">AK Sobering</name></author><author><name sortKey="Romeo, Mj" uniqKey="Romeo M">MJ Romeo</name></author><author><name sortKey="Levin, De" uniqKey="Levin D">DE Levin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kadosh, D" uniqKey="Kadosh D">D Kadosh</name></author><author><name sortKey="Johnson, Ad" uniqKey="Johnson A">AD Johnson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Kuo, A" uniqKey="Kuo A">A Kuo</name></author><author><name sortKey="Nagy, Lg" uniqKey="Nagy L">LG Nagy</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Barry, Kw" uniqKey="Barry K">KW Barry</name></author><author><name sortKey="Buscot, F" uniqKey="Buscot F">F Buscot</name></author><author><name sortKey="Canb Ck, B" uniqKey="Canb Ck B">B Canbäck</name></author><author><name sortKey="Choi, C" uniqKey="Choi C">C Choi</name></author><author><name sortKey="Cichocki, N" uniqKey="Cichocki N">N Cichocki</name></author><author><name sortKey="Clum, A" uniqKey="Clum A">A Clum</name></author><author><name sortKey="Colpaert, J" uniqKey="Colpaert J">J Colpaert</name></author><author><name sortKey="Copeland, A" uniqKey="Copeland A">A Copeland</name></author><author><name sortKey="Costa, Md" uniqKey="Costa M">MD Costa</name></author><author><name sortKey="Dore, J" uniqKey="Dore J">J Doré</name></author><author><name sortKey="Floudas, D" uniqKey="Floudas D">D Floudas</name></author><author><name sortKey="Gay, G" uniqKey="Gay G">G Gay</name></author><author><name sortKey="Girlanda, M" uniqKey="Girlanda M">M Girlanda</name></author><author><name sortKey="Henrissat, B" uniqKey="Henrissat B">B Henrissat</name></author><author><name sortKey="Herrmann, S" uniqKey="Herrmann S">S Herrmann</name></author><author><name sortKey="Hess, J" uniqKey="Hess J">J Hess</name></author><author><name sortKey="Hogberg, N" uniqKey="Hogberg N">N Högberg</name></author><author><name sortKey="Johansson, T" uniqKey="Johansson T">T Johansson</name></author><author><name sortKey="Khouja, Hr" uniqKey="Khouja H">HR Khouja</name></author><author><name sortKey="Labutti, K" uniqKey="Labutti K">K LaButti</name></author><author><name sortKey="Lahrmann, U" uniqKey="Lahrmann U">U Lahrmann</name></author><author><name sortKey="Levasseur, A" uniqKey="Levasseur A">A Levasseur</name></author><author><name sortKey="Lindquist, Ea" uniqKey="Lindquist E">EA Lindquist</name></author><author><name sortKey="Lipzen, A" uniqKey="Lipzen A">A Lipzen</name></author><author><name sortKey="Marmeisse, R" uniqKey="Marmeisse R">R Marmeisse</name></author><author><name sortKey="Martino, E" uniqKey="Martino E">E Martino</name></author><author><name sortKey="Murat, C" uniqKey="Murat C">C Murat</name></author><author><name sortKey="Ngan, Cy" uniqKey="Ngan C">CY Ngan</name></author><author><name sortKey="Nehls, U" uniqKey="Nehls U">U Nehls</name></author><author><name sortKey="Plett, Jm" uniqKey="Plett J">JM Plett</name></author><author><name sortKey="Pringle, A" uniqKey="Pringle A">A Pringle</name></author><author><name sortKey="Ohm, Ra" uniqKey="Ohm R">RA Ohm</name></author><author><name sortKey="Perotto, S" uniqKey="Perotto S">S Perotto</name></author><author><name sortKey="Peter, M" uniqKey="Peter M">M Peter</name></author><author><name sortKey="Riley, R" uniqKey="Riley R">R Riley</name></author><author><name sortKey="Rineau, F" uniqKey="Rineau F">F Rineau</name></author><author><name sortKey="Ruytinx, J" uniqKey="Ruytinx J">J Ruytinx</name></author><author><name sortKey="Salamov, A" uniqKey="Salamov A">A Salamov</name></author><author><name sortKey="Shah, F" uniqKey="Shah F">F Shah</name></author><author><name sortKey="Sun, H" uniqKey="Sun H">H Sun</name></author><author><name sortKey="Tarkka, M" uniqKey="Tarkka M">M Tarkka</name></author><author><name sortKey="Tritt, A" uniqKey="Tritt A">A Tritt</name></author><author><name sortKey="Veneault Fourrey, C" uniqKey="Veneault Fourrey C">C Veneault-Fourrey</name></author><author><name sortKey="Zuccaro, A" uniqKey="Zuccaro A">A Zuccaro</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author><author><name sortKey="Grigoriev, Iv" uniqKey="Grigoriev I">IV Grigoriev</name></author><author><name sortKey="Hibbett, Ds" uniqKey="Hibbett D">DS Hibbett</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Larsen, Pe" uniqKey="Larsen P">PE Larsen</name></author><author><name sortKey="Sreedasyam, A" uniqKey="Sreedasyam A">A Sreedasyam</name></author><author><name sortKey="Trivedi, G" uniqKey="Trivedi G">G Trivedi</name></author><author><name sortKey="Podila, Gk" uniqKey="Podila G">GK Podila</name></author><author><name sortKey="Cseke, Lj" uniqKey="Cseke L">LJ Cseke</name></author><author><name sortKey="Collart, Fr" uniqKey="Collart F">FR Collart</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Le Quere, A" uniqKey="Le Quere A">A Le Queré</name></author><author><name sortKey="Wright, Dp" uniqKey="Wright D">DP Wright</name></author><author><name sortKey="Soderstrom, B" uniqKey="Soderstrom B">B Söderström</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author><author><name sortKey="Johansson, T" uniqKey="Johansson T">T Johansson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lev, S" uniqKey="Lev S">S Lev</name></author><author><name sortKey="Hadar, R" uniqKey="Hadar R">R Hadar</name></author><author><name sortKey="Amedeo, P" uniqKey="Amedeo P">P Amedeo</name></author><author><name sortKey="Baker, Se" uniqKey="Baker S">SE Baker</name></author><author><name sortKey="Yoder, Oc" uniqKey="Yoder O">OC Yoder</name></author><author><name sortKey="Horwitz, Ba" uniqKey="Horwitz B">BA Horwitz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Levati, E" uniqKey="Levati E">E Levati</name></author><author><name sortKey="Sartini, S" uniqKey="Sartini S">S Sartini</name></author><author><name sortKey="Bolchi, A" uniqKey="Bolchi A">A Bolchi</name></author><author><name sortKey="Ottonello, S" uniqKey="Ottonello S">S Ottonello</name></author><author><name sortKey="Montanini, B" uniqKey="Montanini B">B Montanini</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Levati, E" uniqKey="Levati E">E Levati</name></author><author><name sortKey="Sartini, S" uniqKey="Sartini S">S Sartini</name></author><author><name sortKey="Ottonello, S" uniqKey="Ottonello S">S Ottonello</name></author><author><name sortKey="Montanini, B" uniqKey="Montanini B">B Montanini</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Aerts, A" uniqKey="Aerts A">A Aerts</name></author><author><name sortKey="Ahren, D" uniqKey="Ahren D">D Ahrén</name></author><author><name sortKey="Brun, A" uniqKey="Brun A">A Brun</name></author><author><name sortKey="Danchin, Eg" uniqKey="Danchin E">EG Danchin</name></author><author><name sortKey="Duchaussoy, F" uniqKey="Duchaussoy F">F Duchaussoy</name></author><author><name sortKey="Gibon, J" uniqKey="Gibon J">J Gibon</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Lindquist, E" uniqKey="Lindquist E">E Lindquist</name></author><author><name sortKey="Pereda, V" uniqKey="Pereda V">V Pereda</name></author><author><name sortKey="Salamov, A" uniqKey="Salamov A">A Salamov</name></author><author><name sortKey="Shapiro, Hj" uniqKey="Shapiro H">HJ Shapiro</name></author><author><name sortKey="Wuyts, J" uniqKey="Wuyts J">J Wuyts</name></author><author><name sortKey="Blaudez, D" uniqKey="Blaudez D">D Blaudez</name></author><author><name sortKey="Buee, M" uniqKey="Buee M">M Buée</name></author><author><name sortKey="Brokstein, P" uniqKey="Brokstein P">P Brokstein</name></author><author><name sortKey="Canb Ck, B" uniqKey="Canb Ck B">B Canbäck</name></author><author><name sortKey="Cohen, D" uniqKey="Cohen D">D Cohen</name></author><author><name sortKey="Courty, Pe" uniqKey="Courty P">PE Courty</name></author><author><name sortKey="Coutinho, Pm" uniqKey="Coutinho P">PM Coutinho</name></author><author><name sortKey="Delaruelle, C" uniqKey="Delaruelle C">C Delaruelle</name></author><author><name sortKey="Detter, Jc" uniqKey="Detter J">JC Detter</name></author><author><name sortKey="Deveau, A" uniqKey="Deveau A">A Deveau</name></author><author><name sortKey="Difazio, S" uniqKey="Difazio S">S DiFazio</name></author><author><name sortKey="Duplessis, S" uniqKey="Duplessis S">S Duplessis</name></author><author><name sortKey="Fraissinet Tachet, L" uniqKey="Fraissinet Tachet L">L Fraissinet-Tachet</name></author><author><name sortKey="Lucic, E" uniqKey="Lucic E">E Lucic</name></author><author><name sortKey="Frey Klett, P" uniqKey="Frey Klett P">P Frey-Klett</name></author><author><name sortKey="Fourrey, C" uniqKey="Fourrey C">C Fourrey</name></author><author><name sortKey="Feussner, I" uniqKey="Feussner I">I Feussner</name></author><author><name sortKey="Gay, G" uniqKey="Gay G">G Gay</name></author><author><name sortKey="Grimwood, J" uniqKey="Grimwood J">J Grimwood</name></author><author><name sortKey="Hoegger, Pj" uniqKey="Hoegger P">PJ Hoegger</name></author><author><name sortKey="Jain, P" uniqKey="Jain P">P Jain</name></author><author><name sortKey="Kilaru, S" uniqKey="Kilaru S">S Kilaru</name></author><author><name sortKey="Labbe, J" uniqKey="Labbe J">J Labbé</name></author><author><name sortKey="Lin, Yc" uniqKey="Lin Y">YC Lin</name></author><author><name sortKey="Legue, V" uniqKey="Legue V">V Legué</name></author><author><name sortKey="Le Tacon, F" uniqKey="Le Tacon F">F Le Tacon</name></author><author><name sortKey="Marmeisse, R" uniqKey="Marmeisse R">R Marmeisse</name></author><author><name sortKey="Melayah, D" uniqKey="Melayah D">D Melayah</name></author><author><name sortKey="Montanini, B" uniqKey="Montanini B">B Montanini</name></author><author><name sortKey="Muratet, M" uniqKey="Muratet M">M Muratet</name></author><author><name sortKey="Nehls, U" uniqKey="Nehls U">U Nehls</name></author><author><name sortKey="Niculita Hirzel, H" uniqKey="Niculita Hirzel H">H Niculita-Hirzel</name></author><author><name sortKey="Oudot Le Secq, Mp" uniqKey="Oudot Le Secq M">MP Oudot-Le Secq</name></author><author><name sortKey="Peter, M" uniqKey="Peter M">M Peter</name></author><author><name sortKey="Quesneville, H" uniqKey="Quesneville H">H Quesneville</name></author><author><name sortKey="Rajashekar, B" uniqKey="Rajashekar B">B Rajashekar</name></author><author><name sortKey="Reich, M" uniqKey="Reich M">M Reich</name></author><author><name sortKey="Rouhier, N" uniqKey="Rouhier N">N Rouhier</name></author><author><name sortKey="Schmutz, J" uniqKey="Schmutz J">J Schmutz</name></author><author><name sortKey="Yin, T" uniqKey="Yin T">T Yin</name></author><author><name sortKey="Chalot, M" uniqKey="Chalot M">M Chalot</name></author><author><name sortKey="Henrissat, B" uniqKey="Henrissat B">B Henrissat</name></author><author><name sortKey="Kues, U" uniqKey="Kues U">U Kües</name></author><author><name sortKey="Lucas, S" uniqKey="Lucas S">S Lucas</name></author><author><name sortKey="Van De Peer, Y" uniqKey="Van De Peer Y">Y Van de Peer</name></author><author><name sortKey="Podila, Gk" uniqKey="Podila G">GK Podila</name></author><author><name sortKey="Polle, A" uniqKey="Polle A">A Polle</name></author><author><name sortKey="Pukkila, Pj" uniqKey="Pukkila P">PJ Pukkila</name></author><author><name sortKey="Richardson, Pm" uniqKey="Richardson P">PM Richardson</name></author><author><name sortKey="Rouze, P" uniqKey="Rouze P">P Rouzé</name></author><author><name sortKey="Sanders, Ir" uniqKey="Sanders I">IR Sanders</name></author><author><name sortKey="Stajich, Je" uniqKey="Stajich J">JE Stajich</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author><author><name sortKey="Tuskan, G" uniqKey="Tuskan G">G Tuskan</name></author><author><name sortKey="Grigoriev, Iv" uniqKey="Grigoriev I">IV Grigoriev</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Murat, C" uniqKey="Murat C">C Murat</name></author><author><name sortKey="Veneault Fourrey, C" uniqKey="Veneault Fourrey C">C Veneault-Fourrey</name></author><author><name sortKey="Hibbett, Ds" uniqKey="Hibbett D">DS Hibbett</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Murat, C" uniqKey="Murat C">C Murat</name></author><author><name sortKey="Balestrini, R" uniqKey="Balestrini R">R Balestrini</name></author><author><name sortKey="Coutinho, Pm" uniqKey="Coutinho P">PM Coutinho</name></author><author><name sortKey="Jaillon, O" uniqKey="Jaillon O">O Jaillon</name></author><author><name sortKey="Montanini, B" uniqKey="Montanini B">B Montanini</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Noel, B" uniqKey="Noel B">B Noel</name></author><author><name sortKey="Percudani, R" uniqKey="Percudani R">R Percudani</name></author><author><name sortKey="Porcel, B" uniqKey="Porcel B">B Porcel</name></author><author><name sortKey="Rubini, A" uniqKey="Rubini A">A Rubini</name></author><author><name sortKey="Amicucci, A" uniqKey="Amicucci A">A Amicucci</name></author><author><name sortKey="Amselem, J" uniqKey="Amselem J">J Amselem</name></author><author><name sortKey="Anthouard, V" uniqKey="Anthouard V">V Anthouard</name></author><author><name sortKey="Arcioni, S" uniqKey="Arcioni S">S Arcioni</name></author><author><name sortKey="Artiguenave, F" uniqKey="Artiguenave F">F Artiguenave</name></author><author><name sortKey="Aury, Jm" uniqKey="Aury J">JM Aury</name></author><author><name sortKey="Ballario, P" uniqKey="Ballario P">P Ballario</name></author><author><name sortKey="Bolchi, A" uniqKey="Bolchi A">A Bolchi</name></author><author><name sortKey="Brenna, A" uniqKey="Brenna A">A Brenna</name></author><author><name sortKey="Brun, A" uniqKey="Brun A">A Brun</name></author><author><name sortKey="Buee, M" uniqKey="Buee M">M Buée</name></author><author><name sortKey="Cantarel, B" uniqKey="Cantarel B">B Cantarel</name></author><author><name sortKey="Chevalier, G" uniqKey="Chevalier G">G Chevalier</name></author><author><name sortKey="Couloux, A" uniqKey="Couloux A">A Couloux</name></author><author><name sortKey="Da Silva, C" uniqKey="Da Silva C">C Da Silva</name></author><author><name sortKey="Denoeud, F" uniqKey="Denoeud F">F Denoeud</name></author><author><name sortKey="Duplessis, S" uniqKey="Duplessis S">S Duplessis</name></author><author><name sortKey="Ghignone, S" uniqKey="Ghignone S">S Ghignone</name></author><author><name sortKey="Hilselberger, B" uniqKey="Hilselberger B">B Hilselberger</name></author><author><name sortKey="Iotti, M" uniqKey="Iotti M">M Iotti</name></author><author><name sortKey="Marcais, B" uniqKey="Marcais B">B Marçais</name></author><author><name sortKey="Mello, A" uniqKey="Mello A">A Mello</name></author><author><name sortKey="Miranda, M" uniqKey="Miranda M">M Miranda</name></author><author><name sortKey="Pacioni, G" uniqKey="Pacioni G">G Pacioni</name></author><author><name sortKey="Quesneville, H" uniqKey="Quesneville H">H Quesneville</name></author><author><name sortKey="Riccioni, C" uniqKey="Riccioni C">C Riccioni</name></author><author><name sortKey="Ruotolo, R" uniqKey="Ruotolo R">R Ruotolo</name></author><author><name sortKey="Splivallo, R" uniqKey="Splivallo R">R Splivallo</name></author><author><name sortKey="Stocchi, V" uniqKey="Stocchi V">V Stocchi</name></author><author><name sortKey="Tisserant, E" uniqKey="Tisserant E">E Tisserant</name></author><author><name sortKey="Viscomi, Ar" uniqKey="Viscomi A">AR Viscomi</name></author><author><name sortKey="Zambonelli, A" uniqKey="Zambonelli A">A Zambonelli</name></author><author><name sortKey="Zampieri, E" uniqKey="Zampieri E">E Zampieri</name></author><author><name sortKey="Henrissat, B" uniqKey="Henrissat B">B Henrissat</name></author><author><name sortKey="Lebrun, Mh" uniqKey="Lebrun M">MH Lebrun</name></author><author><name sortKey="Paolocci, F" uniqKey="Paolocci F">F Paolocci</name></author><author><name sortKey="Bonfante, P" uniqKey="Bonfante P">P Bonfante</name></author><author><name sortKey="Ottonello, S" uniqKey="Ottonello S">S Ottonello</name></author><author><name sortKey="Wincker, P" uniqKey="Wincker P">P Wincker</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Massicotte, Hb" uniqKey="Massicotte H">HB Massicotte</name></author><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author><author><name sortKey="Ackerley, Ca" uniqKey="Ackerley C">CA Ackerley</name></author><author><name sortKey="Piche, Y" uniqKey="Piche Y">Y Piché</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Massicotte, Hb" uniqKey="Massicotte H">HB Massicotte</name></author><author><name sortKey="Melville, Lh" uniqKey="Melville L">LH Melville</name></author><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Massicotte, Hb" uniqKey="Massicotte H">HB Massicotte</name></author><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author><author><name sortKey="Ashford, Ae" uniqKey="Ashford A">AE Ashford</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Massicotte, Hb" uniqKey="Massicotte H">HB Massicotte</name></author><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author><author><name sortKey="Ackerley, Ca" uniqKey="Ackerley C">CA Ackerley</name></author><author><name sortKey="Ashford, Ae" uniqKey="Ashford A">AE Ashford</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Massicotte, Hb" uniqKey="Massicotte H">HB Massicotte</name></author><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author><author><name sortKey="Melville, Lh" uniqKey="Melville L">LH Melville</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Massicotte, Hb" uniqKey="Massicotte H">HB Massicotte</name></author><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author><author><name sortKey="Ackerley, Ca" uniqKey="Ackerley C">CA Ackerley</name></author><author><name sortKey="Melville, Lh" uniqKey="Melville L">LH Melville</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mehrabi, R" uniqKey="Mehrabi R">R Mehrabi</name></author><author><name sortKey="Ding, S" uniqKey="Ding S">S Ding</name></author><author><name sortKey="Xu, Jr" uniqKey="Xu J">JR Xu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Montanini, B" uniqKey="Montanini B">B Montanini</name></author><author><name sortKey="Levati, E" uniqKey="Levati E">E Levati</name></author><author><name sortKey="Bolchi, A" uniqKey="Bolchi A">A Bolchi</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Tisserant, E" uniqKey="Tisserant E">E Tisserant</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Ottonello, S" uniqKey="Ottonello S">S Ottonello</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nylund, Je" uniqKey="Nylund J">JE Nylund</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Olsen, An" uniqKey="Olsen A">AN Olsen</name></author><author><name sortKey="Ernst, Ha" uniqKey="Ernst H">HA Ernst</name></author><author><name sortKey="Leggio, Ll" uniqKey="Leggio L">LL Leggio</name></author><author><name sortKey="Skriver, K" uniqKey="Skriver K">K Skriver</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ohm, Ra" uniqKey="Ohm R">RA Ohm</name></author><author><name sortKey="De Jong, Jf" uniqKey="De Jong J">JF de Jong</name></author><author><name sortKey="De Bekker, C" uniqKey="De Bekker C">C de Bekker</name></author><author><name sortKey="Wosten, Ha" uniqKey="Wosten H">HA Wosten</name></author><author><name sortKey="Lugones, Lg" uniqKey="Lugones L">LG Lugones</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Peter, M" uniqKey="Peter M">M Peter</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Ohm, Ra" uniqKey="Ohm R">RA Ohm</name></author><author><name sortKey="Kuo, A" uniqKey="Kuo A">A Kuo</name></author><author><name sortKey="Krutzmann, J" uniqKey="Krutzmann J">J Krützmann</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Arend, M" uniqKey="Arend M">M Arend</name></author><author><name sortKey="Barry, Kw" uniqKey="Barry K">KW Barry</name></author><author><name sortKey="Binder, M" uniqKey="Binder M">M Binder</name></author><author><name sortKey="Choi, C" uniqKey="Choi C">C Choi</name></author><author><name sortKey="Clum, A" uniqKey="Clum A">A Clum</name></author><author><name sortKey="Copeland, A" uniqKey="Copeland A">A Copeland</name></author><author><name sortKey="Grisel, N" uniqKey="Grisel N">N Grisel</name></author><author><name sortKey="Haridas, S" uniqKey="Haridas S">S Haridas</name></author><author><name sortKey="Kipfer, T" uniqKey="Kipfer T">T Kipfer</name></author><author><name sortKey="Labutti, K" uniqKey="Labutti K">K LaButti</name></author><author><name sortKey="Lindquist, E" uniqKey="Lindquist E">E Lindquist</name></author><author><name sortKey="Lipzen, A" uniqKey="Lipzen A">A Lipzen</name></author><author><name sortKey="Maire, R" uniqKey="Maire R">R Maire</name></author><author><name sortKey="Meier, B" uniqKey="Meier B">B Meier</name></author><author><name sortKey="Mihaltcheva, S" uniqKey="Mihaltcheva S">S Mihaltcheva</name></author><author><name sortKey="Molinier, V" uniqKey="Molinier V">V Molinier</name></author><author><name sortKey="Murat, C" uniqKey="Murat C">C Murat</name></author><author><name sortKey="Poggeler, S" uniqKey="Poggeler S">S Pöggeler</name></author><author><name sortKey="Quandt, Ca" uniqKey="Quandt C">CA Quandt</name></author><author><name sortKey="Sperisen, C" uniqKey="Sperisen C">C Sperisen</name></author><author><name sortKey="Tritt, A" uniqKey="Tritt A">A Tritt</name></author><author><name sortKey="Tisserant, E" uniqKey="Tisserant E">E Tisserant</name></author><author><name sortKey="Crous, Pw" uniqKey="Crous P">PW Crous</name></author><author><name sortKey="Henrissat, B" uniqKey="Henrissat B">B Henrissat</name></author><author><name sortKey="Nehls, U" uniqKey="Nehls U">U Nehls</name></author><author><name sortKey="Egli, S" uniqKey="Egli S">S Egli</name></author><author><name sortKey="Spatafora, Jw" uniqKey="Spatafora J">JW Spatafora</name></author><author><name sortKey="Grigoriev, Iv" uniqKey="Grigoriev I">IV Grigoriev</name></author><author><name sortKey="Martin, Fm" uniqKey="Martin F">FM Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Peterson, Rl" uniqKey="Peterson R">RL Peterson</name></author><author><name sortKey="Bonfante, P" uniqKey="Bonfante P">P Bonfante</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pfaffl, Mw" uniqKey="Pfaffl M">MW Pfaffl</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plett, Jm" uniqKey="Plett J">JM Plett</name></author><author><name sortKey="Daguerre, Y" uniqKey="Daguerre Y">Y Daguerre</name></author><author><name sortKey="Wittulsky, S" uniqKey="Wittulsky S">S Wittulsky</name></author><author><name sortKey="Vayssieres, A" uniqKey="Vayssieres A">A Vayssières</name></author><author><name sortKey="Deveau, A" uniqKey="Deveau A">A Deveau</name></author><author><name sortKey="Melton, Sj" uniqKey="Melton S">SJ Melton</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Morrell Falvey, Jl" uniqKey="Morrell Falvey J">JL Morrell-Falvey</name></author><author><name sortKey="Brun, A" uniqKey="Brun A">A Brun</name></author><author><name sortKey="Veneault Fourrey, C" uniqKey="Veneault Fourrey C">C Veneault-Fourrey</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plett, Jm" uniqKey="Plett J">JM Plett</name></author><author><name sortKey="Gibon, J" uniqKey="Gibon J">J Gibon</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Duffy, K" uniqKey="Duffy K">K Duffy</name></author><author><name sortKey="Hoegger, Pj" uniqKey="Hoegger P">PJ Hoegger</name></author><author><name sortKey="Velagapudi, R" uniqKey="Velagapudi R">R Velagapudi</name></author><author><name sortKey="Han, J" uniqKey="Han J">J Han</name></author><author><name sortKey="Kues, U" uniqKey="Kues U">U Kües</name></author><author><name sortKey="Grigoriev, Iv" uniqKey="Grigoriev I">IV Grigoriev</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plett, Jm" uniqKey="Plett J">JM Plett</name></author><author><name sortKey="Kemppainen, M" uniqKey="Kemppainen M">M Kemppainen</name></author><author><name sortKey="Kale, Sd" uniqKey="Kale S">SD Kale</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Legue, V" uniqKey="Legue V">V Legué</name></author><author><name sortKey="Brun, A" uniqKey="Brun A">A Brun</name></author><author><name sortKey="Tyler, Bm" uniqKey="Tyler B">BM Tyler</name></author><author><name sortKey="Pardo, Ag" uniqKey="Pardo A">AG Pardo</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plett, Jm" uniqKey="Plett J">JM Plett</name></author><author><name sortKey="Montanini, B" uniqKey="Montanini B">B Montanini</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Ottonello, S" uniqKey="Ottonello S">S Ottonello</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plett, Jm" uniqKey="Plett J">JM Plett</name></author><author><name sortKey="Tisserant, E" uniqKey="Tisserant E">E Tisserant</name></author><author><name sortKey="Brun, A" uniqKey="Brun A">A Brun</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Grigoriev, Iv" uniqKey="Grigoriev I">IV Grigoriev</name></author><author><name sortKey="Kuo, A" uniqKey="Kuo A">A Kuo</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Read, Dj" uniqKey="Read D">DJ Read</name></author><author><name sortKey="Perez Moreno, J" uniqKey="Perez Moreno J">J Perez-Moreno</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Rocha, Mc" uniqKey="Rocha M">MC Rocha</name></author><author><name sortKey="Fabri, Jh" uniqKey="Fabri J">JH Fabri</name></author><author><name sortKey="Franco De Godoy, K" uniqKey="Franco De Godoy K">K Franco de Godoy</name></author><author><name sortKey="Alves De Castro, P" uniqKey="Alves De Castro P">P Alves de Castro</name></author><author><name sortKey="Hori, Ji" uniqKey="Hori J">JI Hori</name></author><author><name sortKey="Ferreira Da Cunha, A" uniqKey="Ferreira Da Cunha A">A Ferreira da Cunha</name></author><author><name sortKey="Arentshorst, M" uniqKey="Arentshorst M">M Arentshorst</name></author><author><name sortKey="Ram, Af" uniqKey="Ram A">AF Ram</name></author><author><name sortKey="Van Den Hondel, Ca" uniqKey="Van Den Hondel C">CA van den Hondel</name></author><author><name sortKey="Goldman, Gh" uniqKey="Goldman G">GH Goldman</name></author><author><name sortKey="Malavazi, I" uniqKey="Malavazi I">I Malavazi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shi, Y" uniqKey="Shi Y">Y Shi</name></author><author><name sortKey="Shi, Y" uniqKey="Shi Y">Y Shi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shin, Ks" uniqKey="Shin K">KS Shin</name></author><author><name sortKey="Kim, Yh" uniqKey="Kim Y">YH Kim</name></author><author><name sortKey="Yu, Jh" uniqKey="Yu J">JH Yu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Smith, Se" uniqKey="Smith S">SE Smith</name></author><author><name sortKey="Read, Dj" uniqKey="Read D">DJ Read</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stajich, Je" uniqKey="Stajich J">JE Stajich</name></author><author><name sortKey="Wilke, Sk" uniqKey="Wilke S">SK Wilke</name></author><author><name sortKey="Ahren, D" uniqKey="Ahren D">D Ahrén</name></author><author><name sortKey="Au, Ch" uniqKey="Au C">CH Au</name></author><author><name sortKey="Birren, Bw" uniqKey="Birren B">BW Birren</name></author><author><name sortKey="Borodovsky, M" uniqKey="Borodovsky M">M Borodovsky</name></author><author><name sortKey="Burns, C" uniqKey="Burns C">C Burns</name></author><author><name sortKey="Canb Ck, B" uniqKey="Canb Ck B">B Canbäck</name></author><author><name sortKey="Casselton, La" uniqKey="Casselton L">LA Casselton</name></author><author><name sortKey="Cheng, Ck" uniqKey="Cheng C">CK Cheng</name></author><author><name sortKey="Deng, J" uniqKey="Deng J">J Deng</name></author><author><name sortKey="Dietrich, Fs" uniqKey="Dietrich F">FS Dietrich</name></author><author><name sortKey="Fargo, Dc" uniqKey="Fargo D">DC Fargo</name></author><author><name sortKey="Farman, Ml" uniqKey="Farman M">ML Farman</name></author><author><name sortKey="Gathman, Ac" uniqKey="Gathman A">AC Gathman</name></author><author><name sortKey="Goldberg, J" uniqKey="Goldberg J">J Goldberg</name></author><author><name sortKey="Guig, R" uniqKey="Guig R">R Guigó</name></author><author><name sortKey="Hoegger, Pj" uniqKey="Hoegger P">PJ Hoegger</name></author><author><name sortKey="Hooker, Jb" uniqKey="Hooker J">JB Hooker</name></author><author><name sortKey="Huggins, A" uniqKey="Huggins A">A Huggins</name></author><author><name sortKey="James, Ty" uniqKey="James T">TY James</name></author><author><name sortKey="Kamada, T" uniqKey="Kamada T">T Kamada</name></author><author><name sortKey="Kilaru, S" uniqKey="Kilaru S">S Kilaru</name></author><author><name sortKey="Kodira, C" uniqKey="Kodira C">C Kodira</name></author><author><name sortKey="Kues, U" uniqKey="Kues U">U Kües</name></author><author><name sortKey="Kupfer, D" uniqKey="Kupfer D">D Kupfer</name></author><author><name sortKey="Kwan, Hs" uniqKey="Kwan H">HS Kwan</name></author><author><name sortKey="Lomsadze, A" uniqKey="Lomsadze A">A Lomsadze</name></author><author><name sortKey="Li, W" uniqKey="Li W">W Li</name></author><author><name sortKey="Lilly, Ww" uniqKey="Lilly W">WW Lilly</name></author><author><name sortKey="Ma, Lj" uniqKey="Ma L">LJ Ma</name></author><author><name sortKey="Mackey, Aj" uniqKey="Mackey A">AJ Mackey</name></author><author><name sortKey="Manning, G" uniqKey="Manning G">G Manning</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Muraguchi, H" uniqKey="Muraguchi H">H Muraguchi</name></author><author><name sortKey="Natvig, Do" uniqKey="Natvig D">DO Natvig</name></author><author><name sortKey="Palmerini, H" uniqKey="Palmerini H">H Palmerini</name></author><author><name sortKey="Ramesh, Ma" uniqKey="Ramesh M">MA Ramesh</name></author><author><name sortKey="Rehmeyer, Cj" uniqKey="Rehmeyer C">CJ Rehmeyer</name></author><author><name sortKey="Roe, Ba" uniqKey="Roe B">BA Roe</name></author><author><name sortKey="Shenoy, N" uniqKey="Shenoy N">N Shenoy</name></author><author><name sortKey="Stanke, M" uniqKey="Stanke M">M Stanke</name></author><author><name sortKey="Ter Hovhannisyan, V" uniqKey="Ter Hovhannisyan V">V Ter-Hovhannisyan</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author><author><name sortKey="Velagapudi, R" uniqKey="Velagapudi R">R Velagapudi</name></author><author><name sortKey="Vision, Tj" uniqKey="Vision T">TJ Vision</name></author><author><name sortKey="Zeng, Q" uniqKey="Zeng Q">Q Zeng</name></author><author><name sortKey="Zolan, Me" uniqKey="Zolan M">ME Zolan</name></author><author><name sortKey="Pukkila, Pj" uniqKey="Pukkila P">PJ Pukkila</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stegmaier, P" uniqKey="Stegmaier P">P Stegmaier</name></author><author><name sortKey="Kel, Ae" uniqKey="Kel A">AE Kel</name></author><author><name sortKey="Wingender, E" uniqKey="Wingender E">E Wingender</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stracke, R" uniqKey="Stracke R">R Stracke</name></author><author><name sortKey="Werber, M" uniqKey="Werber M">M Werber</name></author><author><name sortKey="Weisshaar, B" uniqKey="Weisshaar B">B Weisshaar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Titz, B" uniqKey="Titz B">B Titz</name></author><author><name sortKey="Thomas, S" uniqKey="Thomas S">S Thomas</name></author><author><name sortKey="Rajagopala, Sv" uniqKey="Rajagopala S">SV Rajagopala</name></author><author><name sortKey="Chiba, T" uniqKey="Chiba T">T Chiba</name></author><author><name sortKey="Ito, T" uniqKey="Ito T">T Ito</name></author><author><name sortKey="Uetz, P" uniqKey="Uetz P">P Uetz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Todd, Rb" uniqKey="Todd R">RB Todd</name></author><author><name sortKey="Murphy, Rl" uniqKey="Murphy R">RL Murphy</name></author><author><name sortKey="Martin, Hm" uniqKey="Martin H">HM Martin</name></author><author><name sortKey="Sharp, Ja" uniqKey="Sharp J">JA Sharp</name></author><author><name sortKey="Davis, Ma" uniqKey="Davis M">MA Davis</name></author><author><name sortKey="Katz, Me" uniqKey="Katz M">ME Katz</name></author><author><name sortKey="Hynes, Mj" uniqKey="Hynes M">MJ Hynes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Todd, Rb" uniqKey="Todd R">RB Todd</name></author><author><name sortKey="Zhou, M" uniqKey="Zhou M">M Zhou</name></author><author><name sortKey="Ohm, Ra" uniqKey="Ohm R">RA Ohm</name></author><author><name sortKey="Leeggangers, Ha" uniqKey="Leeggangers H">HA Leeggangers</name></author><author><name sortKey="Visser, L" uniqKey="Visser L">L Visser</name></author><author><name sortKey="De Vries, Rp" uniqKey="De Vries R">RP de Vries</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tripathi, G" uniqKey="Tripathi G">G Tripathi</name></author><author><name sortKey="Wiltshire, C" uniqKey="Wiltshire C">C Wiltshire</name></author><author><name sortKey="Macaskill, S" uniqKey="Macaskill S">S Macaskill</name></author><author><name sortKey="Tournu, H" uniqKey="Tournu H">H Tournu</name></author><author><name sortKey="Budge, S" uniqKey="Budge S">S Budge</name></author><author><name sortKey="Brown, Ajp" uniqKey="Brown A">AJP Brown</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Van Der Heijden, Mg" uniqKey="Van Der Heijden M">MG van der Heijden</name></author><author><name sortKey="Martin, Fm" uniqKey="Martin F">FM Martin</name></author><author><name sortKey="Selosse, Ma" uniqKey="Selosse M">MA Selosse</name></author><author><name sortKey="Sanders, Ir" uniqKey="Sanders I">IR Sanders</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vayssieres, A" uniqKey="Vayssieres A">A Vayssières</name></author><author><name sortKey="P N K, A" uniqKey="P N K A">A Pěnčík</name></author><author><name sortKey="Felten, J" uniqKey="Felten J">J Felten</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Ljung, K" uniqKey="Ljung K">K Ljung</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author><author><name sortKey="Legue, V" uniqKey="Legue V">V Legué</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Veneault Fourrey, C" uniqKey="Veneault Fourrey C">C Veneault-Fourrey</name></author><author><name sortKey="Commun, C" uniqKey="Commun C">C Commun</name></author><author><name sortKey="Kohler, A" uniqKey="Kohler A">A Kohler</name></author><author><name sortKey="Morin, E" uniqKey="Morin E">E Morin</name></author><author><name sortKey="Balestrini, R" uniqKey="Balestrini R">R Balestrini</name></author><author><name sortKey="Plett, J" uniqKey="Plett J">J Plett</name></author><author><name sortKey="Danchin, E" uniqKey="Danchin E">E Danchin</name></author><author><name sortKey="Coutinho, P" uniqKey="Coutinho P">P Coutinho</name></author><author><name sortKey="Wiebenga, A" uniqKey="Wiebenga A">A Wiebenga</name></author><author><name sortKey="De Vries, Rp" uniqKey="De Vries R">RP de Vries</name></author><author><name sortKey="Henrissat, B" uniqKey="Henrissat B">B Henrissat</name></author><author><name sortKey="Martin, F" uniqKey="Martin F">F Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Watanabe, Y" uniqKey="Watanabe Y">Y Watanabe</name></author><author><name sortKey="Irie, K" uniqKey="Irie K">K Irie</name></author><author><name sortKey="Matsumoto, K" uniqKey="Matsumoto K">K Matsumoto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wong Sak Hoi, J" uniqKey="Wong Sak Hoi J">J Wong Sak Hoi</name></author><author><name sortKey="Dumas, B" uniqKey="Dumas B">B Dumas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wright, Dp" uniqKey="Wright D">DP Wright</name></author><author><name sortKey="Johansson, T" uniqKey="Johansson T">T Johansson</name></author><author><name sortKey="Le Quere, A" uniqKey="Le Quere A">A Le Quere</name></author><author><name sortKey="Soderstrom, B" uniqKey="Soderstrom B">B Söderström</name></author><author><name sortKey="Tunlid, A" uniqKey="Tunlid A">A Tunlid</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhang, Z" uniqKey="Zhang Z">Z Zhang</name></author><author><name sortKey="Li, H" uniqKey="Li H">H Li</name></author><author><name sortKey="Qin, G" uniqKey="Qin G">G Qin</name></author><author><name sortKey="He, C" uniqKey="He C">C He</name></author><author><name sortKey="Li, B" uniqKey="Li B">B Li</name></author><author><name sortKey="Tian, S" uniqKey="Tian S">S Tian</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Genomics</journal-id><journal-id journal-id-type="iso-abbrev">BMC Genomics</journal-id><journal-title-group><journal-title>BMC Genomics</journal-title></journal-title-group><issn pub-type="epub">1471-2164</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28923004</article-id><article-id pub-id-type="pmc">5604158</article-id><article-id pub-id-type="publisher-id">4114</article-id><article-id pub-id-type="doi">10.1186/s12864-017-4114-7</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus <italic>Laccaria bicolor</italic></article-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Daguerre</surname><given-names>Y.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Levati</surname><given-names>E.</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Ruytinx</surname><given-names>J.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Tisserant</surname><given-names>E.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Morin</surname><given-names>E.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Kohler</surname><given-names>A.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Montanini</surname><given-names>B.</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Ottonello</surname><given-names>S.</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Brun</surname><given-names>A.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" corresp="yes" equal-contrib="yes"><name><surname>Veneault-Fourrey</surname><given-names>C.</given-names></name><address><email>claire.fourrey@univ-lorraine.fr</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Martin</surname><given-names>F.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>54280 Champenoux, France</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2194 6418</institution-id><institution-id institution-id-type="GRID">grid.29172.3f</institution-id><institution>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE,</institution></institution-wrap>F-54500 Vandoeuvre-lès-, Nancy, France</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1758 0937</institution-id><institution-id institution-id-type="GRID">grid.10383.39</institution-id><institution>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale,</institution><institution>Università degli Studi di Parma,</institution></institution-wrap>Parco Area delle Scienze 23/A, 43124 Parma, Italy</aff><aff id="Aff4"><label>4</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8578 2742</institution-id><institution-id institution-id-type="GRID">grid.6341.0</institution-id><institution>Present address: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology,</institution><institution>Swedish University of Agricultural Sciences,</institution></institution-wrap>901 83, Umea, Sweden</aff><aff id="Aff5"><label>5</label>Present address: Hasselt University, Centre for Environmental Sciences, Agoralaan building D, 3590 Diepenbeek, Belgium</aff></contrib-group><pub-date pub-type="epub"><day>18</day><month>9</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>18</day><month>9</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>18</volume><elocation-id>737</elocation-id><history><date date-type="received"><day>10</day><month>4</month><year>2017</year></date><date date-type="accepted"><day>4</day><month>9</month><year>2017</year></date></history><permissions><copyright-statement>© The Author(s). 2017</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p id="Par1">Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus <italic>Laccaria bicolor</italic>.</p></sec><sec><title>Results</title><p id="Par2">We curated the <italic>L. bicolor</italic> gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The <italic>L. bicolor</italic> core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of <italic>L. bicolor</italic> and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs).</p></sec><sec><title>Conclusions</title><p id="Par3">Transcriptional regulators required for ECM symbiosis development in <italic>L. bicolor</italic> have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (10.1186/s12864-017-4114-7) contains supplementary material, which is available to authorized users.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Transcription factors</kwd><kwd>symbiosis</kwd><kwd>secreted proteins</kwd><kwd>transcriptional activator trap assay</kwd><kwd>yeast</kwd><kwd>transcriptome</kwd><kwd>ectomycorrhiza development</kwd></kwd-group><funding-group><award-group><funding-source><institution>French Ministère de la Recherche et de la Technologie</institution></funding-source></award-group><award-group><funding-source><institution>AgreenSkills Marie Sklodowska Curie postdoctoral fellow </institution></funding-source><award-id>FP7-267196</award-id></award-group><award-group><funding-source><institution>LABEX ARBRE</institution></funding-source><award-id>ANR-12-LABX-0002_ARBRE</award-id></award-group><award-group><funding-source><institution>the Oak Ridge National Laboratory Genomic Science Program, U.S. Department of Energy, Office of Science – Biological and Environmental Research as part of the Plant Microbe Interfaces Scientific Focus Area </institution></funding-source></award-group><award-group><funding-source><institution>Italian Interuniversity Consortium for Biotechnologies </institution></funding-source></award-group><award-group><funding-source><institution>University of Parma (local funding, FIL program)</institution></funding-source></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2017</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Background</title><p id="Par9">Ectomycorrhizae (ECM) are symbiotic interactions between plant roots and ectomycorrhizal fungi. The plant provides the fungus with photosynthetic sugars and the fungal symbiont gives back low bio-available mineral elements in forest soils for plants, such as nitrogen and phosphorus [<xref ref-type="bibr" rid="CR36">36</xref>, <xref ref-type="bibr" rid="CR61">61</xref>]. Thus, mycorrhizae are crucial for the growth and health of trees in forest ecosystems. The ability to form mutualistic relationships with ECM fungi is restricted to approximately 20,000 plant species, but the ecological and economical importance of these plants is amplified by their widespread occupancy of terrestrial ecosystems [<xref ref-type="bibr" rid="CR5">5</xref>, <xref ref-type="bibr" rid="CR56">56</xref>, <xref ref-type="bibr" rid="CR69">69</xref>]. The ECM fungal colony in forest soils is comprised of three main morphological and functional structures: (i) the extramatrical hyphae, so-called free living mycelia (FLM), prospecting the soil for nutrients and receptive host roots, (ii) the symbiotic ECM root tips and (iii) the fruiting body (FB) [<xref ref-type="bibr" rid="CR34">34</xref>, <xref ref-type="bibr" rid="CR61">61</xref>]. ECM root tips are characterized by the presence of three fungal structural components: (i) a mantle of aggregated hyphae ensheathing the rootlets, (ii) a network of coenocytic hyphae (called the Hartig net) penetrating between epidermal and cortical cells, and (iii) a web of extraradical hyphae which forms an essential connection between the colonized root and soil hyphae prospecting the soil for nutrients and with the hyphae forming the fruiting body [<xref ref-type="bibr" rid="CR37">37</xref>–<xref ref-type="bibr" rid="CR42">42</xref>, <xref ref-type="bibr" rid="CR49">49</xref>, <xref ref-type="bibr" rid="CR61">61</xref>]. Fungal colonization leads to striking morphological changes in the plant host roots. The root system in contact with ECM hyphae displays an increased number of lateral roots, a more pronounced elongation of epidermal cells and an arrest of meristematic growth [<xref ref-type="bibr" rid="CR6">6</xref>, <xref ref-type="bibr" rid="CR15">15</xref>, <xref ref-type="bibr" rid="CR16">16</xref>, <xref ref-type="bibr" rid="CR70">70</xref>]. ECM ontogenesis is also accompanied by significant alterations of the host plant defense system. In contrast with pathogenic fungi that generally induce strong host defense responses, ECM fungi are able to colonize their hosts while inducing only weak and transient defense reactions. Indeed, plant genes involved in defense responses are upregulated during mantle and Hartig net formation but are repressed at later stages of ECM development as observed in the ECM associations <italic>Paxillus involutus</italic>-<italic>Betula pendula</italic>, <italic>Pisolithus microcarpus</italic>-<italic>Eucalyptus globulus</italic> and <italic>Laccaria bicolor-Populus</italic> [<xref ref-type="bibr" rid="CR14">14</xref>, <xref ref-type="bibr" rid="CR23">23</xref>, <xref ref-type="bibr" rid="CR28">28</xref>, <xref ref-type="bibr" rid="CR29">29</xref>, <xref ref-type="bibr" rid="CR33">33</xref>, <xref ref-type="bibr" rid="CR74">74</xref>]. The early stages of ECM development are characterized by the up-regulation of fungal genes involved in cell wall adhesion (e.g., hydrophobins) [<xref ref-type="bibr" rid="CR52">52</xref>, <xref ref-type="bibr" rid="CR57">57</xref>] and remodeling (e.g. polygalacturonases and endo glucanases) [<xref ref-type="bibr" rid="CR71">71</xref>] as well as signaling such as Mycorrhiza-induced Small Secreted Proteins (MiSSPs) [<xref ref-type="bibr" rid="CR26">26</xref>, <xref ref-type="bibr" rid="CR33">33</xref>, <xref ref-type="bibr" rid="CR34">34</xref>, <xref ref-type="bibr" rid="CR48">48</xref>]. Among these MiSSPs, the <italic>L. bicolor</italic> 7 kDa MiSSP (MiSSP7) is a symbiotic effector required for controlling the plant jasmonate-signaling pathway, a pre-requisite for fungal colonization [<xref ref-type="bibr" rid="CR51">51</xref>]. The later stages of ECM development are characterized by the up-regulation of genes involved in carbon and nitrogen metabolism, as well as in mitochondrial respiration [<xref ref-type="bibr" rid="CR11">11</xref>, <xref ref-type="bibr" rid="CR12">12</xref>, <xref ref-type="bibr" rid="CR14">14</xref>, <xref ref-type="bibr" rid="CR28">28</xref>, <xref ref-type="bibr" rid="CR29">29</xref>, <xref ref-type="bibr" rid="CR33">33</xref>]. All together, symbiosis development leads to a substantial and coordinated transcriptional reprogramming in both partners [<xref ref-type="bibr" rid="CR34">34</xref>]. However, the regulatory mechanisms triggering and controlling the expression of fungal and plant signaling genes and the developmental pathways leading to ECM symbiosis are largely unknown.</p><p id="Par10">Transcription factors (TF) are master regulators of gene expression. Positively acting TFs, known as “activators”, generally consist of at least one DNA-binding domain (DBD) and one activation-domain (AD). DBD recognizes and binds sequence-specific DNA elements in the promoter region of target genes whether AD recruits and interacts with the transcriptional machinery. TFs are classified into several families based on conserved folds and structures within their DBDs. ADs, instead, are structurally quite variable and this lack of conservation complicates their bioinformatic identification/prediction [<xref ref-type="bibr" rid="CR63">63</xref>]. To date, only a single study has addressed the genome-wide profiling of TFs in an ECM fungus [<xref ref-type="bibr" rid="CR44">44</xref>]. Focusing on the ECM symbiosis between the ascomycete <italic>Tuber melanosporum</italic> and hazelnut (<italic>Corylus avellana</italic>), this study identified multiple mycorrhiza-regulated TFs associated with root cell wall remodeling and fatty acid metabolism. In particular, two orthologs of the <italic>XlnR</italic> activator of genes involved in cellulose and xylan degradation were found to be dramatically upregulated in ECM [<xref ref-type="bibr" rid="CR44">44</xref>].</p><p id="Par11">The aim of the present work was to identify, classify and functionally characterize from a regulatory point of view potential regulators of symbiosis development within the TF repertoire of <italic>L. bicolor</italic>. Combined genomic and transcriptomic analyses provided a comprehensive view of the <italic>L. bicolor</italic> TF repertoire and its regulation during mycorrhizal development. A transcriptional activator trap (TAT) assay, performed in the yeast <italic>Saccharomyces cerevisiae</italic> [<xref ref-type="bibr" rid="CR31">31</xref>, <xref ref-type="bibr" rid="CR44">44</xref>, <xref ref-type="bibr" rid="CR65">65</xref>], was used to functionally validate in silico and gene expression data.</p></sec><sec id="Sec2"><title>Results</title><sec id="Sec3"><title>Comparative analysis of <italic>L. bicolor</italic> repertoire of predicted TFs</title><p id="Par12">We curated 285 TFs derived from the <italic>L. bicolor</italic> gene catalogue v2.0. As revealed by a DBD-based classification, putative <italic>Laccaria</italic> TFs belong to 28 different classes (Additional file <xref rid="MOESM1" ref-type="media">1</xref>: Table S1)<italic>.</italic> This <italic>in silico</italic> generated TF repertoire was compared with the corresponding repertoires of 70 saprotrophic, endophytic, mycorrhizal and pathogenic fungi of diverse clades (Ascomycota and Basidiomycota) [<xref ref-type="bibr" rid="CR26">26</xref>]. The overall distribution within known TF families is highly similar for the TF repertoires of these fungi and apparently not related to their different lifestyles. Amongst the examined fungi, the three most prevalent TF families are those containing the C2H2 Zinc-finger (PF00096), the Zn2/Cys6 Zinc-cluster (PF00172) and the fungal-specific TF (PF04280) domains (Fig. <xref rid="Fig1" ref-type="fig">1</xref>, Additional file <xref rid="MOESM2" ref-type="media">2</xref>: Table S2). The number of Zn-cluster and fungal-specific TFs was higher in Ascomycota compared to Basidiomycota. For example, although the predicted proteomes of the ericoid Ascomycete <italic>Meliniomyces variabilis</italic> and the ECM Basidiomycete <italic>Cortinarius glaucopus</italic> are similarly sized (20,389 and 20,377 predicted proteins each), they encode, respectively, 554 and 61 Zn-cluster TFs. In general, Zn-cluster TFs appear to be more represented than Zn-finger TFs in Ascomycota (Fig. <xref rid="Fig1" ref-type="fig">1</xref> and Additional file <xref rid="MOESM2" ref-type="media">2</xref>: Table S2), whereas a slight prevalence of the homeobox, GATA, Heat Stress TF (HSF) and High Mobility Group (HMG)-box TF families is observed in Basidiomycota compared to Ascomycota. For instance, eight GATA TFs are encoded by the genome of <italic>M. variabilis</italic>, whereas 13 GATA TF genes are present in the genome of <italic>C. glaucopus</italic> (Fig. <xref rid="Fig1" ref-type="fig">1</xref> and Additional file <xref rid="MOESM2" ref-type="media">2</xref>: Table S2).<fig id="Fig1"><label>Fig. 1</label><caption><p>Distribution of TFs in different families in 70 fungal genomes. The heatmap represents the abundance on each TF family in each genome. Abundance levels range from pale to saturated colour (black for absence, yellow for low abundance, red for high abundance). ECM: ectomycorrhiza; ERM: ericoid mycorrhiza; ORM: orchid mycorrhiza</p></caption><graphic xlink:href="12864_2017_4114_Fig1_HTML" id="MO1"></graphic></fig></p><p id="Par13">One hundred eighty three of the 285 predicted <italic>Laccaria</italic> TFs displayed similarities with characterized fungal TFs (Additional file <xref rid="MOESM1" ref-type="media">1</xref>: Table S1 lines 5 to 187). Among them, 91 were identified as orthologs of known fungal transcription factors by a BLASTP search conducted against the non-redundant GenBank database, using reciprocal BLAST to infer orthologous relationships (Table <xref rid="Tab1" ref-type="table">1</xref>). These TFs were classified into different functional categories (e.g. cell wall modification, development, cell cycle, metabolism, or response to stress and stimuli) based on the putative or known function(s) of their orthologs (Table <xref rid="Tab1" ref-type="table">1</xref>). Eight additional orthologs of known fungal TFs were retrieved from a BLASTP search using DBD-lacking regulatory proteins as a reference (Additional file <xref rid="MOESM1" ref-type="media">1</xref>: Table S1 lines 284 to 291); 94 predicted <italic>L. bicolor</italic> TFs displayed no similarity to any known fungal transcription factor (Additional file <xref rid="MOESM1" ref-type="media">1</xref>: Table S1 lines 189 to 282).<table-wrap id="Tab1"><label>Table 1</label><caption><p>List of putative transcription factors in <italic>Laccaria bicolor</italic> genome</p></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="2">Protein ID gene names and functional classes<sup>a,b</sup></th><th>Putative gene product function<sup>c</sup></th></tr></thead><tbody><tr><td colspan="3">Cell wall</td></tr><tr><td> 247,901</td><td>LbACE1–1</td><td>Repressor of plant cell wall-degrading enzymes</td></tr><tr><td> 622,364</td><td>LbACE1–2</td><td>Repressor of plant cell wall-degrading enzymes</td></tr><tr><td> 293,207</td><td>LbRlm1–1</td><td>Maintenance of cell wall integrity</td></tr><tr><td> 302,141</td><td>LbRlm1–2</td><td>Maintenance of cell wall integrity</td></tr><tr><td colspan="3">Development</td></tr><tr><td colspan="3">
<italic>Sexual development and fruiting body formation</italic></td></tr><tr><td>
<bold>393,192</bold></td><td><bold>LbSte12α</bold></td><td><bold>Regulator of fruiting body development</bold></td></tr><tr><td> 522,619</td><td>LbMcm1</td><td>Regulator of pheromone response</td></tr><tr><td> 668,161</td><td>LbNosA</td><td>Number of sexual spores, regulator of sexual development</td></tr><tr><td> 301,103</td><td>LbHD1</td><td>Mating-type protein</td></tr><tr><td> 379,291</td><td>LbHD2</td><td>Mating-type protein</td></tr><tr><td> 324,166</td><td>LbHom1–1</td><td>Regulator of fruiting body development; Involved in mushroom tissue formation</td></tr><tr><td> 399,669</td><td>LbHom1–2</td><td>Regulator of fruiting body development; Involved in mushroom tissue formation</td></tr><tr><td> 293,988</td><td>LbHom2</td><td>Regulator of fruiting body development; Regulation of the formation of the auto-inhibitor and of dikaryon-specific hydrophobins</td></tr><tr><td> 487,295</td><td>LbC2h2</td><td>Regulator of fruiting body development; Involved in primordia formation</td></tr><tr><td> 585,149</td><td>LbFst3</td><td>Negative regulator of fruiting body development; Inhibits the formation of clusters of mushrooms</td></tr><tr><td> 585,421</td><td>LbNsdD</td><td>Regulator of sexual development</td></tr><tr><td> 644,689</td><td>LbExp1</td><td>Regulator of the final phase of fruiting-body morphogenesis</td></tr><tr><td> 308,722</td><td>LbFst4</td><td>Positive regulator of fruiting body development; Involves in the switch between the vegetative and the reproductive phase and in aggregate formation</td></tr><tr><td> 685,209</td><td>LbGat1</td><td>Regulator of fruiting body development; Involved in mushroom tissue formation</td></tr><tr><td> 300,824</td><td>LbItc1</td><td>Subunit of ATP-dependent Isw2p-Itc1p chromatin remodeling complex required for repression of a-specific genes, early meiotic genes during mitotic growth, and INO1</td></tr><tr><td>
<bold>386,478</bold></td><td><bold>LbPcc1</bold></td><td><bold>Regulator of sexual development</bold></td></tr><tr><td> 381,332</td><td>LbPriB</td><td>Primordia formation, Regulator of sexual development</td></tr><tr><td> 705,566</td><td>LbCDC5</td><td>Regulator of sexual development</td></tr><tr><td> 313,811</td><td>LbMoc3</td><td>Regulator of sexual development, ascus formation, and stress response</td></tr><tr><td> 680,902</td><td>LbPrf1</td><td>Regulator of pheromone signalling, filamentous growth and pathogenic development</td></tr><tr><td> 700,295</td><td>LbBri1</td><td>Regulator of fruiting body development; Regulation of the formation of the auto-inhibitor and of dikaryon-specific hydrophobins</td></tr><tr><td> 293,563</td><td>LbSnf5</td><td>Regulator of sexual development</td></tr><tr><td> 311,495</td><td>LbRum1</td><td>Repressor for genes regulated by the b mating type locus, involved in spore development</td></tr><tr><td> 451,323</td><td>LbMedA-1</td><td>Regulator of sexual and asexual development</td></tr><tr><td> 483,117</td><td>LbMedA-2</td><td>Regulator of sexual and asexual development</td></tr><tr><td colspan="3">
<italic>Asexual development and basal hyphal growth</italic></td></tr><tr><td> 685,688</td><td>LbCol21</td><td>Colonial, regulator of hyphal growth</td></tr><tr><td> 657,026</td><td>LbDevR</td><td>Required for conidiophore development</td></tr><tr><td>
<bold>298,274</bold></td><td><bold>LbAbaA</bold></td><td><bold>Regulator of conidiation</bold></td></tr><tr><td> 292,045</td><td>LbCon7</td><td>Cell morphology regulator</td></tr><tr><td> 481,451</td><td>LbReb1</td><td>Regulator of growth</td></tr><tr><td> 190,760</td><td>LbRsc8</td><td>Component of the RSC chromatin remodeling complex essential for viability and mitotic growth</td></tr><tr><td> 608,593</td><td>LbSnt2</td><td>Regulator of conidiation, hyphal growth and septation</td></tr><tr><td colspan="3">
<italic>Others</italic></td></tr><tr><td> 231,949</td><td>LbADA2</td><td>All development altered, regulator of basal hyphal growth and asexual and sexual development</td></tr><tr><td colspan="3">Cell cycle</td></tr><tr><td> 694,007</td><td>LbSwi6</td><td>MBF complex, regulator of cell cycle</td></tr><tr><td> 709,955</td><td>LbMbp1</td><td>MBF complex, regulator of cell cycle</td></tr><tr><td> 164,524</td><td>LbSep1</td><td>Activator for a small subset of mitotic genes involved in septation</td></tr><tr><td> 476,882</td><td>LbFkh2</td><td>Regulator of cell cycle</td></tr><tr><td>
<bold>481,652</bold></td><td><bold>LbSak1</bold></td><td><bold>Positive regulator of cAMP-dependent protein kinase-mediated exit from the mitotic cell cycle</bold></td></tr><tr><td> 622,520</td><td>LbCbf11</td><td>Regulator of cell adhesion and cell and nuclear division</td></tr><tr><td> 691,497</td><td>LbSFP1</td><td>Regulator of ribosomal protein, biogenesis genes, response to nutrients, stress and DNA-damage, G2/M transitions during mitotic cell cycle and cell size</td></tr><tr><td colspan="3">Metabolism</td></tr><tr><td colspan="3">
<italic>Carbon</italic></td></tr><tr><td> 443,509</td><td>LbCreA</td><td>Major carbon catabolite repression protein</td></tr><tr><td> 296,037</td><td>LbNrg1</td><td>Carbon catabolite repression</td></tr><tr><td> 399,488</td><td>LbAcuk</td><td>Positive regulator of gluconeogenesis</td></tr><tr><td> 567,783</td><td>LbAcuM-1</td><td>Positive regulator of gluconeogenesis</td></tr><tr><td> 670,648</td><td>LbAcuM-2</td><td>Positive regulator of gluconeogenesis</td></tr><tr><td> 708,062</td><td>LbAcuM-3</td><td>Positive regulator of gluconeogenesis</td></tr><tr><td> 708,164</td><td>LbRgm1</td><td>Positive regulator of monosaccharide catabolism and aldehyde metabolism</td></tr><tr><td> 308,583</td><td>LbCmr1</td><td>Regulator of melanin biosynthesis</td></tr><tr><td> 696,532</td><td>LbTrm2</td><td>Regulator of methanol-inducible gene expression</td></tr><tr><td colspan="3">
<italic>Nitrogen</italic></td></tr><tr><td> 488,576</td><td>LbAreA</td><td>Major, positively acting, nitrogen regulatory protein</td></tr><tr><td> 301,157</td><td>LbNirA-1</td><td>Pathway specific, positively acting nitrate regulatory protein</td></tr><tr><td> 317,073</td><td>LbNirA-2</td><td>Pathway specific, positively acting nitrate regulatory protein</td></tr><tr><td>
<bold>293,242</bold></td><td><bold>LbGcn4</bold></td><td><bold>Positive regulator of the transcriptional response to amino acid starvation</bold></td></tr><tr><td> 301,697</td><td>LbBAS1</td><td>Transcription factor, involved in regulating basal and induced expression of genes of the purine and histidine biosynthesis pathways; also involved in regulation of meiotic recombination at specific genes</td></tr><tr><td colspan="3">
<italic>Sulfur</italic></td></tr><tr><td> 706,529</td><td>LbCBF1</td><td>Activator of sulfur metabolism; centromere binding protein</td></tr><tr><td> 476,130</td><td>LbMetR-1</td><td>Activator of sulfur metabolism</td></tr><tr><td> 490,310</td><td>LbMetR-2</td><td>Activator of sulfur metabolism</td></tr><tr><td>
<italic>Lipid</italic></td><td></td><td></td></tr><tr><td> 654,679</td><td>LbFarA</td><td>Activates transcription of genes required for acetate utilization</td></tr><tr><td> 573,592</td><td>LbOaf3</td><td>Negative regulator of fatty acid metabolism</td></tr><tr><td colspan="3">
<italic>Others</italic></td></tr><tr><td> 459,853</td><td>LbHap2</td><td>CCAAT binding complex, subunit B</td></tr><tr><td> 708,105</td><td>LbHap3</td><td>CCAAT binding complex, subunit C</td></tr><tr><td> 694,786</td><td>LbHap5</td><td>CCAAT binding complex, subunit E</td></tr><tr><td> 574,778</td><td>LbHapX</td><td>CCAAT binding complex, subunit X; iron-responsive factor</td></tr><tr><td> 709,764 + 617,537</td><td>LbUrbs1</td><td>Negative Regulator of siderophore biosynthesis genes</td></tr><tr><td> 293,949</td><td>LbSfu1</td><td>Negative Regulator of Iron Uptake</td></tr><tr><td> 709,867</td><td>LbIec1</td><td>Subunit of the Ino80 complex, involved in nucleotide metabolism and phosphate metabolism</td></tr><tr><td colspan="3">
<italic>Stress and stimuli response</italic></td></tr><tr><td> 459,072</td><td>LbAsg1</td><td>Regulator of stress response and drug resistance</td></tr><tr><td> 699,455</td><td>LbHsf1</td><td>Heat shock transcription factor</td></tr><tr><td>
<bold>665,554</bold></td><td><bold>LbYap1</bold></td><td><bold>Regulator of oxidative stress tolerance</bold></td></tr><tr><td> 582,197 + 625,683</td><td>LbSkn7</td><td>Response to osmotic and oxidative stress</td></tr><tr><td> 379,257</td><td>LbPacC</td><td>Activator of alkaline-induced genes; repressor of acid-induced genes</td></tr><tr><td> 150,072</td><td>LbCrz1–1</td><td>Activator of genes involved in stress response</td></tr><tr><td> 636,734</td><td>LbCrz1–2</td><td>Activator of genes involved in stress response</td></tr><tr><td> 681,767</td><td>LbMSN4</td><td>Activator of genes involved in stress response</td></tr><tr><td> 607,158</td><td>LbZap1</td><td>Activator of zinc responsive genes</td></tr><tr><td> 652,780</td><td>LbHxl1</td><td>Unfolded protein response</td></tr><tr><td> 387,518</td><td>LbWC1</td><td>Light response and circadian rhythm regulator</td></tr><tr><td> 306,097</td><td>LbWC2</td><td>Light response and circadian rhythm regulator</td></tr><tr><td> 636,228</td><td>LbMbf1</td><td>Transcriptional coactivator involved in DNA replication stress and GCN4-dependent transcriptional activation</td></tr><tr><td> 442,607</td><td>LbXbp1</td><td>Stress-induced transcriptional repressor during mitosis, and late in meiosis</td></tr><tr><td colspan="3">Others</td></tr><tr><td> 301,089</td><td>LbBdp1</td><td>Transcription factor, involved in transcription of genes encoding tRNAs, 5S rRNA, U6 snRNA, and other small RNAs</td></tr><tr><td> 619,068</td><td>LbFhl1</td><td>Regulator of ribosomal protein (RP) transcription</td></tr><tr><td> 636,637</td><td>LbIIIA</td><td>Transcription factor, required for transcription of 5S rRNA</td></tr><tr><td> 149,540</td><td>LbNCB1 subunit alpha</td><td>Subunit of a heterodimeric NC2 transcription regulator complex</td></tr><tr><td> 660,430</td><td>LbNCB2 subunit beta</td><td>Subunit of a heterodimeric NC2 transcription regulator complex</td></tr><tr><td> 571,647</td><td>LbSql1</td><td>General transcriptional co-repressor</td></tr><tr><td> 667,862</td><td>LbAtf2</td><td></td></tr><tr><td> 309,497</td><td>LbDpb4</td><td>Subunit of the chromatin remodeling complex ISW2</td></tr><tr><td> 294,914</td><td>LbAbf2</td><td>Mitochondrial nucleoid protein</td></tr><tr><td> 474,585</td><td>LbNhp6B</td><td>Activator of the RNA polymerase III SNR6 gene</td></tr><tr><td> 625,238</td><td>LbPli1</td><td>SUMO E3 ligase involved in centromere and telomere maintenance</td></tr><tr><td> 669,147</td><td>LbSet3</td><td>Histone deacetylase involved in the regulation of cytokinesis</td></tr><tr><td> 702,907</td><td>LbSwc4</td><td>Subunit of the chromatin-remodeling complexes NuA4 and SWR1</td></tr><tr><td> 611,756</td><td>LbCdc39</td><td>Subunit of the CCR4-NOT1 core complex</td></tr><tr><td> 686,238</td><td>LbSnu66</td><td>Subunit of the U4/U6.U5 snRNP complex</td></tr></tbody></table><table-wrap-foot><p><sup>a</sup>TFs retrieved from and functionally validated by the TAT screen are in bold. See also Fig. <xref rid="Fig8" ref-type="fig">8</xref></p><p><sup>b</sup><italic>L. bicolor</italic> transcription factors were grouped into major functional classes based on homology with functionally characterized TFs from other fungi; gene names were derived from those of the corresponding homologs (see Additional file <xref rid="MOESM1" ref-type="media">1</xref>: Table S1 for further sequence information)</p><p><sup>c</sup>Specific putative function of <italic>L. bicolor</italic> TFs as deduced from the known function of their characterized homologs</p></table-wrap-foot></table-wrap></p></sec><sec id="Sec4"><title>TF expression profiling during ectomycorrhizal development</title><p id="Par14">We profiled the expression of <italic>Laccaria</italic> TFs during symbiosis development in 2-, 4-, 6- and 12-week-old <italic>Populus trichocarpa</italic> and <italic>Pseudotsuga menziesii</italic> ECM root tips [<xref ref-type="bibr" rid="CR55">55</xref>]. Each of the above time-points corresponds to a distinct ECM developmental stage (Fig. <xref rid="Fig2" ref-type="fig">2a</xref>). Two weeks post-contact, <italic>L. bicolor</italic> hyphae colonize the root surface and loosely aggregate onto rhizodermal root cells. After 4 weeks, hyphae ensheath plant roots forming the inner mantle, a multilayer hyphal pseudoparenchyma, in which fungal hyphae penetrate between rhizodermal cells. At 6 weeks, hyphae have formed the Hartig net and reached the cortical cell layer. After 12 weeks, the Hartig net is fully differentiated between cortical cells, whereas rhizodermal cells have collapsed. Douglas fir ECMs are considered to be anatomically differentiated and functional after six weeks, wheras 12 weeks are required to reach the same developmental stage in <italic>P. trichocarpa</italic> ECMs<italic>.</italic> Manual clustering maps of TFs differentially expressed compared to the free-living mycelium (≥ or ≤2.5-fold, corrected <italic>p</italic>-value ≤0.05) in poplar and Douglas fir ECMs are shown in Figs. <xref rid="Fig2" ref-type="fig">2b</xref> and <xref rid="Fig3" ref-type="fig">3</xref>, respectively.<fig id="Fig2"><label>Fig. 2</label><caption><p>Differential expression of <italic>L. bicolor</italic> TFs during the development of poplar (<italic>P. trichocarpa</italic>) ECM. <bold>a</bold> Laser-scanning confocal microscopy images of transverse sections of <italic>P. trichocarpa</italic> roots 2, 4, 6 and 12 weeks after contact with <italic>L. bicolor</italic> hyphae. Plant root cells are counterstained with propidium iodide and fungal cell walls are revealed using WGA-AlexaFluor 488. Bars indicate 10 μm. <bold>b</bold> Clustering of 100 differentially expressed <italic>L. bicolor</italic> TF transcripts (>2.5-fold; BH, modified <italic>t</italic>-test <0.05) during ECM development (2, 4, 6 and 12 weeks after contact) compared to free-living mycelium (see Additional file <xref rid="MOESM3" ref-type="media">3</xref>: Table S3 for the list of transcripts). Log2 transformed data were manually clustered. Each gene is represented by a row of coloured boxes (corresponding to ratio values) and a single column represents each developmental time-point. Regulation levels range from pale to saturated colours (red for induction; blue for repression). White indicates no change in gene expression. Protein IDs are given for each cluster. TFs up- or downregulated during both poplar and Douglas fir ECM development are shown in red and blue, respectively. TFs regulated in an opposite manner in ECM root tips of <italic>P. trichocarpa</italic> or <italic>P. menziesii</italic> are in green</p></caption><graphic xlink:href="12864_2017_4114_Fig2_HTML" id="MO2"></graphic></fig><fig id="Fig3"><label>Fig. 3</label><caption><p>Differential expression of <italic>L. bicolor</italic> TFs during the development of Douglas fir (<italic>P. menziesii</italic>) ECM. Clustering of 79 differentially-expressed <italic>L. bicolor</italic> TF transcripts (>2.5-fold; BH, modified <italic>t</italic>-test <0.05) during ECM development (2, 4 and 6 weeks after contact) compared to free-living mycelium (see Additional file <xref rid="MOESM4" ref-type="media">4</xref>: Table S4 for the list of transcripts). Log2 transformed data were manually clustered. Each gene is represented by a row of coloured boxes (corresponding to ratio values) and a single column represents each time-point. Regulation levels range from pale to saturated colours (red for induction; blue for repression). White indicates no change in gene expression. Protein IDs are given for each cluster. TFs up- or downregulated during both poplar and Douglas fir ECM development are shown in red and blue, respectively. TFs regulated in an opposite manner in ECM root tips of <italic>P. trichocarpa</italic> or <italic>P. menziesii</italic> are in green</p></caption><graphic xlink:href="12864_2017_4114_Fig3_HTML" id="MO3"></graphic></fig></p></sec><sec id="Sec5"><title>Transcription factor expression patterns during <italic>P. trichocarpa</italic> – <italic>L. bicolor</italic> Mycorrhiza development</title><p id="Par15">We manually identified five distinct clusters of differentially TF genes in <italic>P. trichocarpa</italic>- <italic>L. bicolor</italic> mycorrhizae compared to the free-living mycelium stage (Fig. <xref rid="Fig2" ref-type="fig">2</xref>, Additional file <xref rid="MOESM3" ref-type="media">3</xref>: Table S3). Cluster I corresponds to TFs upregulated during the latest stage of ECM development (6 and/or 12 weeks). They likely regulate the expression of genes involved in ECM functioning and in bi-directional nutrient exchanges. One of them, JGI ID# 443509, is related to the C2H2-type Zinc finger regulator CreA, involved in carbon catabolite repression in <italic>Aspergillus nidulans</italic>. Cluster II comprises TFs upregulated throughout ECM development (at least in 3 over the 4 time-points), suggesting a possible role of these components during the entire course of symbiosis development or even a general role throughout fungal development. Only four of these TFs are homologous to proteins of known function. LbRlm1–2 (JGI ID# 302141) is related to the MADS-box transcription factor RlmA, which regulates cell wall reinforcement in response to physical stress, whereas LbAbaA (JGI ID# 298274) is homologous to AbaA, a TEA/ATTS superfamily TF regulating hyphal growth. LbHom1–1 (JGI ID# 324166) belongs to the HOX homeodomain TF superfamily and LbCmr1 (JGI ID# 308583) is homologous to Cmr1, a regulator of pigment production.</p><p id="Par16">Clusters III, IV and V comprise downregulated TFs. Cluster III contains TF transcripts downregulated at four and six weeks. One of these transcripts codes for LbNirA1 a homolog of the nitrate assimilation pathway activator NirA. Its downregulation might be instrumental to finely tune nitrate metabolism during ECM formation. TFs in cluster IV are downregulated at either early (2 weeks) or late (12 weeks) stages of ECM development. The expression profiles of most of these TFs (46 out of 58) are unique to poplar-<italic>L. bicolor</italic> mycorrhizae. This cluster also contains TFs ressembling known regulators of nutrient (especially lipid) metabolism, such as LbMetR (JGI ID# 476130) and LbFarA (JGI ID# 654679). Several others TFs are related to regulators involved in fruiting body development (LbFst3, JGI ID# 585149; LbC2H2, JGI ID# 487295; LbHom2, JGI ID# 293988), hyphal growth (LbCol21, JGI ID# 685688; LbReb1, JGI ID# 481451)) and stress response (LbCrz1–2, JGI ID# 636734; LbPacC, JGI ID# 379257). TF transcripts downregulated throughout ECM development (at least in 3 over the 4 time-points) are grouped in cluster V, which includes the putative iron responsive factor LbHapX (JGI ID# 574778) and the cell cycle regulator LbMbp1 (JGI ID#709955).</p></sec><sec id="Sec6"><title>Transcription factor expression patterns during <italic>P. menziesii</italic> – <italic>L. bicolor</italic> Mycorrhiza development</title><p id="Par17">TF genes differentially expressed during Douglas fir- <italic>L. bicolor</italic> ECM formation were categorized into six distinct clusters according to their expression patterns (Fig. <xref rid="Fig3" ref-type="fig">3</xref>, Additional file <xref rid="MOESM4" ref-type="media">4</xref>: Table S4). Cluster I comprises TFs upregulated in the latest stage of mycorrhiza development (4 and/or 6 weeks) and similar to the situation previously observed in the case of the poplar symbiosis, it also includes LbCreA (JGI ID# 443509). This suggests that this particular TF may play a key role during the final stages of mycorrhiza development.</p><p id="Par18">Cluster II contains three TFs upregulated during the earlier stages of ECM development (2 and/or 4 weeks), which might be involved in the initial aggregation of the hyphae onto the root surface. One Zn-finger (JGI ID# 445505) protein is unique of <italic>L. bicolor</italic>. Another member of this group (JGI ID# 658142) is a HMG-box transcription factor.</p><p id="Par19">Cluster III is comprised of TFs upregulated throughout ECM development. The activator of the zinc responsive TF LbZap1 belongs to this cluster.</p><p id="Par20">TFs in Cluster IV are downregulated at six weeks. They include LbCon7 (JGI ID# 292045), a C2H2 Zn-finger TF homologous to Con7p, the central regulator of infection-related morphogenesis in the rice blast fungus <italic>Magnaporthe grisea</italic> and LbNrg1 (JGI ID# 296037), the homolog of the carbon catabolite Zn-finger repressor Nrg1 from <italic>Cryptococcus</italic>. Expression of these two genes is unique to Douglas fir- <italic>L. bicolor</italic> mycorrhizae.</p><p id="Par21">TFs downregulated at two and four weeks post-contact are grouped in Cluster V. One of them (JGI ID# 231949) is homologous to Ada2, the regulator of asexual development and basal hyphal growth in <italic>Neurospora crassa</italic>, and another one (JGI ID# 379291) is related to the <italic>Coprinellus disseminatus</italic> mating-type regulator HD2.</p><p id="Par22">Cluster VI contains TFs downregulated throughout ECM development. It includes the homologs of the stress response regulators PacC (JGI ID# 379257) and Skn7 (JGI ID# 625683), the regulator of sexual development, ascus formation and DNA integrity Moc3 (JGI ID# 313811) and the negative regulator of fatty acid metabolism Oaf3 (JGI ID# 573592). Interestingly, the nitrate metabolism regulator LbNirA1, also a member of this cluster, is constitutively downregulated all along Douglas- <italic>L. bicolor</italic> ECM development (Fig. <xref rid="Fig3" ref-type="fig">3</xref>, Cluster VI), whereas it was downregulated only at 2, 4 and 6 weeks post-contact, but slightly upregulated in mature mycorrhizae in the case of the poplar-<italic>L. bicolor</italic> interaction (Fig. <xref rid="Fig2" ref-type="fig">2b</xref>, Cluster III). It thus seems as if the host plant can regulate the expression of fungal transcription factors involved in nitrate assimilation.</p></sec><sec id="Sec7"><title>Commonalities and differences in the regulation of <italic>L. bicolor</italic> TF genes differentially expressed during poplar or Douglas fir ectomycorrhiza development</title><p id="Par23">The expression of 30 and 25 transcription factors is significantly upregulated in Douglas fir and poplar mycorrhizae, respectively. Twelve of them follow the same expression trend in both associations, while 18 and 13 TFs are uniquely upregulated in either Douglas fir or poplar mycorrhizae (Figs. <xref rid="Fig2" ref-type="fig">2b</xref> and <xref rid="Fig3" ref-type="fig">3</xref>, Additional files <xref rid="MOESM3" ref-type="media">3</xref> and <xref rid="MOESM4" ref-type="media">4</xref>: Tables S3 and S4). Transcriptional activators sharing the same expression trend belong to the core set of symbiosis-regulated TFs. They likely regulate the transcription of genes required for symbiosis development. Interestingly, the <italic>Laccaria</italic> orthologs of Cmr1 (JGI ID# 308583), CreA (JGI ID# 443509), AbaA (JGI ID# 298274) and Rlm1–2 (JGI ID# 302141) are part of this group. One gene sharing similarities with the amino acid biosynthesis regulator GCN4 (JGI ID# 395214), and other TFs similar to TFs involved in the regulation of acetate utilization (e.g., the homologs of <italic>Aspergillus nidulans</italic> FacB (JGI ID# 383085) and of <italic>Neurospora crassa</italic> Acu15 (JGI ID# 296682) belong to this group. Seven TFs belonging to this core set of similarly regulated transcription factors were subjected to an independent quantitative RT-Real Time-PCR validation conducted on <italic>L. bicolor – P. trichocarpa</italic> ECM root tips. This confirmed the expression trend revealed by oligo-array analysis for all but one transcription factor (JGI ID# 484885) (Fig. <xref rid="Fig4" ref-type="fig">4</xref>) and also highlighted the strikingly high expression levels of the hyphal growth regulator LbAbaA (JGI ID# 298274) [<xref ref-type="bibr" rid="CR50">50</xref>].<fig id="Fig4"><label>Fig. 4</label><caption><p>Real-time quantification of TF gene expression in mature <italic>P. trichocarpa</italic> – <italic>L. bicolor</italic> root tips. Gene expression level in ECM is shown for selected TF’s as the fold change compared to free-living mycelium. Mean values (<italic>n</italic> = 3) +/− S.E are represented. Significantly upregulated genes are indicated by * (<italic>p</italic> < 0,05; student T-test) or ** (<italic>p</italic> < 0,01; student T-test)</p></caption><graphic xlink:href="12864_2017_4114_Fig4_HTML" id="MO4"></graphic></fig></p><p id="Par24">Conversely, expression of 52 and 76 transcription factors is significantly downregulated in Douglas fir- and poplar mycorrhizae, respectively. Twenty-two of these TFs are concordantly regulated in both types of ECM root tips, while 30 and 54 of them are uniquely downregulated in either Douglas fir or poplar mycorrhizae (Figs. <xref rid="Fig2" ref-type="fig">2b</xref> and <xref rid="Fig3" ref-type="fig">3</xref>, Additional files <xref rid="MOESM3" ref-type="media">3</xref> and <xref rid="MOESM4" ref-type="media">4</xref>: Tables S3 and S4). TFs putatively involved in sexual development, fruiting body development and stress response are part of the <italic>L. bicolor</italic> downregulated core regulome, and include orthologs of <italic>Schizosaccharomyces pombe</italic> Moc3 (JGI ID# 313811) and <italic>Aspergillus nidulans</italic> PacC (JGI ID# 379257) as well as homologs to <italic>Ustilago maydis</italic> Prf1 (JGI ID# 482609) and <italic>Schizophyllum commune</italic> Fst4 (JGI ID# 304495). LbNirA (JGI ID# 301157), the ortholog of the <italic>A. nidulans</italic> nitrate assimilation regulator is also downregulated in both mycorrhizae, albeit with a different time-course. Four transcription factors are instead oppositely regulated in Douglas fir and poplar mycorrhizae. Three of these TFs, the putative regulators of sexual development and fruiting body formation LbNosA (JGI ID# 668161), LbC2H2 (JGI ID# 487295) and a TF apparently unique to <italic>Laccaria</italic> (JGI ID# 445505), are selectively upregulated in Douglas fir ECMs, whereas the fourth TF (JGI ID# 296675) is selectively upregulated in poplar ECMs (Figs. <xref rid="Fig2" ref-type="fig">2b</xref> and <xref rid="Fig3" ref-type="fig">3</xref>).</p></sec><sec id="Sec8"><title>TF expression regulation in other mutualistic interactions</title><p id="Par25"><italic>L. bicolor</italic> TF genes regulated during Poplar or Douglas fir ECM development mainly belong to the Zn-cluster-, fungal specific- and C2H2 Zn-finger-superfamilies of DNA binding domains (Fig. <xref rid="Fig4" ref-type="fig">4</xref>). To find out whether this is a unique feature of <italic>Laccaria</italic> or a general property of ECM fungi, we searched for differentially expressed TFs (≥2.5-fold, <italic>p</italic>-value <0.05) (Additional file <xref rid="MOESM5" ref-type="media">5</xref>: Table S5) in the transcriptomes of the ectomycorrhizal fungi <italic>Amanita muscaria, Cenococcum geophilum, Hebeloma cylindrosporum, Paxillus involutus, Piloderma croceum, Suillus luteus,</italic> and <italic>Tuber melanosporum</italic> [<xref ref-type="bibr" rid="CR26">26</xref>]. The orchid mycorrhizal fungi <italic>Sebacina vermifera</italic> and <italic>Tulasnella calospora,</italic> and the ericoid mycorrhizal fungus <italic>Oidiodendron maius</italic> were also included in this survey (Additional file <xref rid="MOESM5" ref-type="media">5</xref>: Table S5). Depending on the species, upregulated TFs represent 4.8% to 15.9% of the total TF repertoire, and, as in <italic>Laccaria</italic>, they mainly belong to the Zn-cluster-, fungal-specific- and C2H2 Zn -finger-superfamilies (Fig. <xref rid="Fig5" ref-type="fig">5</xref>). In half of the examined species, the Zn-cluster- and/or fungal-specific TF families show a statistically significant enrichment in upregulated transcripts compared to their genome abundance (Fisher exact test).<fig id="Fig5"><label>Fig. 5</label><caption><p>Distribution of differentially-expressed TF gene families in several types of mycorrhizal associations. We retrieved gene expression data of TF-encoding genes from roots colonized by the following species: ECM fungi (<italic>L. bicolor, A. muscaria, H. cylindrosporum, P. croceum, S. luteus, P. involutus, C. geophilum</italic> and <italic>T. melanosporum</italic>), orchid mycorrhizal fungi (<italic>S. vermifera</italic> and <italic>T. calospora</italic>) and one ericoid fungus <italic>O. maius</italic> from Kohler et al. [<xref ref-type="bibr" rid="CR26">26</xref>]. Differentially-expressed TF genes (≥ 2.5-fold, <italic>p</italic>-value ≤0.05) (<bold>a</bold>, upregualted; <bold>b</bold>, down regulated) in mycorrhizal roots in comparison to free-living mycelium. The histograms show the distribution of TFs from each family as a percentage of the total of TFs in the genome of the corresponding fungi. The total number of regulated TFs for each fungus is indicated between brackets. Stars (*) Indicate families enriched in up-regulated genes compared to the number of these genes in the respective genome (Fisher exact test <italic>p</italic> < 0.05)</p></caption><graphic xlink:href="12864_2017_4114_Fig5_HTML" id="MO5"></graphic></fig></p><p id="Par26">The fraction of downregulated TFs depends on the ECM fungal species and ranges from 0.8% to 27.4% (Fig. <xref rid="Fig5" ref-type="fig">5</xref>). No significant enrichment of specific TF families could be identified within downregulated transcription factors, except for the <italic>H. cylindrosporum</italic> symbiotic transcriptome, which is enriched in both histone-fold and Myb TF families, and the C2H2 Zn-finger TF enrichment observed in <italic>T. calospora</italic>.</p><p id="Par27">Assuming that the core set of differentially expressed <italic>L. bicolor</italic> TFs is essential for ECM development, we then examined other ECM fungal genomes/transcriptomes for the presence and mode of regulation of homologous TFs (Additional file <xref rid="MOESM6" ref-type="media">6</xref>: Table S6). Interestingly, none of the homologous TF genes upregulated in <italic>L. bicolor</italic> ECM was found to be similarly upregulated in all other symbiotic transcriptomes [<xref ref-type="bibr" rid="CR26">26</xref>]. However, despite this lack of regulatory overlap, all homologs of upregulated <italic>L. bicolor</italic> TF genes are expressed at above background levels in all ECM fungi and two of them (LbRlm1–2, LbAbaA) are upregulated in all mycorrhizae involving a fungal partner belonging to the Agaricales (i.e., <italic>L. bicolor</italic>, <italic>A. muscaria</italic> and <italic>H. cylindrosporum</italic>). Homologs of LbCreA are also upregulated in <italic>A. muscaria</italic> and <italic>C. geophilum</italic>. Conversely, TFs homologous to the Zn-cluster regulator LbMoc3 (JGI ID# 313811) are concordantly downregulated in the Basidiomycota <italic>A. muscaria</italic>, <italic>H. cylindrosporum</italic>, <italic>S. luteus</italic> and <italic>P. involutus</italic>, and in the Ascomycete <italic>C. geophilum,</italic> suggesting that downregulation of this particular TF is somehow required for ECM development. Altogether, these results suggest that each ECM fungus evolved its own TF network to regulate symbiosis development and functioning. The most notable exceptions are the few TFs (i.e., Rlm1, AbaA and Moc3) that are concordantly regulated in different ECM transcriptomes, which will require more in-depth investigations in order to understand their specific role in mycorrhizal development.</p></sec><sec id="Sec9"><title>Functional screening and validation of <italic>L. bicolor</italic> and poplar transcriptional activators in yeast</title><p id="Par28">To functionally validate some of the predicted TFs and to uncover potentially new (hard to predict) transcriptional activators, we coupled <italic>in silico</italic> analysis with a heterologous gene transactivation screen, known as transcriptional activator trap (TAT), performed in the yeast <italic>S. cerevisiae</italic> [<xref ref-type="bibr" rid="CR31">31</xref>, <xref ref-type="bibr" rid="CR44">44</xref>, <xref ref-type="bibr" rid="CR53">53</xref>, <xref ref-type="bibr" rid="CR54">54</xref>, <xref ref-type="bibr" rid="CR65">65</xref>]. To this end, three distinct full-length cDNA libraries were prepared from: (i) a mix of free-living mycelium (FLM) and fruiting bodies (FB) (FLM + FB library); (ii) <italic>L. bicolor</italic>/<italic>P. trichocarpa</italic> mycorrhizae of different ages (2, 4, 6 and 12 weeks-old) (ECM library); and (iii) non-mycorrhizal <italic>P. trichocarpa</italic> roots (Root library). Yeast transformants harbouring an in-frame fusion between a <italic>L. bicolor</italic> or <italic>P. trichocarpa</italic> transcriptional activation domain and the DNA-binding domain of the yeast regulator GAL4 were positively selected via reporter gene transactivation assays. Approximately 1.7, 2.0 and 0.8 million colonies were screened for the FLM + FB, ECM and Root libraries, respectively. A total of 596 sequences (196 from the FLM + FB library, 213 from the ECM library, and 187 from the Root library) were found to be capable of activating the expression of three distinct reporter genes and were retained for further analysis. They were organized into 83 contigs and 137 singletons corresponding to a total of 220 unisequences (Fig. <xref rid="Fig6" ref-type="fig">6</xref>).<fig id="Fig6"><label>Fig. 6</label><caption><p>Venn diagram of the number of independent clones (left) and corresponding unisequences (right) isolated from the TAT screening of the FLM + FB, Roots and ECM libraries. The number of DBD-containing clones is shown in brackets. Sequences of plant origin retrieved from the screening of the Roots and ECM library are shown on a gray background</p></caption><graphic xlink:href="12864_2017_4114_Fig6_HTML" id="MO6"></graphic></fig></p><p id="Par29">Approximately 63% (140 out of 220) of the retrieved unisequences were of plant origin and the remaining ones were from the fungal partner (Fig. <xref rid="Fig6" ref-type="fig">6</xref>). Nearly half of the plant-derived sequences (66 out of 140) encoded either a DNA-binding domain matching the DBDs of <italic>in silico</italic> predicted TFs (61 sequences), or a diverse but still recognizable nucleic acid binding domain (5 sequences). Overall, the TAT assay thus allowed the identification of 61 bona fide plant TFs mainly belonging to the ERF, Myb, NAC, WRKY, Dof and EINL families (Additional file <xref rid="MOESM7" ref-type="media">7</xref>: Table S7).</p><p id="Par30">As expected, the TAT screen of the ECM library yielded a large fraction of sequences (80 out of 117 unisequences) of plant origin (Fig. <xref rid="Fig6" ref-type="fig">6</xref>). Interestingly, half of these putative poplar TFs shared a significant similarity with other plant transcriptional activators known to be involved in plant-microbe interactions, both pathogenic [<xref ref-type="bibr" rid="CR46">46</xref>, <xref ref-type="bibr" rid="CR59">59</xref>, <xref ref-type="bibr" rid="CR64">64</xref>] and mutualistic [<xref ref-type="bibr" rid="CR44">44</xref>] (Fig. <xref rid="Fig7" ref-type="fig">7</xref>). On the other hand, only 16 of the in silico identified <italic>L. bicolor</italic> TFs were confirmed and identified by the TAT screen, three of which belong to the core set of symbiosis-regulated TFs. Thirtheen of those genes are within the 20% of the most highly expressed genes at least in one time point of the ectomycorrhiza time-course (80th percentile, data not shown). In addition, the TAT-screen allowed the identification of two DBD-containing activators that were not retrieved from <italic>in silico</italic> analysis (JGI ID# 457991 and JGI ID# 700637) and five activators containing an aspecific nucleic acid binding domain (Table <xref rid="Tab2" ref-type="table">2</xref>). The other 57 TAT-positive putative TFs, all of which lacking a recognizable DBD, are collectively designated as ‘unconventional transcriptional activators’ (see below).<fig id="Fig7"><label>Fig. 7</label><caption><p>Distribution of plant proteins retrieved from the TAT screening of the ECM library into TF families. The DBD-containing transcription factors of the plant mycorrhizal partner retrieved from the TAT screening of the ECM library are assigned to TF families, either for <italic>T. melanosporum-Corylus avellana</italic> ECM root tips (<bold>a</bold>) and for <italic>L. bicolor-P. trichocarpa</italic> ECM root tips (<bold>b</bold>). Families of TFs related to plant-microbe interactions and pathogen defence [<xref ref-type="bibr" rid="CR46">46</xref>, <xref ref-type="bibr" rid="CR59">59</xref>, <xref ref-type="bibr" rid="CR64">64</xref>] are highly represented</p></caption><graphic xlink:href="12864_2017_4114_Fig7_HTML" id="MO7"></graphic></fig><table-wrap id="Tab2"><label>Table 2</label><caption><p>List of <italic>L. bicolor</italic> TFs, unconventional activators, and putative unconventional activators retrieved from, and functionally validated by, the TAT screen of FLM + FB and ECM libraries</p></caption><table frame="hsides" rules="groups"><thead><tr><th colspan="4">Sequence information</th><th colspan="3">BlastP results</th><th colspan="2">Conserved domains</th></tr><tr><th>seq ID</th><th>Protein ID</th><th>FLM/FB</th><th>ECM</th><th>ACC number</th><th>Description</th><th>Organism</th><th>IPR number</th><th>Description</th></tr></thead><tbody><tr><td colspan="9"><italic>Transcription factors (bearing a recognizable and specific DBD)</italic></td></tr><tr><td> Contig05</td><td>293242</td><td>59</td><td>10</td><td>BAC55240.1</td><td>C-Gcn4</td><td><italic>Candida maltosa</italic></td><td>IPR011616</td><td>bZIP</td></tr><tr><td> ECM-L2_G03</td><td>298274</td><td>0</td><td>1</td><td>XP_001388805.1</td><td>regulatory protein AbaA</td><td><italic>Aspergillus niger</italic></td><td>IPR000818</td><td>TEA/ATTS</td></tr><tr><td> ECM-L1_F11</td><td>307744</td><td>0</td><td>1</td><td>XP_002173151.1</td><td>meiotically upregulated gene product</td><td><italic>Schizosaccharomyces japonicus</italic></td><td>IPR014778</td><td>Myb</td></tr><tr><td> Contig62</td><td>386478</td><td>7</td><td>0</td><td>XP_001830477.1</td><td>PCC1</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR000910</td><td>HMG1/HMG2</td></tr><tr><td> Contig41</td><td>393192</td><td>3</td><td>0</td><td>XP_001886200.1</td><td>STE12-like</td><td><italic>Laccaria bicolor</italic></td><td>IPR013087</td><td>C2H2</td></tr><tr><td> ECM-L1_A03</td><td>457991</td><td>0</td><td>1</td><td>XP_002910064.1</td><td>NWD2</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR000253</td><td>Forkhead</td></tr><tr><td> Contig40</td><td>458057</td><td>15</td><td>1</td><td>XP_001383328.2</td><td>ROX1-like HMG-box TF</td><td><italic>Scheffersomyces stipitis</italic></td><td>IPR000910</td><td>HMG1/HMG2</td></tr><tr><td> Contig65</td><td>481652</td><td>3</td><td>1</td><td>XP_003501811.1</td><td>RFX2</td><td><italic>Cricetulus griseus</italic></td><td>IPR003150</td><td>RFX</td></tr><tr><td> FLM-L2_D07</td><td>482609</td><td>1</td><td>0</td><td>XP_001828950.2</td><td>specific transcriptional repressor</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR000910</td><td>HMG1/HMG2</td></tr><tr><td> FLM-L2_D05</td><td>486090</td><td>1</td><td>0</td><td>XP_003034605.1</td><td>expressed protein</td><td><italic>Schizophyllum commune</italic></td><td>IPR001138</td><td>Zn2Cys6</td></tr><tr><td> Contig46</td><td>628355</td><td>1</td><td>1</td><td>XP_567555.1</td><td>transcriptional regulatory protein</td><td><italic>Cryptococcus neoformans</italic></td><td>IPR007219</td><td>Transcription factor, fungi</td></tr><tr><td> FLM-L2_A08</td><td>633206</td><td>1</td><td>0</td><td>XP_001368548.1</td><td>zinc finger protein 850-like</td><td><italic>Musca domestica</italic></td><td>IPR013087</td><td>C2H2</td></tr><tr><td> Contig43</td><td>640940</td><td>3</td><td>1</td><td>AAC32736.1</td><td>Prf1</td><td><italic>Ustilago maydis</italic></td><td>IPR000910</td><td>HMG1/HMG2</td></tr><tr><td> Contig38</td><td>648888</td><td>6</td><td>3</td><td>AAC32736.1</td><td>Prf1</td><td><italic>Ustilago maydis</italic></td><td>IPR000910</td><td>HMG1/HMG2</td></tr><tr><td> ECM-L1_H01</td><td>656449</td><td>0</td><td>1</td><td>XP_001819986.2</td><td>regulatory protein abaA</td><td><italic>Aspergillus oryzae</italic></td><td>IPR000818</td><td>TEA/ATTS</td></tr><tr><td> Contig75</td><td>665554</td><td>2</td><td>0</td><td>AAS64313.1</td><td>Chap1</td><td><italic>Cochliobolus heterostrophus</italic></td><td>IPR011616</td><td>bZIP</td></tr><tr><td> Contig07</td><td>682475</td><td>2</td><td>0</td><td>XP_001399919.1</td><td>C6 transcription factor (Mut3)</td><td><italic>Aspergillus niger</italic></td><td>IPR001138</td><td>Zn2Cys6</td></tr><tr><td> Contig42</td><td>700637</td><td>16</td><td>5</td><td>EGO20236.1</td><td>hypothetical protein</td><td><italic>Serpula lacrymans</italic></td><td>IPR000433</td><td>ZZ Zinc finger</td></tr><tr><td colspan="9"><italic>Proteins containing an aspecific nucleic acid binding domain</italic></td></tr><tr><td> Contig27</td><td>451329</td><td>0</td><td>2</td><td>XP_002911693</td><td>CAP-Gly domain-containing protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR001878</td><td>Zinc finger, CCHC-type</td></tr><tr><td> Contig39</td><td>585018</td><td>2</td><td>0</td><td>XP_001836279.2</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR001606</td><td>ARID/BRIGHT DNA-binding domain</td></tr><tr><td> Contig45</td><td>699941</td><td>2</td><td>0</td><td>XP_001828564.2</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR019787</td><td>Zinc finger, PHD-finger</td></tr><tr><td> FLM-L1_B12</td><td>640654</td><td>1</td><td>0</td><td>XP_003507462.1</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR018957</td><td>Zinc finger, C3HC4 RING-type</td></tr><tr><td> ECM-L1_E11</td><td>705628</td><td>0</td><td>1</td><td>XP_002172787.1</td><td>cps3</td><td><italic>Schizosaccharomyces japonicus</italic></td><td>IPR000571</td><td>Zinc finger, CCCH-type</td></tr><tr><td colspan="9"><italic>Unconventional activators with nuclear localization</italic></td></tr><tr><td> FLM-L3_C01</td><td>299583</td><td>1</td><td>0</td><td>XP_001836340.2</td><td>TKL/TKL-ccin protein kinase</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR017442</td><td>Serine/threonine-PK-like domain</td></tr><tr><td> FLM-L2_B06</td><td>300643</td><td>1</td><td>0</td><td>CCA73543.1</td><td>rec8- related meiotic recombination</td><td><italic>Piriformospora indica</italic></td><td>IPR006910</td><td>Rad21/Rec8-like protein, N-terminal</td></tr><tr><td> ECM-L2_D08</td><td>468224</td><td>0</td><td>1</td><td>XP_001828858.2</td><td>Rad21 protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR006909</td><td>Rad21/Rec8-like protein, C-terminal</td></tr><tr><td> Contig70</td><td>459401</td><td>0</td><td>3</td><td>XP_001833620.2</td><td>ubiquitin-protein ligase</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR000008</td><td>C2 calcium-dependent membrane targeting</td></tr><tr><td> FLM-L2_F09</td><td>610588</td><td>1</td><td>0</td><td>BAG24499.1</td><td>rad57</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR013632</td><td>DNA recombination and repair protein</td></tr><tr><td> Contig72</td><td>636246</td><td>0</td><td>2</td><td>CCA72600.1</td><td>EDE1-related, endocytosis</td><td><italic>Piriformospora indica</italic></td><td>IPR000449</td><td>Ub-associated/transl elongation factor EF1B</td></tr><tr><td> ECM-L2_D05</td><td>685195</td><td>0</td><td>1</td><td>NP_595780.1</td><td>ribosome biogenesis protein Nop6</td><td><italic>Schizosaccharomyces pombe</italic></td><td></td><td></td></tr><tr><td> ECM-L1_B01</td><td>698517</td><td>0</td><td>1</td><td>XP_002472728.1</td><td>60S acidic ribosomal protein P1</td><td><italic>Postia placenta</italic></td><td>IPR001813</td><td>Ribosomal protein 60S</td></tr><tr><td> FLM-L2_D02</td><td>700143</td><td>1</td><td>0</td><td>XP_001828708.2</td><td>CMGC/RCK/MAK protein kinase</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR017442</td><td>Serine/threonine-PL-like domain</td></tr><tr><td colspan="9"><italic>Putative unconventional activators with intracellular localization</italic></td></tr><tr><td> Contig03</td><td>190404</td><td>0</td><td>3</td><td>XP_001880663.1</td><td>aspartic peptidase A1</td><td><italic>Laccaria bicolor</italic></td><td>IPR001461</td><td>Peptidase A1</td></tr><tr><td> FLM-L1_F07</td><td>192523</td><td>1</td><td>0</td><td>XP_001877048.1</td><td>tubulin alpha</td><td><italic>Laccaria bicolor</italic></td><td>IPR003008</td><td>Tubulin/FtsZ, GTPase domain</td></tr><tr><td> FLM-L2_D04</td><td>243371</td><td>1</td><td>0</td><td>XP_002912138.1</td><td>aconitate hydratase</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR000573</td><td>Aconitase A/isopropylmalate dehydratase</td></tr><tr><td> Contig36</td><td>294384</td><td>5</td><td>0</td><td>XP_568826.1</td><td>tubulin binding protein</td><td><italic>Cryptococcus neoformans</italic></td><td></td><td></td></tr><tr><td> ECM-L3_B06</td><td>324430</td><td>0</td><td>1</td><td>XP_001877591.1</td><td>copper transporter</td><td><italic>Laccaria bicolor</italic></td><td>IPR007274</td><td>Ctr copper transporter</td></tr><tr><td> ECM-L3_A03</td><td>327303</td><td>0</td><td>1</td><td>XP_001274183.1</td><td>mitochondrial GTPase (YlqF)</td><td><italic>Aspergillus clavatus</italic></td><td>IPR023179</td><td>GTP-binding protein</td></tr><tr><td> Contig01</td><td>444552</td><td>4</td><td>0</td><td>XP_001835217.1</td><td>peroxin19</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR006708</td><td>Pex19 protein</td></tr><tr><td> ECM-L3_D03</td><td>521043</td><td>0</td><td>1</td><td>CCA67049.1</td><td>related to PDR16- lipid biosynthesis</td><td><italic>Piriformospora indica</italic></td><td>IPR001251</td><td>Cellular retinaldehyde-binding</td></tr><tr><td> Contig09</td><td>583617</td><td>8</td><td>0</td><td>CCA71746.1</td><td>related to proteophosphoglycan ppg4</td><td><italic>Piriformospora indica</italic></td><td></td><td></td></tr><tr><td> ECM-L2_F10</td><td>608638</td><td>0</td><td>1</td><td>XP_001831367.1</td><td>gamma-adaptin</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR002553</td><td>Clathrin/coatomer adaptor, adaptin-like</td></tr><tr><td> FLM-L2_H04</td><td>656953</td><td>1</td><td>0</td><td>XP_001837070.1</td><td>vacuole protein</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> FLM-L2_E08</td><td>659644</td><td>1</td><td>0</td><td>XP_001839900.1</td><td>elongation factor 3</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR015688</td><td>Elongation Factor 3</td></tr><tr><td> FLM-L2_E09</td><td>671307</td><td>1</td><td>0</td><td>XP_001830051.1</td><td>peroxisomal targeting signal 1 receptor</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR001440</td><td>Tetratricopeptide TPR-1</td></tr><tr><td> FLM-L2_D03</td><td>695354</td><td>1</td><td>0</td><td>XP_001840019.1</td><td>mitochondrial carrier protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR018108</td><td>Mitochondrial substrate/solute carrier</td></tr><tr><td> ECM-L2_E11</td><td>703237</td><td>0</td><td>1</td><td>XP_002911229.1</td><td>rho GDP-dissociation inhibitor</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR000406</td><td>RHO protein GDP dissociation inhibitor</td></tr><tr><td> FLM-L2_A07</td><td>707485</td><td>1</td><td>0</td><td>XP_002910841.1</td><td>guanine nucleotide exchange factor</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR003123</td><td>Vacuolar sorting protein 9</td></tr><tr><td> ECM-L1_B05</td><td>311818</td><td>0</td><td>1</td><td>XP_003037815.1</td><td>hypothetical protein</td><td><italic>Schizophyllum commune</italic></td><td></td><td></td></tr><tr><td> FLM-L2_F11</td><td>321043</td><td>1</td><td>0</td><td>XP_001829416.1</td><td>hypothetical protein CC1G_00595</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> ECM-L2_D01</td><td>325350</td><td>0</td><td>1</td><td>P_001837732.1</td><td>hypothetical protein CC1G_06938</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> FLM-L2_H02</td><td>390988</td><td>1</td><td>0</td><td>XP_001841219.1</td><td>hypothetical protein CC1G_11382</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> FLM-L1_C04</td><td>439929</td><td>1</td><td>0</td><td>EGO18585.1</td><td>hypothetical protein</td><td><italic>Serpula lacrymans</italic></td><td></td><td></td></tr><tr><td> Contig32</td><td>459061</td><td>0</td><td>3</td><td>XP_003026161.1</td><td>hypothetical protein</td><td><italic>Schizophyllum commune</italic></td><td></td><td></td></tr><tr><td> Contig10</td><td>509577</td><td>1</td><td>1</td><td>XP_001882083.1</td><td>predicted protein</td><td><italic>Laccaria bicolor</italic></td><td></td><td></td></tr><tr><td> FLM-L3_F02</td><td>546684</td><td>1</td><td>0</td><td>EGO29111.1</td><td>hypothetical protein</td><td><italic>Serpula lacrymans</italic></td><td></td><td></td></tr><tr><td> Contig54</td><td>549772</td><td>4</td><td>1</td><td>XP_001833470.2</td><td>hypothetical protein CC1G_05170</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> Contig76</td><td>576504</td><td>5</td><td>0</td><td>XP_001828840.2</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> Contig37</td><td>604174</td><td>2</td><td>0</td><td>XP_001834463.1</td><td>hypothetical protein CC1G_02199</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> Contig24</td><td>613652</td><td>2</td><td>0</td><td>XP_001830379.1</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> ECM-L3_B04</td><td>622202</td><td>0</td><td>1</td><td>XP_001828856.1</td><td>hypothetical protein CC1G_03650</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> ECM-L2_E05</td><td>626440</td><td>0</td><td>1</td><td>NP_587684.1</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR019350</td><td>RNA polymerase I-specific transcription initiation factor RRN6-like</td></tr><tr><td> FLM-L1_G10</td><td>634434</td><td>1</td><td>0</td><td>XP_001831375.1</td><td>hypothetical protein CC1G_00922</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> FLM-L2_F03</td><td>656382</td><td>1</td><td>0</td><td>XP_001875331.1</td><td>predicted protein</td><td><italic>Laccaria bicolor</italic></td><td></td><td></td></tr><tr><td> Contig78</td><td>680010</td><td>5</td><td>0</td><td>XP_002476516.1</td><td>predicted protein</td><td><italic>Postia placenta</italic></td><td></td><td></td></tr><tr><td> FLM-L2_E07</td><td>686252</td><td>1</td><td>0</td><td>XP_001836432.2</td><td>hypothetical protein CC1G_07079</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> ECM-L3_C02</td><td>688275</td><td>0</td><td>1</td><td>XP_001835642.2</td><td>hypothetical protein CC1G_03424</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR016021</td><td>MIF4-like, type 1/2/3</td></tr><tr><td> Contig58</td><td>693322</td><td>0</td><td>4</td><td>XP_001830639.2</td><td>hypothetical protein CC1G_06905</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR003864</td><td>Domain of unknown function DUF221</td></tr><tr><td> ECM-L1_B02</td><td>693899</td><td>0</td><td>1</td><td>EGO22612.1</td><td>hypothetical protein</td><td><italic>Serpula lacrymans</italic></td><td></td><td></td></tr><tr><td> FLM-L1_E04</td><td>708222</td><td>1</td><td>0</td><td>XP_003036324.1</td><td>expressed protein</td><td><italic>Schizophyllum commune</italic></td><td></td><td></td></tr><tr><td> Contig68</td><td>708574</td><td>0</td><td>2</td><td>XP_001833764.1</td><td>hypothetical protein</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td colspan="9"><italic>Secreted protein</italic></td></tr><tr><td> ECM-L1_H02</td><td>394934</td><td>0</td><td>1</td><td>ZP_01463678.1</td><td>sphingolipid ceramide N-deacylase</td><td><italic>Stigmatella aurantiaca</italic></td><td></td><td></td></tr><tr><td> Contig44</td><td>643792</td><td>3</td><td>0</td><td>XP_001836617.1</td><td>hypothetical protein CC1G_06204</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> FLM-L3_H05</td><td>658920</td><td>1</td><td>0</td><td>XP_001830283.1</td><td>hypothetical protein CC1G_01919</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td> FLM-L2_G08</td><td>660445</td><td>1</td><td>0</td><td>XP_001835021.1</td><td>hypothetical protein CC1G_09912</td><td><italic>Coprinopsis cinerea</italic></td><td>IPR018499</td><td>Tetraspanin</td></tr><tr><td> FLM-L1_G04</td><td>688063</td><td>1</td><td>0</td><td>XP_001835466.2</td><td>hypothetical protein CC1G_05428</td><td><italic>Coprinopsis cinerea</italic></td><td></td><td></td></tr><tr><td colspan="9"><italic>Secreted proteins with nuclear localization signal (STAPs)</italic></td></tr><tr><td> FLM-L1_A04</td><td>304792</td><td>1</td><td>0</td><td>XP_001840014.1</td><td>hypothetical protein CC1G_10398</td><td>Coprinopsis cinerea</td><td></td><td></td></tr><tr><td> FLM-L1_F01</td><td>391051</td><td>1</td><td>0</td><td>XP_001840014.1</td><td>hypothetical protein</td><td>Coprinopsis cinerea</td><td></td><td></td></tr><tr><td> FLM-L1_D07</td><td>455116</td><td>1</td><td>0</td><td>XP_001884865.1</td><td>predicted protein</td><td>Laccaria bicolor</td><td></td><td></td></tr><tr><td> Contig64</td><td>659547</td><td>77</td><td>1</td><td>AAD01986.1</td><td>ras related protein</td><td>Laccaria bicolor</td><td></td><td></td></tr></tbody></table></table-wrap></p><p id="Par31">Of note, nine of the 16 functionally validated <italic>L. bicolor</italic> TFs resemble known transcription factors regulating development and invasiveness (or pathogenicity). These include two genes closely related to Prf1, the pheromone signalling and filamentous growth regulator of <italic>Ustilago maydis</italic> [<xref ref-type="bibr" rid="CR21">21</xref>] and two genes similar, respectively, to Pcc1, a regulator of mating and fruiting body formation in <italic>Coprinopsis cinerea</italic> [<xref ref-type="bibr" rid="CR4">4</xref>, <xref ref-type="bibr" rid="CR62">62</xref>], and to Ste12, a TF involved in mating, cell fusion, and in some cases invasive growth regulation in various fungi (reviewed in [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR73">73</xref>]). Five additional TAT-validated TFs resemble the <italic>Aspergillus nidulans</italic> conidiophore regulator AbaA [<xref ref-type="bibr" rid="CR1">1</xref>], the <italic>Candida albicans</italic> filamentous growth/virulence regulator Rfg1/Rox1 [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR25">25</xref>], the oxidative stress tolerance regulator Yap1/Chap1 [<xref ref-type="bibr" rid="CR10">10</xref>, <xref ref-type="bibr" rid="CR30">30</xref>], and the amino acid starvation response transcription factor GCN4 [<xref ref-type="bibr" rid="CR68">68</xref>] (see Table <xref rid="Tab2" ref-type="table">2</xref> for further details). The TAT results of a representative subset of these TFs described in Table <xref rid="Tab1" ref-type="table">1</xref> are shown in Fig. <xref rid="Fig8" ref-type="fig">8</xref>.<fig id="Fig8"><label>Fig. 8</label><caption><p>Functional validation of <italic>L. bicolor</italic> transcriptional activators. Representative example of TAT results conducted on the six TFs similar to known function genes. Colonies were isolated from the TAT assay plates and analyzed by serial dilution assays (starting from an OD600 of 1.0) and 2 μl of each dilution were plated on selective plates. Resistance to 50 mM His3 enzyme inhibitor 3-amino-triazole (3-AT) and uracil prototrophy were used to assay the expression of the HIS3 and URA3 reporter genes. For the LacZ (β -Gal) gene reporter assay, 2 μl of yeast cell dilutions (OD600 = 0.1) were spotted on YPD plates overlaid by a nylon membrane, which were then incubated overnight at 30 °C, prior to β -galactosidase assay. Empty pDEST32 vector transformants were used as negative control; wt, m1 and m2 are internal assay controls</p></caption><graphic xlink:href="12864_2017_4114_Fig8_HTML" id="MO8"></graphic></fig></p></sec><sec id="Sec10"><title>Unconventional transcriptional activators</title><p id="Par32">In addition to the validation of a subset of <italic>in silico</italic> predicted TFs, the TAT screen also allowed the identification of 57 putative transcriptional activators lacking a recognizable DBD, and thus designated as ‘unconventional transcriptional activators’ (Table <xref rid="Tab2" ref-type="table">2</xref>). Nine of them resemble known nuclear (e.g., Nop6, Rad21 and Rad 57) or nucleo-cytoplasmic (e.g., Ede 1) proteins, for which a direct or indirect role in transcriptional regulation and/or other nuclear processes (e.g., ribosome biogenesis, double-strand break repair and chromatid cohesion) has been previously documented (Table <xref rid="Tab2" ref-type="table">2</xref>). The remaining TAT-positive sequences code for intracellular proteins without a known transcriptional role, including metabolic enzymes, mitochondrial and peroxisomal proteins, plus 19 conserved hypothetical proteins. Interestingly, nine of these TAT-positive sequences code for predicted secreted proteins, four of which contain a recognizable nuclear localization signal (NLS). We named the latter proteins <underline>S</underline>ecreted <underline>T</underline>ranscriptional <underline>A</underline>ctivator <underline>P</underline>roteins (STAPs) (Table <xref rid="Tab2" ref-type="table">2</xref>). One (JGI ID# 293293) and two (JGI ID# 487613 and JGI ID# 659555) paralogs of the STAPs JGI ID# 391051 and JGI ID# 659547 are present in the <italic>L. bicolor</italic> genome, but only the products of the latter gene models are capable of transcription activation in the yeast system. No conserved shared domain could be recognized in the STAPs, even though some of them contain sequence motifs (an LL motif in JGI ID# 659547 and a coiled-coil region in JGI ID# 391051, JGI ID# 455116 and JGI ID# 659547) known to mediate protein-protein interactions. Of note, the three STAPs (JGI ID# 391051; JGI ID# 304792; JGI ID# 659547) are expressed at fairly high levels in ECM roots (within the 10% of the genes the most highly expressed), suggesting that they may play an important, but as yet unknown role in symbiosis development.</p></sec></sec><sec id="Sec11"><title>Discussion</title><p id="Par33">This study provides a genome-wide overview of the repertoire of transcriptional activators of the ECM basidiomycete <italic>L. bicolor</italic> and its regulation during symbiosis development. The latter is a complex multistep process involving a series of sequential morphological changes, with a substantial cell wall remodelling, but also an attenuation (and avoidance) of the host plant defense systems and an extensive metabolic reprogramming.</p><p id="Par34">A total of 285 TFs were <italic>in silico</italic> predicted in the genome assembly v2.0, classified according to their DBDs, and compared with the TFs of 70 fungal species with different lifestyles and taxonomic designations. In accordance with previous data [<xref ref-type="bibr" rid="CR67">67</xref>], the three most abundant TF families are those containing C2H2 zinc-finger (PF00096), Zn2/Cys6 Zn-cluster (PF00172) and fungal-specific (PF04280) DNA binding domains. The number of Zn-cluster and fungal-specific TFs is higher in species belonging to the phylum Ascomycota compared to species of the phylum Basidiomycota. Prevalence of Homeobox, GATA, HSF and HMG-box TF families is slightly higher in the latter group of fungi. Only one third of the predicted <italic>L. bicolor</italic> TFs is homologous to known TFs. This rather small fraction of homologs may reflect the preponderance of transcription factors functionally characterized in model Ascomycetes such as <italic>N. crassa</italic> and <italic>A. nidulans</italic>.</p><p id="Par35">TF transcript profiling at different stages of Douglas fir and poplar mycorrhizae development identified a core set of differentially expressed transcription factors. One of the most upregulated TFs in this set is LbRlm1–2 (JGI ID# 302141), a MADS box transcription factor involved in cell wall integrity maintenance and invasive growth [<xref ref-type="bibr" rid="CR17">17</xref>, <xref ref-type="bibr" rid="CR24">24</xref>, <xref ref-type="bibr" rid="CR72">72</xref>] that is required for pathogenicity in the plant pathogens <italic>Magnaporthe oryzae</italic> [<xref ref-type="bibr" rid="CR43">43</xref>] and <italic>Botrytis cinerea</italic> [<xref ref-type="bibr" rid="CR75">75</xref>], as well as in the human pathogen <italic>Aspergillus fumigatus</italic> [<xref ref-type="bibr" rid="CR58">58</xref>]. In both <italic>M. oryzae</italic> and <italic>A. fumigatus</italic>, <italic>Rlm1</italic> mutants are impaired in invasive growth, with an altered expression of multiple genes coding for cell-wall associated protein. Root apoplastic space invasion by colonizing hyphae is a key step in Hartig net development and in the formation of a symbiotic interface composed of cell wall polysaccharides from the fungus and the host plant [<xref ref-type="bibr" rid="CR13">13</xref>, <xref ref-type="bibr" rid="CR45">45</xref>]. Indeed, multiple transcripts coding for secreted glycosyl hydrolases likely involved in plant and fungal cell wall remodeling are differentially expressed during ECM development in <italic>L. bicolor</italic> [<xref ref-type="bibr" rid="CR71">71</xref>]. It is thus conceivable to imagine a role for LbRlm1–2 in the regulation of fungal genes coding for glycohydrolytic enzymes shaping the symbiotic interfacial matrix. Rlm1 orthologs are similarly upregulated in the ECMs of the closely related Agaricales <italic>A. muscaria</italic> and <italic>H. cylindrosporum</italic>, whereas the corresponding ortholog in the mycorrizal ascomycete <italic>T. melanosporum</italic> (<italic>TmelRlmA</italic>) is expressed at high levels but not regulated [<xref ref-type="bibr" rid="CR44">44</xref>]. This suggests that different regulatory strategies may be used by different ECM fungi to accomplish overall similar developmental programs.</p><p id="Par36">Despite the central role of nutrient exchange in ECM symbiosis, expression of TFs known to regulate nutrient uptake and assimilation is generally not regulated during ECM development. Expression of those genes could be very localized or very transiently activated as previously shown for nutrient transporter expression [<xref ref-type="bibr" rid="CR19">19</xref>]. As we harvested entire ECM root tips, it is thus possible that RNAs corresponding to TF genes are diluted. In addition, it is worth to note that we compare expression level between in vitro free-living mycelium (except for <italic>P. involutus</italic> for which extramatricial patches were harvested) and ECM root tips. However, media for fungal growth and ECM production as well as host-plants are all-different due to different needs from both fungal and plant sides. It could be a reason explaining why we did not find TF-related to nutrition commonly regulated in all symbiotic tissues. Notwithstanding this, the <italic>L. bicolor</italic> homolog of CreA, a transcription factor involved in glucose-mediated carbon catabolite repression in various fungi [<xref ref-type="bibr" rid="CR9">9</xref>], is strongly up-regulated at a late stage of mycorrhiza formation, when the Hartig net is well differentiated and actively engaged in nutrient exchange and is similarly modulated in <italic>A. muscaria</italic> and <italic>C. geophilum</italic>. In this context, LbCreA, likely represses the expression of genes coding for polysaccharide degrading enzymes such as cellulases and hemicellulases. Upregulation of <italic>LbCreA</italic> at a late stage of ECM development might correlate with the arrest of cell wall remodelling by endoglucanases, polygalacturonate lyases and pectate lyases [<xref ref-type="bibr" rid="CR71">71</xref>].</p><p id="Par37">Another member of the core set of ECM-regulated TFs is the ortholog of the <italic>A. nidulans</italic> regulatory protein AbaA, which is similarly upregulated in the Agaricales <italic>A. muscaria</italic> and <italic>H. cylindrosporum</italic>, but not in other mycorrhizal fungi. First identified in <italic>A. nidulans</italic> as a regulatory protein required for conidiophore development and maturation [<xref ref-type="bibr" rid="CR1">1</xref>], AbaA was subsequently shown to be also involved in mycotoxin production, autolysis and cell death [<xref ref-type="bibr" rid="CR60">60</xref>]. The latter functions suggest a possible role of this TF in the maintenance/turnover of colonizing hyphae as well as in secondary metabolism, at least within the Agaricales.</p><p id="Par38">Three ECM-upregulated TFs display similarities with <italic>N. crassa Acu15</italic> [<xref ref-type="bibr" rid="CR2">2</xref>] and <italic>A. nidulans FacB</italic> [<xref ref-type="bibr" rid="CR66">66</xref>], which regulate lipid metabolism in these fungi. Two other related regulators are <italic>M. oryzae</italic> FAR1 and FAR2, which are responsible for differential expression of genes involved in fatty acid β-oxidation, acetyl-CoA translocation, peroxisomal biogenesis, and the glyoxylate cycle in response to lipid availability [<xref ref-type="bibr" rid="CR3">3</xref>]. Interestingly, the FacB/Acu15 homologues of the mycorrhizal basidiomycetes <italic>A. muscaria, P. involutus, S. luteus</italic> and <italic>P. croceum</italic> are also upregulated in symbiotic tissues, suggesting that controlled expression of fatty acid/lipid metabolism genes is causally linked to ECM development.</p><p id="Par39">Five TF genes downregulated during mycorrhiza formation in <italic>L. bicolor</italic> and in at least four additional ECM basidiomycetes (<italic>A. muscaria, H. cylindrosporum</italic>, <italic>S. luteus</italic> and <italic>P. involutus</italic>) but not in other plant-symbiotic fungi, are homologous to sexual development regulators. The closest matches are <italic>Moc3</italic>, which positively regulates mating efficiency in <italic>S. pombe</italic> [<xref ref-type="bibr" rid="CR18">18</xref>], <italic>Fst4,</italic> a positive regulator of mushroom development in <italic>Schizophyllum commune</italic> [<xref ref-type="bibr" rid="CR47">47</xref>]; and <italic>Prf1</italic>, a pheromone response factor coordinating filamentous growth in <italic>U. maydis</italic> [<xref ref-type="bibr" rid="CR21">21</xref>].</p><p id="Par40"><italic>In silico </italic>TF annotation was at least in part confirmed by the results obtained with the yeast TAT assay. This screen allowed the functional validation of 16 <italic>in silico</italic> predicted TFs as transcriptional activators and the identification of two DBD-containing activators that were not retrieved from <italic>in silico</italic> analysis. The fraction of TAT-validated <italic>Laccaria</italic> TFs is significantly lower (~6%) than that obtained in <italic>T. melanosporum</italic> (20%; [<xref ref-type="bibr" rid="CR44">44</xref>]) and in the homologous <italic>S. cerevisiae</italic> system (40%, [<xref ref-type="bibr" rid="CR65">65</xref>]), using similar numbers of assayed transformants. Even though ADs are known to be poorly structured and quite permissive to sequence variations, this relatively low validation rate might be explained by a more marked divergence of basidiomycete (<italic>Laccaria</italic>) TFs from the prototypic amino acid composition of ascomycete (yeast and <italic>Tuber</italic>) activation domains [<xref ref-type="bibr" rid="CR65">65</xref>]. TAT-validated TFs were generally highly expressed and three of them belonged to the core set of ECM-regulated transcription factors (one upregulated and two downregulated).</p><p id="Par41">In addition to fungal TFs, the TAT screen allowed the functional validation of 61 <italic>in silico</italic> predicted TFs from the host plant <italic>P. trichocarpa</italic>. Most of these TFs belong to the ERF, Myb, NAC, WRKY or EINL families of plant transcription factors, many members of which are known to be involved in the regulation of defense reactions during plant-microbe interaction [<xref ref-type="bibr" rid="CR46">46</xref>, <xref ref-type="bibr" rid="CR59">59</xref>, <xref ref-type="bibr" rid="CR64">64</xref>]. Mycorrhiza-induced plant TFs identified by the TAT screen of the ECM cDNA library are likely playing an important role in the control of plant responses to fungal colonisation and thus represent high-priority candidates for future more detailed functional analyses.</p><p id="Par42">The TAT screening also uncovered novel putative fungal activators lacking a DNA binding domain, some of which (e.g., Ede1 and Rsp5) were also identified as “unconventional activators” in <italic>T. melanosporum</italic> [<xref ref-type="bibr" rid="CR44">44</xref>]. Although quite a few false-positives may be expected due to the presence of a vector-borne NLS that can force the nuclear localization of otherwise cytoplasmic proteins, the occurrence of nuclear moonlighting proteins (capable of a dual function, both in the cytoplasm and in the nucleus) is in line with recent findings in yeast and other micro-organisms [<xref ref-type="bibr" rid="CR20">20</xref>, <xref ref-type="bibr" rid="CR22">22</xref>]. The latter include the ECM ascomycete <italic>T. melanosporum</italic>, in which a cytosolic sulfur metabolic enzyme has been shown to be capable of autonomous nuclear translocation and transcriptional activation in the heterologous host <italic>S. cerevisae</italic> [<xref ref-type="bibr" rid="CR31">31</xref>].</p><p id="Par43">Of particular interest is the identification, among the “unconventional activators” of the NLS-containing Secreted Transcriptional Activator Proteins. These are reminiscent of the <italic>L. bicolor</italic> effectors Mycorrhiza-induced Small Secreted Proteins [<xref ref-type="bibr" rid="CR33">33</xref>, <xref ref-type="bibr" rid="CR53">53</xref>, <xref ref-type="bibr" rid="CR54">54</xref>], one of which (MiSSP7) has been shown to be secreted by the fungus, imported into plant cells through endocytosis and relocalized to the nucleus, where it interacts with, and negatively regulates, the jasmonate pathway co-receptor JAZ6 to attenuate host defence responses [<xref ref-type="bibr" rid="CR51">51</xref>]. Similar to MiSSPs, the expression levels of the STAPs genes are particularly elevated in ECM root tips. In contrast with MiSSPs, however, STAPs are expressed at high levels also in free-living mycelium, suggesting a role for these proteins also in vegetative growth. Another characteristic MiSSPS and STAPs have in common is their lack of orthologs in other mycorrhizal or non-mycorrhizal fungi. The sole exception was <italic>Laccaria amethystina</italic>, a close relative of <italic>L. bicolor</italic>, indicating that STAPs are largely unique, and at best clade<italic>-</italic>specific, proteins. Although additional data are required to better delineate the in vivo function of these proteins, it is tempting to speculate that STAPs may represent a novel class of intercellularly trafficked transcriptional regulators that may act on the symbiotic plant partner, but, perhaps, also on surrounding fungal hyphae and on other rhizosphere microbes.</p></sec><sec id="Sec12"><title>Conclusions</title><p id="Par44">We identify <italic>L. bicolor</italic> TF regulome, which contains TF-genes commonly regulated in both ectomycorrhizal root tips with two distinct host plants, one Angiosperm (<italic>Populus</italic>) and one Gymnosperm (Douglas fir). We provide evidence that each ECM fungi use its own set of TFs to integrate exogenous signals and drive transcriptional changes leading to ECM development. This could be explained that despite similar morphological changes to occur, the signals could be highly variable in their nature requiring specific TFs to combine them. Nevertheless, keeping in mind the extreme species-specificity of the regulators employed by different ECM fungi to implement an ultimately quite similar symbiotic program, ECM-regulated TFs identified in this work require further investigation, particularly with regard to the gene networks they control. The TAT screening also allowed the isolation of protein without a DNA binding site. These components, especially those without a prior record of nuclear localization and activity, represent a significant outcome of this work. This points to the existence of an as yet largely unexplored set of “hard to predict” transcriptional regulators, as the new class of NLS-bearing, secreted proteins, so-called STAPs. STAPs were not up regulated during ECM development and their constitutive high expression may reflect a role in controlling competing rhizospheric microbes. Therefore, STAPs could be a new class of effectors secreted by <italic>L. bicolor</italic> to control the host plant gene expression during ECM development and/or competing rhizospheric microbes.</p></sec><sec id="Sec13"><title>Methods</title><sec id="Sec14"><title>Microorganism and plant material</title><p id="Par45"><italic>Saccharomyces cerevisiae</italic> strain MaV103 (MATa, <italic>leu</italic>2–3112, <italic>trp</italic>1–901, <italic>his</italic>3∆200, <italic>ade</italic>2–101, <italic>gal</italic>4∆, <italic>gal</italic>80∆, <italic>SPAL</italic>10<italic>::URA</italic>3, <italic>GAL</italic>1::<italic>lac</italic>Z, <italic>HIS</italic>3UASGAL1<italic>::HIS</italic>3@<italic>LYS</italic>2, <italic>can</italic>1R, <italic>cyh</italic>2R) was propagated on YAPD medium (1% yeast extract, 2% peptone, 2% glucose, and 40 mg/L adenine) and cultured at 30 °C.</p><p id="Par46">The <italic>Populus trichocarpa – Laccaria bicolor</italic> and <italic>Douglas</italic> fir- <italic>Laccaria bicolor</italic> ECM root tips were obtained as described in [<xref ref-type="bibr" rid="CR55">55</xref>].</p></sec><sec id="Sec15"><title>Bioinformatic predictions and annotations of TF</title><p id="Par47">Fungal genome assemblies and annotations used in this study are available via the JGI fungal genome portal MycoCosm (<ext-link ext-link-type="uri" xlink:href="http://jgi.doe.gov/fungi">http://jgi.doe.gov/fungi</ext-link>) (Additional file <xref rid="MOESM2" ref-type="media">2</xref>: Table S2). Each DNA-binding domains (DBD) of eukaryotic transcription factors is related to a pfam domain, used in combination with other DBD-characteristiscs to classify transcription factors (TFs). Searching for proteins having a TF specific pfam domain retrieved TFs from <italic>L. bicolor</italic> and the other fungi. Functional annotations were performed using BLASTP (<ext-link ext-link-type="uri" xlink:href="https://blast.ncbi.nlm.nih.gov/Blast.cgi">https://blast.ncbi.nlm.nih.gov/Blast.cgi</ext-link>) search against the nr database from the National Center for Biotechnology Information (NCBI) with a threshold e-value of 10<sup>−5</sup>. Best hits associated with experimentally characterization and/or publications were reported. The presence of NLS and coiled coil regions were inferred with PSORT II prediction at <ext-link ext-link-type="uri" xlink:href="http://psort1.hgc.jp/">http://psort1.hgc.jp/</ext-link>. N-terminal signal peptides and cleavage sites were predicted using SignalP at <ext-link ext-link-type="uri" xlink:href="http://www.cbs.dtu.dk/services/SignalP/">http://www.cbs.dtu.dk/services/SignalP/</ext-link>. To further confirm that the sequence similarity with experimentally characterised TFs was not limited to the highly conserved DBD, BLAST analysis was also performed masking the query DBD (see [<xref ref-type="bibr" rid="CR32">32</xref>, <xref ref-type="bibr" rid="CR44">44</xref>] for further details). Results summarising the outcome of this analysis (i.e. the query is still similar to experimentally characterised TFs) are shown in Additional file <xref rid="MOESM1" ref-type="media">1</xref>: Table S1.</p></sec><sec id="Sec16"><title>Transcript profiling of TF-encoding genes in ECM</title><p id="Par48">To retrieve expression data on ectomycorrhizal root tips for different mutualistic interactions, we used the complete expression datasets published and available as series at the Gene Expression Omnibus at the National Center for Biotechnology Information website (<ext-link ext-link-type="uri" xlink:href="http://www.ncbi.nlm.nih.gov/geo">http://www.ncbi.nlm.nih.gov/geo/</ext-link>). <italic>L. bicolor- P. trichocarpa, L-bicolor- Douglas</italic> fir time course experiments are available under GSE62225 and GSE62226 accession numbers [<xref ref-type="bibr" rid="CR55">55</xref>]. Expression data for <italic>A. muscaria- Populus tremula x tremuloides</italic>, <italic>H. cylindrosporum- Pinus pinaster</italic>, <italic>P. involutus- Betula pendula</italic>, <italic>P. croceum- Quercus robur</italic>, <italic>S. luteus- Pinus sylvestris</italic> ectomycorrhizal root tips, <italic>T. calospora- Serapias vomeracea</italic> mycorrhizal protocorms, <italic>O. maius- Vaccinium myrtillus</italic> mycorrhizal roots and <italic>S. vermifera- Arabidopsis thaliana</italic> mycorrhizal roots are published in [<xref ref-type="bibr" rid="CR26">26</xref>] and available at GSE63947 accession number. Expression data of <italic>C. geophilum- P. sylvestris</italic> are available under GSE83909 accession number [<xref ref-type="bibr" rid="CR48">48</xref>]. Expression data of <italic>T. melanospsorum</italic>- hazelnut ECM are available under GSE17529 accession number [<xref ref-type="bibr" rid="CR35">35</xref>]. In all cases, only transcription factors significantly regulated (up- or down-regulation ≥ or ≤2.5 fold, Benjamini Hochberg, modified t-test <italic>p</italic>-value <0.05,) were considered for the comparative analysis. When microarray data were used, only transcription factors with an expression ≥200 (arbitrary units) in at least one of the condition tested were retained. For <italic>L. bicolor</italic> time course, clustering of the transcription factors with significant regulation was performed manually, according to their expression pattern throughout the time-course and explained for each cluster in the results section. Data were normalized using log transformation with a Log base of 2 and the heat maps were generated using the pheatmap package in R [<xref ref-type="bibr" rid="CR27">27</xref>].</p></sec><sec id="Sec17"><title>Quantitative real-time qPCR</title><p id="Par49">cDNA was generated from 500 ng total RNA samples using the i-Script cDNA reverse transcription kit from Biorad. Real-time PCR reactions were prepared using SYBR Green Kit (Biorad) including 10 ng cDNA and 300 nM forward and reverse primer in each reaction. PCR was performed in the RotorGene (Qiagen) with the standard cycle conditions: 95 °C for 3 min; 40 cycles at 95 °C for 15 s and 65 °C for 30 s, followed by a melting curve analysis (temperature range from 65 °C to 95 °C with 0.5 °C increase every 10s) A no template control, containing H<sub>2</sub>O instead of cDNA, was included. Transcript abundance was normalized using <italic>L. bicolor</italic> histone H4 (JGI ID# 319764) and ubiquitin (JGI ID #446085) -encoding genes. Stability of the reference genes was validated using GeNorm. The ratios of expression between two conditions were calculated using Pfaffl et al. 2011 method. The primer pairs for each gene are in Additional file <xref rid="MOESM8" ref-type="media">8</xref>: Table S8. The amplification efficiency (E) was experimentally measured for each primer pair (Additional file <xref rid="MOESM8" ref-type="media">8</xref>: Table S8). Three independent biological replicates were run in duplicate for each experimental condition.</p></sec><sec id="Sec18"><title>cDNA libraries construction</title><p id="Par50">cDNA libraries were constructed as reported in Plett et al., [<xref ref-type="bibr" rid="CR53">53</xref>, <xref ref-type="bibr" rid="CR54">54</xref>]. Briefly, total RNA (500 μg per sample) was prepared from <italic>L. bicolor</italic> fruiting bodies (FB), free-living mycelium (FLM) of <italic>L. bicolor</italic> (strain S238 N) grown in P5 liquid Pachlewski medium for 3 weeks, <italic>L. bicolor</italic> mycorrhiza root tips and non mycorrhiza roots tips of <italic>Populus trichocarpa</italic> during a time course of symbiosis development (2, 4, 6 and 12 weeks). RNA extraction was performed using the RNeasy Plant Mini Kit (Qiagen) (for mycorrhiza and non-mycorrhiza root tips, buffer RLC containing 20 mg ml<sup>−1</sup> of PEG 8000 was used), followed by a DNase I treatment. Total mRNA were purified using Oligotex columns (Qiagen) and used to build FB + FLM and ECM + Roots cDNA libraries with the CloneMiner cDNA Library Construction Kit (Invitrogen), starting from 2 μg and 500 ng of purified total RNA, respectivley. Entry cDNA libraries were then transferred to the yeast-expressible pDEST32 vector using the Gateway system (ProQuest Two-Hybrid System kit, Invitrogen).</p></sec><sec id="Sec19"><title>Transcriptional activator trap assays</title><p id="Par51">Yeast strain MaV103 harboring three Gal4-dependent reporter genes (<italic>LacZ, HIS3 </italic>and <italic>URA3</italic>), was transformed with 20 μg of each pDEST32 cDNA library and plated onto twenty Petri dishes (150 mm diameter) on selective medium (SD-Leu-His) containing 25 mM 3-amino-1, 2, 4-triazole (3AT). About 1.7, 2, and 0.8 million colonies were screened for <italic>Laccaria</italic> FLM/FB, ECM, and Root library, respectively. Colonies growing on SD-Leu-His +3AT were individually transferred to 384-well SD-Leu plates using a 384-multipinner device (V&P). To eliminate false positive and evaluate the strength of the interaction, clones collected for their growth on –His + 3AT in the initial screen were replicated to test for the expression of 3 reporter genes (<italic>LacZ</italic>, <italic>HIS3</italic> and <italic>URA3</italic>) as described [<xref ref-type="bibr" rid="CR44">44</xref>, <xref ref-type="bibr" rid="CR53">53</xref>, <xref ref-type="bibr" rid="CR54">54</xref>]. Transcriptional activator trap-positive clones are defined as colonies that scored positive to the three reporter genes (about 200 colonies for each library). Corresponding DNA sequences were first trimmed and used as queries for a BLASTX search against the <italic>L. bicolor</italic> and <italic>P. trichocarpa</italic> proteomes at the NCBI and a gene model was assigned to each sequence if the identity was >95%. We checked manually DNA sequences corresponding to the same gene model and included them in contig sequences.</p></sec></sec><sec sec-type="supplementary-material"><title>Additional files</title><sec id="Sec20"><p><supplementary-material content-type="local-data" id="MOESM1"><media xlink:href="12864_2017_4114_MOESM1_ESM.xlsx"><label>Additional file 1: Table S1.</label><caption><p>List of <italic>L. bicolor</italic> TFs identified <italic>in silico</italic> displaying similarities with characterized TFs (183 proteins); sharing similarities with predicted or hypothetical proteins with no proved role as transcriptional regulators (94 proteins); sharing similarities with proteins identified as transcriptional regulators without DBD (8 proteins). General information of protein is given (e.g., protein ID from both <italic>L. bicolor</italic> genome version 1 and version 2, length of the polypeptide, TF name, EST support). Accession number, Description, Species, % identity, E-value and Score are related to BLAST results using <italic>L. bicolor</italic> protein as query against fungal NCBI database. m.c. = manually curated. Best Blast reciprocal hit = “YES” indicates that the TF was positive to the Best reciprocal hit analysis. BLAST masked DBD = “YES” indicates that <italic>L. bicolor</italic> TF was still similar to the characterized protein after masking its DBD in a BLAST search. See Methods section for a detailed description. TFs retrieved from and functionally validated by the TAT screen are in bold. (XLSX 48 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM2"><media xlink:href="12864_2017_4114_MOESM2_ESM.xlsx"><label>Additional file 2: Table S2.</label><caption><p>Number of proteins within each TF family for 70 fungal genomes. Data used to generate Fig. <xref rid="Fig1" ref-type="fig">1</xref>. (XLSX 32 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM3"><media xlink:href="12864_2017_4114_MOESM3_ESM.xlsx"><label>Additional file 3: Table S3.</label><caption><p>Gene expression of <italic>L. bicolor</italic> TF-encoding genes that are significantly regulated during ECM development with <italic>Populus trichocarpa</italic> at 2, 4, 6 and/or 12 weeks. Data used to generate Fig. <xref rid="Fig2" ref-type="fig">2b</xref>. (XLSX 26 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM4"><media xlink:href="12864_2017_4114_MOESM4_ESM.xlsx"><label>Additional file 4: Table S4.</label><caption><p>Gene expression of <italic>L. bicolor</italic> TF-encoding genes that are significantly regulated during ECM development with <italic>Pseudotsuga menziesii</italic> at 2, 4 and/or 6 weeks. Data used to generate Fig. <xref rid="Fig3" ref-type="fig">3</xref>. (XLSX 18 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM5"><media xlink:href="12864_2017_4114_MOESM5_ESM.xlsx"><label>Additional file 5: Table S5.</label><caption><p>List and expression level of TF-encoding genes significantly up or downregulated in various mutualistic interaction (expression ratio > 2.5 folds and FDR or BH modified t-test < 0.05): <bold>A</bold>. <italic>A. muscaria- Populus tremula x tremuloides.</italic><bold>B</bold><italic>. C. geophilum- Pinus sylvestris</italic><bold>C.</bold><italic>H. cylindrosporum- Pinus pinaster</italic><bold>D.</bold><italic>P. involutus- Betula pendula</italic><bold>E.</bold><italic>P. croceum-Quercus robur</italic><bold>F.</bold><italic>S. luteus- Pinus</italic><bold>G.</bold><italic>T. melanospsorum</italic>- <italic>C. avellana</italic><bold>H.</bold><italic>S. vermifera- Arabidopsis thaliana</italic><bold>I.</bold><italic>T. calospora- Serapias vomeracea</italic><bold>J.</bold><italic>O. maius- Vaccinium myrtillus</italic>. (XLSX 66 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM6"><media xlink:href="12864_2017_4114_MOESM6_ESM.xlsx"><label>Additional file 6: Table S6.</label><caption><p>List of <italic>L. bicolor</italic> “core” TF orthologues genes in ECM fungi (<italic>A. muscaria; H. cylindrosporum; P. involutus, P. croceum, S. luteus, C. geophilum</italic> and <italic>T. melanospsorum</italic>). The shaded rows indicate orthologues (using Reciprocal Blast Hit) of <italic>L. bicolor</italic> TFs, which are up or downregulated in symbiotic tissues. (XLSX 25 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM7"><media xlink:href="12864_2017_4114_MOESM7_ESM.xlsx"><label>Additional file 7: Table S7.</label><caption><p>List of <italic>P. trichocarpa</italic> TFs, unconventional activators and putative unconventional activators retrieved from, and functionally validated by, the TAT screen of ECM and Roots libraries. For each gene, additional information (e.g. number of clones retrieved, name and other characteristics of the most informative best hit obtained from a BLASTX search carried out in GenBank, IPR domain if any) is reported. (XLSX 27 kb)</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM8"><media xlink:href="12864_2017_4114_MOESM8_ESM.xlsx"><label>Additional file 8: Table S8.</label><caption><p>List and sequences of primers used for qPCR. (XLSX 9 kb)</p></caption></media></supplementary-material></p></sec></sec></body><back><glossary><title>Abbreviations</title><def-list><def-item><term>3AT</term><def><p id="Par4">3-amino-1,2,4-triazole</p></def></def-item><def-item><term>DBD</term><def><p id="Par5">DNA-binding domain</p></def></def-item><def-item><term>ECM</term><def><p id="Par6">Ectomycorrhiza</p></def></def-item><def-item><term>TAT</term><def><p id="Par7">Transcriptional activator trap</p></def></def-item><def-item><term>TF</term><def><p id="Par8">Transcription factor</p></def></def-item></def-list></glossary><fn-group><fn><p><bold>Electronic supplementary material</bold></p><p>The online version of this article (10.1186/s12864-017-4114-7) contains supplementary material, which is available to authorized users.</p></fn></fn-group><ack><title>Acknowledgements</title><p>The authors thank the U.S. Department of Energy Joint Genome Institute and members of the Mycorrhizal Genomics Initiative consortium for access to unpublished genome sequences.</p><sec id="FPar1"><title>Fundings</title><p id="Par52">YD was supported by a Ph.D. scholarship from the French Ministère de la Recherche et de la Technologie. JR was an AgreenSkills Marie Sklodowska Curie postdoctoral fellow co-funded by the European Commission (FP7–267196). This research was sponsored by the Laboratory of Excellence ARBRE (ANR-12-LABX-0002_ARBRE), the Oak Ridge National Laboratory Genomic Science Program, U.S. Department of Energy, Office of Science – Biological and Environmental Research as part of the Plant Microbe Interfaces Scientific Focus Area and the Region Lorraine (to FM). This study was part of the PhD thesis of EL, whose post-doctoral work was supported by a fellowship from the Italian Interuniversity Consortium for Biotechnologies (CIB). Financial support by the University of Parma (local funding, FIL program) to BM and SO is also gratefully acknowledged. The funding bodies did not participate in any of the study design, data collection and analysis, or writing the manuscript.</p></sec><sec id="FPar2"><title>Avaibility of data and materials</title><p id="Par53">All data generated or analysed during this study are included in this published article and its supplementary information files.</p></sec></ack><notes notes-type="author-contribution"><title>Authors’ contributions</title><p>YD, CVF, AB, BM, SO and FM designed the study. YD, EL, JR, CVF performed the experiments. YD, EL, ET, BM, EM, AK, and CVF analysed the data. YD, CVF, EL, BM, SO and FM edited the manuscript. All the authors read and approved the final version of the manuscript.</p></notes><notes notes-type="COI-statement"><sec id="FPar3"><title>Ethics approval and consent to participate</title><p id="Par54"><italic>Populus trichocarpa</italic> derived from cuttings, clone 10,174, Orléans, France. Robin pépinières (France) provided <italic>Pseudotsuga menziesii</italic> seeds. <italic>Laccaria bicolor</italic> S238 N strain was selected and is maintained at Centre INRA Grand-Est (UMR 1136).</p></sec><sec id="FPar4"><title>Consent for publication</title><p id="Par55">Not applicable.</p></sec><sec id="FPar5"><title>Competing interests</title><p id="Par56">The authors declare that they have no competing interests.</p></sec><sec id="FPar6"><title>Publisher’s Note</title><p id="Par57">Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p></sec></notes><ref-list id="Bib1"><title>References</title><ref id="CR1"><label>1.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Andrianopoulos</surname><given-names>A</given-names></name><name><surname>Timberlake</surname><given-names>WE</given-names></name></person-group><article-title>The <italic>Aspergillus nidulans</italic> abaA gene encodes a transcriptional activator that acts as a genetic switch to control development</article-title><source>Mol Cell Biol</source><year>1994</year><volume>14</volume><issue>4</issue><fpage>2503</fpage><lpage>2515</lpage><pub-id pub-id-type="doi">10.1128/MCB.14.4.2503</pub-id><pub-id pub-id-type="pmid">8139553</pub-id></element-citation></ref><ref id="CR2"><label>2.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Bibbins</surname><given-names>M</given-names></name><name><surname>Crepin</surname><given-names>VF</given-names></name><name><surname>Cummings</surname><given-names>NJ</given-names></name><name><surname>Mizote</surname><given-names>T</given-names></name><name><surname>Baker</surname><given-names>K</given-names></name><name><surname>Mellits</surname><given-names>KH</given-names></name><name><surname>Connerton</surname><given-names>IF</given-names></name></person-group><article-title>A regulator gene for acetate utilisation from <italic>Neurospora crassa</italic></article-title><source>Mol Gen Genomics</source><year>2002</year><volume>267</volume><issue>4</issue><fpage>498</fpage><lpage>505</lpage><pub-id pub-id-type="doi">10.1007/s00438-002-0682-5</pub-id></element-citation></ref><ref id="CR3"><label>3.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Bin Yusof</surname><given-names>MT</given-names></name><name><surname>Kershaw</surname><given-names>MJ</given-names></name><name><surname>Soanes</surname><given-names>DM</given-names></name><name><surname>Talbot</surname><given-names>NJ</given-names></name><name><surname>Zhang</surname><given-names>Z</given-names></name></person-group><article-title>FAR1 and FAR2 Regulate the Expression of Genes Associated with Lipid Metabolism in the Rice Blast Fungus Magnaporthe oryzae</article-title><source>PLoS ONE</source><year>2014</year><volume>9</volume><issue>6</issue><fpage>e99760</fpage><pub-id pub-id-type="doi">10.1371/journal.pone.0099760</pub-id><pub-id pub-id-type="pmid">24949933</pub-id></element-citation></ref><ref id="CR4"><label>4.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Brown</surname><given-names>AJ</given-names></name><name><surname>Casselton</surname><given-names>LA</given-names></name></person-group><article-title>Mating in mushrooms: increasing the chances but prolonging the affair</article-title><source>Trends Genet</source><year>2001</year><volume>17</volume><issue>7</issue><fpage>393</fpage><lpage>400</lpage><pub-id pub-id-type="doi">10.1016/S0168-9525(01)02343-5</pub-id><pub-id pub-id-type="pmid">11418220</pub-id></element-citation></ref><ref id="CR5"><label>5.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Brundrett</surname><given-names>MC</given-names></name></person-group><article-title>Coevolution of roots and mycorrhizas of land plants</article-title><source>New Phytol</source><year>2002</year><volume>154</volume><fpage>275</fpage><lpage>304</lpage><pub-id pub-id-type="doi">10.1046/j.1469-8137.2002.00397.x</pub-id></element-citation></ref><ref id="CR6"><label>6.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Burgess</surname><given-names>T</given-names></name><name><surname>Dell</surname><given-names>B</given-names></name><name><surname>Malajczuk</surname><given-names>N</given-names></name></person-group><article-title>Variation in mycorrhizal development and growth stimulation of 20 isolates of <italic>Pisolithus</italic> inoculated onto <italic>Eucalyptus grandis</italic> W. Hill ex Maiden</article-title><source>New Phytol</source><year>1994</year><volume>127</volume><fpage>731</fpage><lpage>739</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.1994.tb02977.x</pub-id></element-citation></ref><ref id="CR7"><label>7.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Chang</surname><given-names>YC</given-names></name><name><surname>Wright</surname><given-names>LC</given-names></name><name><surname>Tscharke</surname><given-names>RL</given-names></name><name><surname>Sorrell</surname><given-names>TC</given-names></name><name><surname>Wilson</surname><given-names>CF</given-names></name><name><surname>Kwon-Chung</surname><given-names>KJ</given-names></name></person-group><article-title>Regulatory roles for the homeodomain and C2H2 zinc finger regions of <italic>Cryptococcus neoformans</italic> Ste12αp</article-title><source>Mol Microbiol</source><year>2004</year><volume>53</volume><issue>5</issue><fpage>1385</fpage><lpage>1396</lpage><pub-id pub-id-type="doi">10.1111/j.1365-2958.2004.04188.x</pub-id><pub-id pub-id-type="pmid">15387817</pub-id></element-citation></ref><ref id="CR8"><label>8.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Cleary</surname><given-names>IA</given-names></name><name><surname>Mulabagal</surname><given-names>P</given-names></name><name><surname>Reinhard</surname><given-names>SM</given-names></name><name><surname>Yadev</surname><given-names>NP</given-names></name><name><surname>Murdoch</surname><given-names>C</given-names></name><name><surname>Thornhill</surname><given-names>MH</given-names></name><name><surname>Lazzell</surname><given-names>AL</given-names></name><name><surname>Monteagudo</surname><given-names>C</given-names></name><name><surname>Thomas</surname><given-names>DP</given-names></name><name><surname>Saville</surname><given-names>SP</given-names></name></person-group><article-title>Pseudohyphal regulation by the transcription factor Rfg1p in <italic>Candida albicans</italic></article-title><source>Eukaryot Cell</source><year>2010</year><volume>9</volume><issue>9</issue><fpage>1363</fpage><lpage>1373</lpage><pub-id pub-id-type="doi">10.1128/EC.00088-10</pub-id><pub-id pub-id-type="pmid">20656914</pub-id></element-citation></ref><ref id="CR9"><label>9.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>David</surname><given-names>H</given-names></name><name><surname>Krogh</surname><given-names>AM</given-names></name><name><surname>Roca</surname><given-names>C</given-names></name><name><surname>Akesson</surname><given-names>M</given-names></name><name><surname>Nielsen</surname><given-names>J</given-names></name></person-group><article-title>CreA influences the metabolic fluxes of <italic>Aspergillus nidulans</italic> during growth on glucose and xylose</article-title><source>Microbiology</source><year>2005</year><volume>151</volume><issue>Pt 7</issue><fpage>2209</fpage><lpage>2221</lpage><pub-id pub-id-type="doi">10.1099/mic.0.27787-0</pub-id><pub-id pub-id-type="pmid">16000711</pub-id></element-citation></ref><ref id="CR10"><label>10.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Delaunay</surname><given-names>A</given-names></name><name><surname>Isnard</surname><given-names>AD</given-names></name><name><surname>Toledano</surname><given-names>MB</given-names></name></person-group><article-title>H2O2 Sensing through oxidation of the Yap1 transcription factor</article-title><source>EMBO J</source><year>2000</year><volume>19</volume><issue>19</issue><fpage>5157</fpage><lpage>5166</lpage><pub-id pub-id-type="doi">10.1093/emboj/19.19.5157</pub-id><pub-id pub-id-type="pmid">11013218</pub-id></element-citation></ref><ref id="CR11"><label>11.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Deveau</surname><given-names>A</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Frey-Klett</surname><given-names>P</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete <italic>Laccaria bicolor</italic> S238N</article-title><source>New Phytol</source><year>2008</year><volume>180</volume><issue>2</issue><fpage>379</fpage><lpage>390</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.2008.02581.x</pub-id><pub-id pub-id-type="pmid">18665900</pub-id></element-citation></ref><ref id="CR12"><label>12.</label><mixed-citation publication-type="other">Doré J, Kohler A, Dubost A, Hundley H, Singan V, Peng Y, Kuo A, Grigoriev IV, Martin F, Marmeisse R, Gay AG. The ectomycorrhizal basidiomycete <italic>Hebeloma cylindrosporum</italic> undergoes early waves of transcriptional reprogramming prior to symbiotic structures differentiation. Environ Microbiol. 2017; 10.1111/1462-2920.13670.</mixed-citation></ref><ref id="CR13"><label>13.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Duddridge</surname><given-names>JA</given-names></name><name><surname>Read</surname><given-names>DJ</given-names></name></person-group><article-title>Modification of the host-fungus interface in mycorrhizas synthesised between <italic>Suillus bovinus</italic> Fr O. Kuntz and <italic>Pinus sylvestris</italic> L</article-title><source>New Phytol</source><year>1984</year><volume>96</volume><fpage>583</fpage><lpage>588</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.1984.tb03593.x</pub-id></element-citation></ref><ref id="CR14"><label>14.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Duplessis</surname><given-names>S</given-names></name><name><surname>Courty</surname><given-names>PE</given-names></name><name><surname>Tagu</surname><given-names>D</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>Transcript patterns associated with ectomycorrhiza development in <italic>Eucalyptus globulus</italic> and <italic>Pisolithus microcarpus</italic></article-title><source>New Phytol</source><year>2005</year><volume>165</volume><fpage>599</fpage><lpage>611</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.2004.01248.x</pub-id><pub-id pub-id-type="pmid">15720670</pub-id></element-citation></ref><ref id="CR15"><label>15.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Felten</surname><given-names>J</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Bhalerao</surname><given-names>RP</given-names></name><name><surname>Palme</surname><given-names>K</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Ditengou</surname><given-names>FA</given-names></name><name><surname>Legué</surname><given-names>V</given-names></name></person-group><article-title>The ectomycorrhizal fungus <italic>Laccaria bicolor</italic> stimulates lateral root formation in poplar and <italic>Arabidopsis</italic> through auxin transport and signaling</article-title><source>Plant Physiol</source><year>2009</year><volume>151</volume><issue>4</issue><fpage>1991</fpage><lpage>2005</lpage><pub-id pub-id-type="doi">10.1104/pp.109.147231</pub-id><pub-id pub-id-type="pmid">19854859</pub-id></element-citation></ref><ref id="CR16"><label>16.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Felten</surname><given-names>J</given-names></name><name><surname>Legué</surname><given-names>V</given-names></name><name><surname>Ditengou</surname><given-names>FA</given-names></name></person-group><article-title>Lateral root stimulation in the early interaction between <italic>Arabidopsis thaliana</italic> and the ectomycorrhizal fungus <italic>Laccaria bicolor</italic>: is fungal auxin the trigger?</article-title><source>Plant Signal Behav</source><year>2010</year><volume>5</volume><issue>7</issue><fpage>864</fpage><lpage>867</lpage><pub-id pub-id-type="doi">10.4161/psb.5.7.11896</pub-id><pub-id pub-id-type="pmid">20448463</pub-id></element-citation></ref><ref id="CR17"><label>17.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Fujioka</surname><given-names>T</given-names></name><name><surname>Mizutani</surname><given-names>O</given-names></name><name><surname>Furukawa</surname><given-names>K</given-names></name><name><surname>Sato</surname><given-names>N</given-names></name><name><surname>Yoshimi</surname><given-names>A</given-names></name><name><surname>Yamagata</surname><given-names>Y</given-names></name><name><surname>Nakajima</surname><given-names>T</given-names></name><name><surname>Abe</surname><given-names>K</given-names></name></person-group><article-title>MpkA-dependent and -independent cell wall integrity signaling in <italic>Aspergillus nidulans</italic></article-title><source>Eukaryot Cell</source><year>2007</year><volume>6</volume><issue>8</issue><fpage>1497</fpage><lpage>1510</lpage><pub-id pub-id-type="doi">10.1128/EC.00281-06</pub-id><pub-id pub-id-type="pmid">17601879</pub-id></element-citation></ref><ref id="CR18"><label>18.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Goldar</surname><given-names>MM</given-names></name><name><surname>Jeong</surname><given-names>HT</given-names></name><name><surname>Tanaka</surname><given-names>K</given-names></name><name><surname>Matsuda</surname><given-names>H</given-names></name><name><surname>Kawamukai</surname><given-names>M</given-names></name></person-group><article-title>Moc3, a novel Zn finger type protein involved in sexual development, ascus formation, and stress response of <italic>Schizosaccharomyces pombe</italic></article-title><source>Curr Genet</source><year>2005</year><volume>48</volume><issue>6</issue><fpage>345</fpage><lpage>355</lpage><pub-id pub-id-type="doi">10.1007/s00294-005-0028-z</pub-id><pub-id pub-id-type="pmid">16273369</pub-id></element-citation></ref><ref id="CR19"><label>19.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hacquard</surname><given-names>S</given-names></name><name><surname>Delaruelle</surname><given-names>C</given-names></name><name><surname>Legué</surname><given-names>V</given-names></name><name><surname>Tisserant</surname><given-names>E</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Frey</surname><given-names>P</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Duplessis</surname><given-names>S</given-names></name></person-group><article-title>Laser capture microdissection of uredinia formed by <italic>Melampsora larici-populina</italic> revealed a transcriptional switch between biotrophy and sporulation</article-title><source>Mol Plant-Microbe Interact</source><year>2010</year><volume>23</volume><issue>10</issue><fpage>1275</fpage><lpage>1286</lpage><pub-id pub-id-type="doi">10.1094/MPMI-05-10-0111</pub-id><pub-id pub-id-type="pmid">20831407</pub-id></element-citation></ref><ref id="CR20"><label>20.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hall</surname><given-names>DA</given-names></name><name><surname>Zhu</surname><given-names>H</given-names></name><name><surname>Zhu</surname><given-names>X</given-names></name><name><surname>Royce</surname><given-names>T</given-names></name><name><surname>Gerstein</surname><given-names>M</given-names></name><name><surname>Snyder</surname><given-names>M</given-names></name></person-group><article-title>Regulation of gene expression by a metabolic enzyme</article-title><source>Science</source><year>2004</year><volume>306</volume><issue>5695</issue><fpage>482</fpage><lpage>484</lpage><pub-id pub-id-type="doi">10.1126/science.1096773</pub-id><pub-id pub-id-type="pmid">15486299</pub-id></element-citation></ref><ref id="CR21"><label>21.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hartmann</surname><given-names>HA</given-names></name><name><surname>Kahmann</surname><given-names>R</given-names></name><name><surname>Bölker</surname><given-names>M</given-names></name></person-group><article-title>The pheromone response factor coordinates filamentous growth and pathogenicity in <italic>Ustilago maydis</italic></article-title><source>EMBO J</source><year>1996</year><volume>15</volume><issue>7</issue><fpage>1632</fpage><lpage>1641</lpage><pub-id pub-id-type="pmid">8612587</pub-id></element-citation></ref><ref id="CR22"><label>22.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Hu</surname><given-names>S</given-names></name><name><surname>Xie</surname><given-names>Z</given-names></name><name><surname>Onishi</surname><given-names>A</given-names></name><name><surname>Yu</surname><given-names>X</given-names></name><name><surname>Jiang</surname><given-names>L</given-names></name><name><surname>Lin</surname><given-names>J</given-names></name><name><surname>Rho</surname><given-names>HS</given-names></name><name><surname>Woodard</surname><given-names>C</given-names></name><name><surname>Wang</surname><given-names>H</given-names></name><name><surname>Jeong</surname><given-names>JS</given-names></name><name><surname>Long</surname><given-names>S</given-names></name><name><surname>He</surname><given-names>X</given-names></name><name><surname>Wade</surname><given-names>H</given-names></name></person-group><article-title>Profiling the human protein-DNA Interactome reveals ERK2 as a transcriptional repressor of interferon signaling</article-title><source>Cell</source><year>2009</year><volume>139</volume><issue>3</issue><fpage>610</fpage><lpage>622</lpage><pub-id pub-id-type="doi">10.1016/j.cell.2009.08.037</pub-id><pub-id pub-id-type="pmid">19879846</pub-id></element-citation></ref><ref id="CR23"><label>23.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Johansson</surname><given-names>T</given-names></name><name><surname>Le Quéré</surname><given-names>A</given-names></name><name><surname>Ahren</surname><given-names>D</given-names></name><name><surname>Söderström</surname><given-names>B</given-names></name><name><surname>Erlandsson</surname><given-names>R</given-names></name><name><surname>Lundeberg</surname><given-names>J</given-names></name><name><surname>Uhlén</surname><given-names>M</given-names></name><name><surname>Tunlid</surname><given-names>A</given-names></name></person-group><article-title>Transcriptional responses of <italic>Paxillus involutus</italic> and <italic>Betula pendula</italic> during formation of ectomycorrhizal root tissue</article-title><source>Mol Plant-Microbe Interact</source><year>2004</year><volume>17</volume><issue>2</issue><fpage>202</fpage><lpage>215</lpage><pub-id pub-id-type="doi">10.1094/MPMI.2004.17.2.202</pub-id><pub-id pub-id-type="pmid">14964534</pub-id></element-citation></ref><ref id="CR24"><label>24.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Jung</surname><given-names>US</given-names></name><name><surname>Sobering</surname><given-names>AK</given-names></name><name><surname>Romeo</surname><given-names>MJ</given-names></name><name><surname>Levin</surname><given-names>DE</given-names></name></person-group><article-title>Regulation of the yeast Rlm1 transcription factor by the Mpk1 cell wall integrity MAP kinase</article-title><source>Mol Microbiol</source><year>2002</year><volume>46</volume><issue>3</issue><fpage>781</fpage><lpage>789</lpage><pub-id pub-id-type="doi">10.1046/j.1365-2958.2002.03198.x</pub-id><pub-id pub-id-type="pmid">12410835</pub-id></element-citation></ref><ref id="CR25"><label>25.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kadosh</surname><given-names>D</given-names></name><name><surname>Johnson</surname><given-names>AD</given-names></name></person-group><article-title>Rfg1, a protein related to the <italic>Saccharomyces cerevisiae</italic> hypoxic regulator Rox1, controls filamentous growth and virulence in <italic>Candida albicans</italic></article-title><source>Mol Cell Biol</source><year>2001</year><volume>21</volume><issue>7</issue><fpage>2496</fpage><lpage>2505</lpage><pub-id pub-id-type="doi">10.1128/MCB.21.7.2496-2505.2001</pub-id><pub-id pub-id-type="pmid">11259598</pub-id></element-citation></ref><ref id="CR26"><label>26.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Kuo</surname><given-names>A</given-names></name><name><surname>Nagy</surname><given-names>LG</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Barry</surname><given-names>KW</given-names></name><name><surname>Buscot</surname><given-names>F</given-names></name><name><surname>Canbäck</surname><given-names>B</given-names></name><name><surname>Choi</surname><given-names>C</given-names></name><name><surname>Cichocki</surname><given-names>N</given-names></name><name><surname>Clum</surname><given-names>A</given-names></name><name><surname>Colpaert</surname><given-names>J</given-names></name><name><surname>Copeland</surname><given-names>A</given-names></name><name><surname>Costa</surname><given-names>MD</given-names></name><name><surname>Doré</surname><given-names>J</given-names></name><name><surname>Floudas</surname><given-names>D</given-names></name><name><surname>Gay</surname><given-names>G</given-names></name><name><surname>Girlanda</surname><given-names>M</given-names></name><name><surname>Henrissat</surname><given-names>B</given-names></name><name><surname>Herrmann</surname><given-names>S</given-names></name><name><surname>Hess</surname><given-names>J</given-names></name><name><surname>Högberg</surname><given-names>N</given-names></name><name><surname>Johansson</surname><given-names>T</given-names></name><name><surname>Khouja</surname><given-names>HR</given-names></name><name><surname>LaButti</surname><given-names>K</given-names></name><name><surname>Lahrmann</surname><given-names>U</given-names></name><name><surname>Levasseur</surname><given-names>A</given-names></name><name><surname>Lindquist</surname><given-names>EA</given-names></name><name><surname>Lipzen</surname><given-names>A</given-names></name><name><surname>Marmeisse</surname><given-names>R</given-names></name><name><surname>Martino</surname><given-names>E</given-names></name><name><surname>Murat</surname><given-names>C</given-names></name><name><surname>Ngan</surname><given-names>CY</given-names></name><name><surname>Nehls</surname><given-names>U</given-names></name><name><surname>Plett</surname><given-names>JM</given-names></name><name><surname>Pringle</surname><given-names>A</given-names></name><name><surname>Ohm</surname><given-names>RA</given-names></name><name><surname>Perotto</surname><given-names>S</given-names></name><name><surname>Peter</surname><given-names>M</given-names></name><name><surname>Riley</surname><given-names>R</given-names></name><name><surname>Rineau</surname><given-names>F</given-names></name><name><surname>Ruytinx</surname><given-names>J</given-names></name><name><surname>Salamov</surname><given-names>A</given-names></name><name><surname>Shah</surname><given-names>F</given-names></name><name><surname>Sun</surname><given-names>H</given-names></name><name><surname>Tarkka</surname><given-names>M</given-names></name><name><surname>Tritt</surname><given-names>A</given-names></name><name><surname>Veneault-Fourrey</surname><given-names>C</given-names></name><name><surname>Zuccaro</surname><given-names>A</given-names></name><collab>Mycorrhizal Genomics Initiative Consortium</collab><name><surname>Tunlid</surname><given-names>A</given-names></name><name><surname>Grigoriev</surname><given-names>IV</given-names></name><name><surname>Hibbett</surname><given-names>DS</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists</article-title><source>Nat Genet</source><year>2015</year><volume>47</volume><issue>4</issue><fpage>410</fpage><lpage>415</lpage><pub-id pub-id-type="doi">10.1038/ng.3223</pub-id><pub-id pub-id-type="pmid">25706625</pub-id></element-citation></ref><ref id="CR27"><label>27.</label><mixed-citation publication-type="other">Kolde R. Pheatmap: pretty Heatmaps. R package version 1.0.8. 2015. <ext-link ext-link-type="uri" xlink:href="https://cran.r-project.org/package=pheatmap">https://CRAN.R-project.org/package=pheatmap</ext-link></mixed-citation></ref><ref id="CR28"><label>28.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Larsen</surname><given-names>PE</given-names></name><name><surname>Sreedasyam</surname><given-names>A</given-names></name><name><surname>Trivedi</surname><given-names>G</given-names></name><name><surname>Podila</surname><given-names>GK</given-names></name><name><surname>Cseke</surname><given-names>LJ</given-names></name><name><surname>Collart</surname><given-names>FR</given-names></name></person-group><article-title>Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome</article-title><source>BMC Syst Biol</source><year>2011</year><volume>5</volume><fpage>70</fpage><pub-id pub-id-type="doi">10.1186/1752-0509-5-70</pub-id><pub-id pub-id-type="pmid">21569493</pub-id></element-citation></ref><ref id="CR29"><label>29.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Le Queré</surname><given-names>A</given-names></name><name><surname>Wright</surname><given-names>DP</given-names></name><name><surname>Söderström</surname><given-names>B</given-names></name><name><surname>Tunlid</surname><given-names>A</given-names></name><name><surname>Johansson</surname><given-names>T</given-names></name></person-group><article-title>Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (<italic>Betula pendula</italic> Roth.) and <italic>Paxillus involutus</italic> (Batsch) Fr</article-title><source>Mol Plant-Microbe Interact</source><year>2005</year><volume>18</volume><issue>7</issue><fpage>659</fpage><lpage>673</lpage><pub-id pub-id-type="doi">10.1094/MPMI-18-0659</pub-id><pub-id pub-id-type="pmid">16042012</pub-id></element-citation></ref><ref id="CR30"><label>30.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Lev</surname><given-names>S</given-names></name><name><surname>Hadar</surname><given-names>R</given-names></name><name><surname>Amedeo</surname><given-names>P</given-names></name><name><surname>Baker</surname><given-names>SE</given-names></name><name><surname>Yoder</surname><given-names>OC</given-names></name><name><surname>Horwitz</surname><given-names>BA</given-names></name></person-group><article-title>Activation of an AP1-like transcription factor of the maize pathogen <italic>Cochliobolus heterostrophus</italic> in response to oxidative stress and plant signals</article-title><source>Eukaryot Cell</source><year>2005</year><volume>4</volume><issue>2</issue><fpage>443</fpage><lpage>454</lpage><pub-id pub-id-type="doi">10.1128/EC.4.2.443-454.2005</pub-id><pub-id pub-id-type="pmid">15701806</pub-id></element-citation></ref><ref id="CR31"><label>31.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Levati</surname><given-names>E</given-names></name><name><surname>Sartini</surname><given-names>S</given-names></name><name><surname>Bolchi</surname><given-names>A</given-names></name><name><surname>Ottonello</surname><given-names>S</given-names></name><name><surname>Montanini</surname><given-names>B</given-names></name></person-group><article-title>Moonlighting transcriptional activation function of a fungal sulfur metabolism enzyme</article-title><source>Sci Rep</source><year>2016</year><volume>6</volume><fpage>25165</fpage><pub-id pub-id-type="doi">10.1038/srep25165</pub-id><pub-id pub-id-type="pmid">27121330</pub-id></element-citation></ref><ref id="CR32"><label>32.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Levati</surname><given-names>E</given-names></name><name><surname>Sartini</surname><given-names>S</given-names></name><name><surname>Ottonello</surname><given-names>S</given-names></name><name><surname>Montanini</surname><given-names>B</given-names></name></person-group><article-title>Dry and wet approaches for genome-wide functional annotation of conventional and unconventional transcriptional activators</article-title><source>Comput Struct Biotechnol J</source><year>2016</year><volume>14</volume><fpage>262</fpage><lpage>270</lpage><pub-id pub-id-type="doi">10.1016/j.csbj.2016.06.004</pub-id><pub-id pub-id-type="pmid">27453771</pub-id></element-citation></ref><ref id="CR33"><label>33.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Aerts</surname><given-names>A</given-names></name><name><surname>Ahrén</surname><given-names>D</given-names></name><name><surname>Brun</surname><given-names>A</given-names></name><name><surname>Danchin</surname><given-names>EG</given-names></name><name><surname>Duchaussoy</surname><given-names>F</given-names></name><name><surname>Gibon</surname><given-names>J</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Lindquist</surname><given-names>E</given-names></name><name><surname>Pereda</surname><given-names>V</given-names></name><name><surname>Salamov</surname><given-names>A</given-names></name><name><surname>Shapiro</surname><given-names>HJ</given-names></name><name><surname>Wuyts</surname><given-names>J</given-names></name><name><surname>Blaudez</surname><given-names>D</given-names></name><name><surname>Buée</surname><given-names>M</given-names></name><name><surname>Brokstein</surname><given-names>P</given-names></name><name><surname>Canbäck</surname><given-names>B</given-names></name><name><surname>Cohen</surname><given-names>D</given-names></name><name><surname>Courty</surname><given-names>PE</given-names></name><name><surname>Coutinho</surname><given-names>PM</given-names></name><name><surname>Delaruelle</surname><given-names>C</given-names></name><name><surname>Detter</surname><given-names>JC</given-names></name><name><surname>Deveau</surname><given-names>A</given-names></name><name><surname>DiFazio</surname><given-names>S</given-names></name><name><surname>Duplessis</surname><given-names>S</given-names></name><name><surname>Fraissinet-Tachet</surname><given-names>L</given-names></name><name><surname>Lucic</surname><given-names>E</given-names></name><name><surname>Frey-Klett</surname><given-names>P</given-names></name><name><surname>Fourrey</surname><given-names>C</given-names></name><name><surname>Feussner</surname><given-names>I</given-names></name><name><surname>Gay</surname><given-names>G</given-names></name><name><surname>Grimwood</surname><given-names>J</given-names></name><name><surname>Hoegger</surname><given-names>PJ</given-names></name><name><surname>Jain</surname><given-names>P</given-names></name><name><surname>Kilaru</surname><given-names>S</given-names></name><name><surname>Labbé</surname><given-names>J</given-names></name><name><surname>Lin</surname><given-names>YC</given-names></name><name><surname>Legué</surname><given-names>V</given-names></name><name><surname>Le Tacon</surname><given-names>F</given-names></name><name><surname>Marmeisse</surname><given-names>R</given-names></name><name><surname>Melayah</surname><given-names>D</given-names></name><name><surname>Montanini</surname><given-names>B</given-names></name><name><surname>Muratet</surname><given-names>M</given-names></name><name><surname>Nehls</surname><given-names>U</given-names></name><name><surname>Niculita-Hirzel</surname><given-names>H</given-names></name><name><surname>Oudot-Le Secq</surname><given-names>MP</given-names></name><name><surname>Peter</surname><given-names>M</given-names></name><name><surname>Quesneville</surname><given-names>H</given-names></name><name><surname>Rajashekar</surname><given-names>B</given-names></name><name><surname>Reich</surname><given-names>M</given-names></name><name><surname>Rouhier</surname><given-names>N</given-names></name><name><surname>Schmutz</surname><given-names>J</given-names></name><name><surname>Yin</surname><given-names>T</given-names></name><name><surname>Chalot</surname><given-names>M</given-names></name><name><surname>Henrissat</surname><given-names>B</given-names></name><name><surname>Kües</surname><given-names>U</given-names></name><name><surname>Lucas</surname><given-names>S</given-names></name><name><surname>Van de Peer</surname><given-names>Y</given-names></name><name><surname>Podila</surname><given-names>GK</given-names></name><name><surname>Polle</surname><given-names>A</given-names></name><name><surname>Pukkila</surname><given-names>PJ</given-names></name><name><surname>Richardson</surname><given-names>PM</given-names></name><name><surname>Rouzé</surname><given-names>P</given-names></name><name><surname>Sanders</surname><given-names>IR</given-names></name><name><surname>Stajich</surname><given-names>JE</given-names></name><name><surname>Tunlid</surname><given-names>A</given-names></name><name><surname>Tuskan</surname><given-names>G</given-names></name><name><surname>Grigoriev</surname><given-names>IV</given-names></name></person-group><article-title>The genome of <italic>Laccaria bicolor</italic> provides insights into mycorrhizal symbiosis</article-title><source>Nature</source><year>2008</year><volume>452</volume><issue>7183</issue><fpage>88</fpage><lpage>92</lpage><pub-id pub-id-type="doi">10.1038/nature06556</pub-id><pub-id pub-id-type="pmid">18322534</pub-id></element-citation></ref><ref id="CR34"><label>34.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Murat</surname><given-names>C</given-names></name><name><surname>Veneault-Fourrey</surname><given-names>C</given-names></name><name><surname>Hibbett</surname><given-names>DS</given-names></name></person-group><article-title>Unearthing the roots of ectomycorrhizal symbioses</article-title><source>Nat Rev Microbiol</source><year>2016</year><volume>14</volume><issue>12</issue><fpage>760</fpage><lpage>773</lpage><pub-id pub-id-type="doi">10.1038/nrmicro.2016.149</pub-id><pub-id pub-id-type="pmid">27795567</pub-id></element-citation></ref><ref id="CR35"><label>35.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Murat</surname><given-names>C</given-names></name><name><surname>Balestrini</surname><given-names>R</given-names></name><name><surname>Coutinho</surname><given-names>PM</given-names></name><name><surname>Jaillon</surname><given-names>O</given-names></name><name><surname>Montanini</surname><given-names>B</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Noel</surname><given-names>B</given-names></name><name><surname>Percudani</surname><given-names>R</given-names></name><name><surname>Porcel</surname><given-names>B</given-names></name><name><surname>Rubini</surname><given-names>A</given-names></name><name><surname>Amicucci</surname><given-names>A</given-names></name><name><surname>Amselem</surname><given-names>J</given-names></name><name><surname>Anthouard</surname><given-names>V</given-names></name><name><surname>Arcioni</surname><given-names>S</given-names></name><name><surname>Artiguenave</surname><given-names>F</given-names></name><name><surname>Aury</surname><given-names>JM</given-names></name><name><surname>Ballario</surname><given-names>P</given-names></name><name><surname>Bolchi</surname><given-names>A</given-names></name><name><surname>Brenna</surname><given-names>A</given-names></name><name><surname>Brun</surname><given-names>A</given-names></name><name><surname>Buée</surname><given-names>M</given-names></name><name><surname>Cantarel</surname><given-names>B</given-names></name><name><surname>Chevalier</surname><given-names>G</given-names></name><name><surname>Couloux</surname><given-names>A</given-names></name><name><surname>Da Silva</surname><given-names>C</given-names></name><name><surname>Denoeud</surname><given-names>F</given-names></name><name><surname>Duplessis</surname><given-names>S</given-names></name><name><surname>Ghignone</surname><given-names>S</given-names></name><name><surname>Hilselberger</surname><given-names>B</given-names></name><name><surname>Iotti</surname><given-names>M</given-names></name><name><surname>Marçais</surname><given-names>B</given-names></name><name><surname>Mello</surname><given-names>A</given-names></name><name><surname>Miranda</surname><given-names>M</given-names></name><name><surname>Pacioni</surname><given-names>G</given-names></name><name><surname>Quesneville</surname><given-names>H</given-names></name><name><surname>Riccioni</surname><given-names>C</given-names></name><name><surname>Ruotolo</surname><given-names>R</given-names></name><name><surname>Splivallo</surname><given-names>R</given-names></name><name><surname>Stocchi</surname><given-names>V</given-names></name><name><surname>Tisserant</surname><given-names>E</given-names></name><name><surname>Viscomi</surname><given-names>AR</given-names></name><name><surname>Zambonelli</surname><given-names>A</given-names></name><name><surname>Zampieri</surname><given-names>E</given-names></name><name><surname>Henrissat</surname><given-names>B</given-names></name><name><surname>Lebrun</surname><given-names>MH</given-names></name><name><surname>Paolocci</surname><given-names>F</given-names></name><name><surname>Bonfante</surname><given-names>P</given-names></name><name><surname>Ottonello</surname><given-names>S</given-names></name><name><surname>Wincker</surname><given-names>P</given-names></name></person-group><article-title>Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis</article-title><source>Nature</source><year>2010</year><volume>464</volume><issue>7291</issue><fpage>1033</fpage><lpage>1038</lpage><pub-id pub-id-type="doi">10.1038/nature08867</pub-id><pub-id pub-id-type="pmid">20348908</pub-id></element-citation></ref><ref id="CR36"><label>36.</label><element-citation publication-type="book"><person-group person-group-type="author"><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Tunlid</surname><given-names>A</given-names></name></person-group><article-title>The ectomycorrhizal symbiosis: a marriage of convenience</article-title><source>In: The Mycota, “Plant Relationships”</source><year>2009</year><edition>2</edition><publisher-loc>Heidelberg, Germany</publisher-loc><publisher-name>Springer-Verlag</publisher-name><fpage>237</fpage><lpage>257</lpage></element-citation></ref><ref id="CR37"><label>37.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Massicotte</surname><given-names>HB</given-names></name><name><surname>Peterson</surname><given-names>RL</given-names></name><name><surname>Ackerley</surname><given-names>CA</given-names></name><name><surname>Piché</surname><given-names>Y</given-names></name></person-group><article-title>Structure and ontogeny of <italic>Alnus crispa - Alpova diplophloeus</italic> ectomycorrhizae</article-title><source>Can J Bot</source><year>1986</year><volume>64</volume><fpage>177</fpage><lpage>192</lpage><pub-id pub-id-type="doi">10.1139/b86-026</pub-id></element-citation></ref><ref id="CR38"><label>38.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Massicotte</surname><given-names>HB</given-names></name><name><surname>Melville</surname><given-names>LH</given-names></name><name><surname>Peterson</surname><given-names>RL</given-names></name></person-group><article-title>Scanning electron microscopy of ectomycorrhizae, potential and limitations</article-title><source>Scanning Microsc</source><year>1987</year><volume>1</volume><fpage>1439</fpage><lpage>1454</lpage></element-citation></ref><ref id="CR39"><label>39.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Massicotte</surname><given-names>HB</given-names></name><name><surname>Peterson</surname><given-names>RL</given-names></name><name><surname>Ashford</surname><given-names>AE</given-names></name></person-group><article-title>Ontogeny of <italic>Eucalyptus pilularis – Pisolithus tinctorius</italic> ectomycorrhizae. I. Light microscopy and scanning electron microscopy</article-title><source>Can J Bot</source><year>1987</year><volume>65</volume><fpage>1927</fpage><lpage>1939</lpage><pub-id pub-id-type="doi">10.1139/b87-264</pub-id></element-citation></ref><ref id="CR40"><label>40.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Massicotte</surname><given-names>HB</given-names></name><name><surname>Peterson</surname><given-names>RL</given-names></name><name><surname>Ackerley</surname><given-names>CA</given-names></name><name><surname>Ashford</surname><given-names>AE</given-names></name></person-group><article-title>Ontogency of <italic>Eucalyptus pilularis – Pisolithus tinctorius</italic> ectomycorrhizae. II. Transmission electron microscopy</article-title><source>Can J Bot</source><year>1987</year><volume>65</volume><fpage>1940</fpage><lpage>1947</lpage><pub-id pub-id-type="doi">10.1139/b87-265</pub-id></element-citation></ref><ref id="CR41"><label>41.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Massicotte</surname><given-names>HB</given-names></name><name><surname>Peterson</surname><given-names>RL</given-names></name><name><surname>Melville</surname><given-names>LH</given-names></name></person-group><article-title>Ontogeny of <italic>Alnus diplophloeus</italic> ectomycorrhizae. I. Light microscopy and scanning electron microscopy</article-title><source>Can J Bot</source><year>1989</year><volume>67</volume><fpage>191</fpage><lpage>200</lpage><pub-id pub-id-type="doi">10.1139/b89-027</pub-id></element-citation></ref><ref id="CR42"><label>42.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Massicotte</surname><given-names>HB</given-names></name><name><surname>Peterson</surname><given-names>RL</given-names></name><name><surname>Ackerley</surname><given-names>CA</given-names></name><name><surname>Melville</surname><given-names>LH</given-names></name></person-group><article-title>Structure and ontogeny of <italic>Betula alleghaniensis-Pisolithus tinctorius</italic> ectomycorrhizae</article-title><source>Can J Bot</source><year>1990</year><volume>68</volume><fpage>579</fpage><lpage>593</lpage><pub-id pub-id-type="doi">10.1139/b90-077</pub-id></element-citation></ref><ref id="CR43"><label>43.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mehrabi</surname><given-names>R</given-names></name><name><surname>Ding</surname><given-names>S</given-names></name><name><surname>Xu</surname><given-names>JR</given-names></name></person-group><article-title>MADS-box transcription factor Mig1 is required for infectious growth in <italic>Magnaporthe grisea</italic></article-title><source>Eukaryot Cell</source><year>2008</year><volume>7</volume><issue>5</issue><fpage>791</fpage><lpage>799</lpage><pub-id pub-id-type="doi">10.1128/EC.00009-08</pub-id><pub-id pub-id-type="pmid">18344407</pub-id></element-citation></ref><ref id="CR44"><label>44.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Montanini</surname><given-names>B</given-names></name><name><surname>Levati</surname><given-names>E</given-names></name><name><surname>Bolchi</surname><given-names>A</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Tisserant</surname><given-names>E</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Ottonello</surname><given-names>S</given-names></name></person-group><article-title>Genome-wide search and functional identification of transcription factors in the mycorrhizal fungus <italic>Tuber melanosporum</italic></article-title><source>New Phytol</source><year>2011</year><volume>189</volume><issue>3</issue><fpage>736</fpage><lpage>750</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.2010.03525.x</pub-id><pub-id pub-id-type="pmid">21058951</pub-id></element-citation></ref><ref id="CR45"><label>45.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Nylund</surname><given-names>JE</given-names></name></person-group><article-title>The ectomycorrhizal information zone and its relation to acid polysaccharides of cortical cell walls</article-title><source>New Phytol</source><year>1987</year><volume>106</volume><fpage>505</fpage><lpage>516</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.1987.tb00128.x</pub-id></element-citation></ref><ref id="CR46"><label>46.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Olsen</surname><given-names>AN</given-names></name><name><surname>Ernst</surname><given-names>HA</given-names></name><name><surname>Leggio</surname><given-names>LL</given-names></name><name><surname>Skriver</surname><given-names>K</given-names></name></person-group><article-title>NAC transcription factors: structurally distinct, functionally diverse</article-title><source>Trends Plant Sci</source><year>2005</year><volume>10</volume><issue>2</issue><fpage>79</fpage><lpage>87</lpage><pub-id pub-id-type="doi">10.1016/j.tplants.2004.12.010</pub-id><pub-id pub-id-type="pmid">15708345</pub-id></element-citation></ref><ref id="CR47"><label>47.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Ohm</surname><given-names>RA</given-names></name><name><surname>de Jong</surname><given-names>JF</given-names></name><name><surname>de Bekker</surname><given-names>C</given-names></name><name><surname>Wosten</surname><given-names>HA</given-names></name><name><surname>Lugones</surname><given-names>LG</given-names></name></person-group><article-title>Transcription factor genes of <italic>Schizophyllum commune</italic> involved in regulation of mushroom formation</article-title><source>Mol Microbiol</source><year>2011</year><volume>81</volume><issue>6</issue><fpage>1433</fpage><lpage>1445</lpage><pub-id pub-id-type="doi">10.1111/j.1365-2958.2011.07776.x</pub-id><pub-id pub-id-type="pmid">21815946</pub-id></element-citation></ref><ref id="CR48"><label>48.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Peter</surname><given-names>M</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Ohm</surname><given-names>RA</given-names></name><name><surname>Kuo</surname><given-names>A</given-names></name><name><surname>Krützmann</surname><given-names>J</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Arend</surname><given-names>M</given-names></name><name><surname>Barry</surname><given-names>KW</given-names></name><name><surname>Binder</surname><given-names>M</given-names></name><name><surname>Choi</surname><given-names>C</given-names></name><name><surname>Clum</surname><given-names>A</given-names></name><name><surname>Copeland</surname><given-names>A</given-names></name><name><surname>Grisel</surname><given-names>N</given-names></name><name><surname>Haridas</surname><given-names>S</given-names></name><name><surname>Kipfer</surname><given-names>T</given-names></name><name><surname>LaButti</surname><given-names>K</given-names></name><name><surname>Lindquist</surname><given-names>E</given-names></name><name><surname>Lipzen</surname><given-names>A</given-names></name><name><surname>Maire</surname><given-names>R</given-names></name><name><surname>Meier</surname><given-names>B</given-names></name><name><surname>Mihaltcheva</surname><given-names>S</given-names></name><name><surname>Molinier</surname><given-names>V</given-names></name><name><surname>Murat</surname><given-names>C</given-names></name><name><surname>Pöggeler</surname><given-names>S</given-names></name><name><surname>Quandt</surname><given-names>CA</given-names></name><name><surname>Sperisen</surname><given-names>C</given-names></name><name><surname>Tritt</surname><given-names>A</given-names></name><name><surname>Tisserant</surname><given-names>E</given-names></name><name><surname>Crous</surname><given-names>PW</given-names></name><name><surname>Henrissat</surname><given-names>B</given-names></name><name><surname>Nehls</surname><given-names>U</given-names></name><name><surname>Egli</surname><given-names>S</given-names></name><name><surname>Spatafora</surname><given-names>JW</given-names></name><name><surname>Grigoriev</surname><given-names>IV</given-names></name><name><surname>Martin</surname><given-names>FM</given-names></name></person-group><article-title>Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus <italic>Cenococcum geophilum</italic></article-title><source>Nat Commun</source><year>2016</year><volume>7</volume><fpage>12662</fpage><pub-id pub-id-type="doi">10.1038/ncomms12662</pub-id><pub-id pub-id-type="pmid">27601008</pub-id></element-citation></ref><ref id="CR49"><label>49.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Peterson</surname><given-names>RL</given-names></name><name><surname>Bonfante</surname><given-names>P</given-names></name></person-group><article-title>Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas</article-title><source>Plant Soil</source><year>1994</year><volume>159</volume><fpage>79</fpage><lpage>88</lpage><pub-id pub-id-type="doi">10.1007/BF00000097</pub-id></element-citation></ref><ref id="CR50"><label>50.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Pfaffl</surname><given-names>MW</given-names></name></person-group><article-title>A new mathematical model for relative quantification in real-time RT-PCR</article-title><source>Nucleic Acids Res</source><year>2001</year><volume>29</volume><issue>9</issue><fpage>e45</fpage><pub-id pub-id-type="doi">10.1093/nar/29.9.e45</pub-id><pub-id pub-id-type="pmid">11328886</pub-id></element-citation></ref><ref id="CR51"><label>51.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Plett</surname><given-names>JM</given-names></name><name><surname>Daguerre</surname><given-names>Y</given-names></name><name><surname>Wittulsky</surname><given-names>S</given-names></name><name><surname>Vayssières</surname><given-names>A</given-names></name><name><surname>Deveau</surname><given-names>A</given-names></name><name><surname>Melton</surname><given-names>SJ</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Morrell-Falvey</surname><given-names>JL</given-names></name><name><surname>Brun</surname><given-names>A</given-names></name><name><surname>Veneault-Fourrey</surname><given-names>C</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>Effector MiSSP7 of the mutualistic fungus <italic>Laccaria bicolor</italic> stabilizes the <italic>Populus</italic> JAZ6 protein and represses jasmonic acid (JA) responsive genes</article-title><source>Proc Natl Acad Sci U S A</source><year>2014</year><volume>111</volume><issue>22</issue><fpage>8299</fpage><lpage>8304</lpage><pub-id pub-id-type="doi">10.1073/pnas.1322671111</pub-id><pub-id pub-id-type="pmid">24847068</pub-id></element-citation></ref><ref id="CR52"><label>52.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Plett</surname><given-names>JM</given-names></name><name><surname>Gibon</surname><given-names>J</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Duffy</surname><given-names>K</given-names></name><name><surname>Hoegger</surname><given-names>PJ</given-names></name><name><surname>Velagapudi</surname><given-names>R</given-names></name><name><surname>Han</surname><given-names>J</given-names></name><name><surname>Kües</surname><given-names>U</given-names></name><name><surname>Grigoriev</surname><given-names>IV</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete <italic>Laccaria bicolor</italic></article-title><source>Fungal Genet Biol</source><year>2012</year><volume>49</volume><issue>3</issue><fpage>199</fpage><lpage>209</lpage><pub-id pub-id-type="doi">10.1016/j.fgb.2012.01.002</pub-id><pub-id pub-id-type="pmid">22293303</pub-id></element-citation></ref><ref id="CR53"><label>53.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Plett</surname><given-names>JM</given-names></name><name><surname>Kemppainen</surname><given-names>M</given-names></name><name><surname>Kale</surname><given-names>SD</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Legué</surname><given-names>V</given-names></name><name><surname>Brun</surname><given-names>A</given-names></name><name><surname>Tyler</surname><given-names>BM</given-names></name><name><surname>Pardo</surname><given-names>AG</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>A secreted effector protein of <italic>Laccaria bicolor</italic> is required for symbiosis development</article-title><source>Curr Biol</source><year>2011</year><volume>21</volume><issue>14</issue><fpage>1197</fpage><lpage>1203</lpage><pub-id pub-id-type="doi">10.1016/j.cub.2011.05.033</pub-id><pub-id pub-id-type="pmid">21757352</pub-id></element-citation></ref><ref id="CR54"><label>54.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Plett</surname><given-names>JM</given-names></name><name><surname>Montanini</surname><given-names>B</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Ottonello</surname><given-names>S</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>Tapping genomics to unravel ectomycorrhizal symbiosis</article-title><source>Methods Mol Biol</source><year>2011</year><volume>722</volume><fpage>249</fpage><lpage>281</lpage><pub-id pub-id-type="doi">10.1007/978-1-61779-040-9_19</pub-id><pub-id pub-id-type="pmid">21590427</pub-id></element-citation></ref><ref id="CR55"><label>55.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Plett</surname><given-names>JM</given-names></name><name><surname>Tisserant</surname><given-names>E</given-names></name><name><surname>Brun</surname><given-names>A</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Grigoriev</surname><given-names>IV</given-names></name><name><surname>Kuo</surname><given-names>A</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name></person-group><article-title>The mutualist <italic>Laccaria bicolor</italic> expresses a Core gene regulon during the colonization of diverse host plants and a variable regulon to counteract host-specific defenses</article-title><source>Mol Plant-Microbe Interact</source><year>2015</year><volume>28</volume><issue>3</issue><fpage>261</fpage><lpage>273</lpage><pub-id pub-id-type="doi">10.1094/MPMI-05-14-0129-FI</pub-id><pub-id pub-id-type="pmid">25338146</pub-id></element-citation></ref><ref id="CR56"><label>56.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Read</surname><given-names>DJ</given-names></name><name><surname>Perez-Moreno</surname><given-names>J</given-names></name></person-group><article-title>Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance?</article-title><source>New Phytol</source><year>2003</year><volume>157</volume><fpage>475</fpage><lpage>492</lpage><pub-id pub-id-type="doi">10.1046/j.1469-8137.2003.00704.x</pub-id></element-citation></ref><ref id="CR57"><label>57.</label><mixed-citation publication-type="other">Rineau F, Lmalem H, Ahren D, Shah F, Johansson T, Coninx L, Ruytinx J, Nguyen H, Grigoriev I, Kuo A, Kohler A, Morin E, Vangronsveld J, Martin F, Colpaert JV. Comparative genomics and expression levels of hydrophobins from eight mycorrhizal genomes. Mycorrhiza. 2017; doi:10.1007/s00572-016-0758-4.</mixed-citation></ref><ref id="CR58"><label>58.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Rocha</surname><given-names>MC</given-names></name><name><surname>Fabri</surname><given-names>JH</given-names></name><name><surname>Franco de Godoy</surname><given-names>K</given-names></name><name><surname>Alves de Castro</surname><given-names>P</given-names></name><name><surname>Hori</surname><given-names>JI</given-names></name><name><surname>Ferreira da Cunha</surname><given-names>A</given-names></name><name><surname>Arentshorst</surname><given-names>M</given-names></name><name><surname>Ram</surname><given-names>AF</given-names></name><name><surname>van den Hondel</surname><given-names>CA</given-names></name><name><surname>Goldman</surname><given-names>GH</given-names></name><name><surname>Malavazi</surname><given-names>I</given-names></name></person-group><article-title><italic>Aspergillus fumigatus</italic> MADS-box transcription factor rlmA is required for regulation of the Cell Wall integrity and virulence</article-title><source>Genes, genomes, Genetics</source><year>2016</year><volume>6</volume><issue>9</issue><fpage>2983</fpage><lpage>3002</lpage><pub-id pub-id-type="pmid">27473315</pub-id></element-citation></ref><ref id="CR59"><label>59.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Shi</surname><given-names>Y</given-names></name><name><surname>Shi</surname><given-names>Y</given-names></name></person-group><article-title>Metabolic enzymes and coenzymes in transcription–a direct link between metabolism and transcription?</article-title><source>Trends Genet</source><year>2004</year><volume>20</volume><issue>9</issue><fpage>445</fpage><lpage>452</lpage><pub-id pub-id-type="doi">10.1016/j.tig.2004.07.004</pub-id><pub-id pub-id-type="pmid">15313554</pub-id></element-citation></ref><ref id="CR60"><label>60.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Shin</surname><given-names>KS</given-names></name><name><surname>Kim</surname><given-names>YH</given-names></name><name><surname>Yu</surname><given-names>JH</given-names></name></person-group><article-title>Proteomic analyses reveal the key roles of BrlA and AbaA in biogenesis of gliotoxin in <italic>Aspergillus fumigatus</italic></article-title><source>Biochem Biophys Res Commun</source><year>2015</year><volume>463</volume><issue>3</issue><fpage>428</fpage><lpage>433</lpage><pub-id pub-id-type="doi">10.1016/j.bbrc.2015.05.090</pub-id><pub-id pub-id-type="pmid">26032501</pub-id></element-citation></ref><ref id="CR61"><label>61.</label><element-citation publication-type="book"><person-group person-group-type="author"><name><surname>Smith</surname><given-names>SE</given-names></name><name><surname>Read</surname><given-names>DJ</given-names></name></person-group><source>In: mycorrhizal Symbiosis</source><year>2008</year><edition>3</edition><publisher-loc>London, UK</publisher-loc><publisher-name>Academic Press</publisher-name></element-citation></ref><ref id="CR62"><label>62.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Stajich</surname><given-names>JE</given-names></name><name><surname>Wilke</surname><given-names>SK</given-names></name><name><surname>Ahrén</surname><given-names>D</given-names></name><name><surname>Au</surname><given-names>CH</given-names></name><name><surname>Birren</surname><given-names>BW</given-names></name><name><surname>Borodovsky</surname><given-names>M</given-names></name><name><surname>Burns</surname><given-names>C</given-names></name><name><surname>Canbäck</surname><given-names>B</given-names></name><name><surname>Casselton</surname><given-names>LA</given-names></name><name><surname>Cheng</surname><given-names>CK</given-names></name><name><surname>Deng</surname><given-names>J</given-names></name><name><surname>Dietrich</surname><given-names>FS</given-names></name><name><surname>Fargo</surname><given-names>DC</given-names></name><name><surname>Farman</surname><given-names>ML</given-names></name><name><surname>Gathman</surname><given-names>AC</given-names></name><name><surname>Goldberg</surname><given-names>J</given-names></name><name><surname>Guigó</surname><given-names>R</given-names></name><name><surname>Hoegger</surname><given-names>PJ</given-names></name><name><surname>Hooker</surname><given-names>JB</given-names></name><name><surname>Huggins</surname><given-names>A</given-names></name><name><surname>James</surname><given-names>TY</given-names></name><name><surname>Kamada</surname><given-names>T</given-names></name><name><surname>Kilaru</surname><given-names>S</given-names></name><name><surname>Kodira</surname><given-names>C</given-names></name><name><surname>Kües</surname><given-names>U</given-names></name><name><surname>Kupfer</surname><given-names>D</given-names></name><name><surname>Kwan</surname><given-names>HS</given-names></name><name><surname>Lomsadze</surname><given-names>A</given-names></name><name><surname>Li</surname><given-names>W</given-names></name><name><surname>Lilly</surname><given-names>WW</given-names></name><name><surname>Ma</surname><given-names>LJ</given-names></name><name><surname>Mackey</surname><given-names>AJ</given-names></name><name><surname>Manning</surname><given-names>G</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Muraguchi</surname><given-names>H</given-names></name><name><surname>Natvig</surname><given-names>DO</given-names></name><name><surname>Palmerini</surname><given-names>H</given-names></name><name><surname>Ramesh</surname><given-names>MA</given-names></name><name><surname>Rehmeyer</surname><given-names>CJ</given-names></name><name><surname>Roe</surname><given-names>BA</given-names></name><name><surname>Shenoy</surname><given-names>N</given-names></name><name><surname>Stanke</surname><given-names>M</given-names></name><name><surname>Ter-Hovhannisyan</surname><given-names>V</given-names></name><name><surname>Tunlid</surname><given-names>A</given-names></name><name><surname>Velagapudi</surname><given-names>R</given-names></name><name><surname>Vision</surname><given-names>TJ</given-names></name><name><surname>Zeng</surname><given-names>Q</given-names></name><name><surname>Zolan</surname><given-names>ME</given-names></name><name><surname>Pukkila</surname><given-names>PJ</given-names></name></person-group><article-title>Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom <italic>Coprinopsis cinerea</italic> (<italic>Coprinus cinereus</italic>)</article-title><source>Proc Natl Acad Sci U S A</source><year>2010</year><volume>107</volume><issue>26</issue><fpage>11889</fpage><lpage>11894</lpage><pub-id pub-id-type="doi">10.1073/pnas.1003391107</pub-id><pub-id pub-id-type="pmid">20547848</pub-id></element-citation></ref><ref id="CR63"><label>63.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Stegmaier</surname><given-names>P</given-names></name><name><surname>Kel</surname><given-names>AE</given-names></name><name><surname>Wingender</surname><given-names>E</given-names></name></person-group><article-title>Systematic DNA-binding domain classification of transcription factors</article-title><source>Genome Inform</source><year>2004</year><volume>15</volume><issue>2</issue><fpage>276</fpage><lpage>286</lpage><pub-id pub-id-type="pmid">15706513</pub-id></element-citation></ref><ref id="CR64"><label>64.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Stracke</surname><given-names>R</given-names></name><name><surname>Werber</surname><given-names>M</given-names></name><name><surname>Weisshaar</surname><given-names>B</given-names></name></person-group><article-title>The R2R3-MYB gene family in <italic>Arabidopsis thaliana</italic></article-title><source>Curr Opin Plant Biol</source><year>2001</year><volume>4</volume><issue>5</issue><fpage>447</fpage><lpage>456</lpage><pub-id pub-id-type="doi">10.1016/S1369-5266(00)00199-0</pub-id><pub-id pub-id-type="pmid">11597504</pub-id></element-citation></ref><ref id="CR65"><label>65.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Titz</surname><given-names>B</given-names></name><name><surname>Thomas</surname><given-names>S</given-names></name><name><surname>Rajagopala</surname><given-names>SV</given-names></name><name><surname>Chiba</surname><given-names>T</given-names></name><name><surname>Ito</surname><given-names>T</given-names></name><name><surname>Uetz</surname><given-names>P</given-names></name></person-group><article-title>Transcriptional activators in yeast</article-title><source>Nucleic Acids Res</source><year>2006</year><volume>34</volume><issue>3</issue><fpage>955</fpage><lpage>967</lpage><pub-id pub-id-type="doi">10.1093/nar/gkj493</pub-id><pub-id pub-id-type="pmid">16464826</pub-id></element-citation></ref><ref id="CR66"><label>66.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Todd</surname><given-names>RB</given-names></name><name><surname>Murphy</surname><given-names>RL</given-names></name><name><surname>Martin</surname><given-names>HM</given-names></name><name><surname>Sharp</surname><given-names>JA</given-names></name><name><surname>Davis</surname><given-names>MA</given-names></name><name><surname>Katz</surname><given-names>ME</given-names></name><name><surname>Hynes</surname><given-names>MJ</given-names></name></person-group><article-title>The acetate regulatory gene facB of <italic>Aspergillus nidulans</italic> encodes a Zn(II)2Cys6 transcriptional activator</article-title><source>Mol Gen Genet</source><year>1997</year><volume>254</volume><issue>5</issue><fpage>495</fpage><lpage>504</lpage><pub-id pub-id-type="doi">10.1007/s004380050444</pub-id><pub-id pub-id-type="pmid">9197408</pub-id></element-citation></ref><ref id="CR67"><label>67.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Todd</surname><given-names>RB</given-names></name><name><surname>Zhou</surname><given-names>M</given-names></name><name><surname>Ohm</surname><given-names>RA</given-names></name><name><surname>Leeggangers</surname><given-names>HA</given-names></name><name><surname>Visser</surname><given-names>L</given-names></name><name><surname>de Vries</surname><given-names>RP</given-names></name></person-group><article-title>Prevalence of transcription factors in ascomycete and basidiomycete fungi</article-title><source>BMC Genomics</source><year>2014</year><volume>15</volume><fpage>214</fpage><pub-id pub-id-type="doi">10.1186/1471-2164-15-214</pub-id><pub-id pub-id-type="pmid">24650355</pub-id></element-citation></ref><ref id="CR68"><label>68.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Tripathi</surname><given-names>G</given-names></name><name><surname>Wiltshire</surname><given-names>C</given-names></name><name><surname>Macaskill</surname><given-names>S</given-names></name><name><surname>Tournu</surname><given-names>H</given-names></name><name><surname>Budge</surname><given-names>S</given-names></name><name><surname>Brown</surname><given-names>AJP</given-names></name></person-group><article-title>Gcn4 Co-ordinates morphogenetic and metabolic responses to amino acid starvation in <italic>Candida albicans</italic></article-title><source>EMBO J</source><year>2002</year><volume>21</volume><issue>20</issue><fpage>5448</fpage><lpage>5456</lpage><pub-id pub-id-type="doi">10.1093/emboj/cdf507</pub-id><pub-id pub-id-type="pmid">12374745</pub-id></element-citation></ref><ref id="CR69"><label>69.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>van der Heijden</surname><given-names>MG</given-names></name><name><surname>Martin</surname><given-names>FM</given-names></name><name><surname>Selosse</surname><given-names>MA</given-names></name><name><surname>Sanders</surname><given-names>IR</given-names></name></person-group><article-title>Mycorrhizal ecology and evolution: the past, the present, and the future</article-title><source>New Phytol</source><year>2015</year><volume>205</volume><issue>4</issue><fpage>1406</fpage><lpage>1423</lpage><pub-id pub-id-type="doi">10.1111/nph.13288</pub-id><pub-id pub-id-type="pmid">25639293</pub-id></element-citation></ref><ref id="CR70"><label>70.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Vayssières</surname><given-names>A</given-names></name><name><surname>Pěnčík</surname><given-names>A</given-names></name><name><surname>Felten</surname><given-names>J</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Ljung</surname><given-names>K</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name><name><surname>Legué</surname><given-names>V</given-names></name></person-group><article-title>Development of the poplar-<italic>Laccaria bicolor</italic> Ectomycorrhiza modifies root auxin metabolism, signaling, and response</article-title><source>Plant Physiol</source><year>2015</year><volume>169</volume><issue>1</issue><fpage>890</fpage><lpage>902</lpage><pub-id pub-id-type="doi">10.1104/pp.114.255620</pub-id><pub-id pub-id-type="pmid">26084921</pub-id></element-citation></ref><ref id="CR71"><label>71.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Veneault-Fourrey</surname><given-names>C</given-names></name><name><surname>Commun</surname><given-names>C</given-names></name><name><surname>Kohler</surname><given-names>A</given-names></name><name><surname>Morin</surname><given-names>E</given-names></name><name><surname>Balestrini</surname><given-names>R</given-names></name><name><surname>Plett</surname><given-names>J</given-names></name><name><surname>Danchin</surname><given-names>E</given-names></name><name><surname>Coutinho</surname><given-names>P</given-names></name><name><surname>Wiebenga</surname><given-names>A</given-names></name><name><surname>de Vries</surname><given-names>RP</given-names></name><name><surname>Henrissat</surname><given-names>B</given-names></name><name><surname>Martin</surname><given-names>F</given-names></name></person-group><article-title>Genomic and transcriptomic analysis of <italic>Laccaria bicolor</italic> CAZome reveals insights into polysaccharides remodelling during symbiosis establishment</article-title><source>Fungal Genet Biol</source><year>2014</year><volume>72</volume><fpage>168</fpage><lpage>181</lpage><pub-id pub-id-type="doi">10.1016/j.fgb.2014.08.007</pub-id><pub-id pub-id-type="pmid">25173823</pub-id></element-citation></ref><ref id="CR72"><label>72.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Watanabe</surname><given-names>Y</given-names></name><name><surname>Irie</surname><given-names>K</given-names></name><name><surname>Matsumoto</surname><given-names>K</given-names></name></person-group><article-title>Yeast RLM1 encodes a serum response factor-like protein that may function downstream of the Mpk1 (Slt2) mitogen-activated protein kinase pathway</article-title><source>Mol Cell Biol</source><year>1995</year><volume>15</volume><issue>10</issue><fpage>5740</fpage><lpage>5749</lpage><pub-id pub-id-type="doi">10.1128/MCB.15.10.5740</pub-id><pub-id pub-id-type="pmid">7565726</pub-id></element-citation></ref><ref id="CR73"><label>73.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Wong Sak Hoi</surname><given-names>J</given-names></name><name><surname>Dumas</surname><given-names>B</given-names></name></person-group><article-title>Ste12 And Ste12-like proteins, fungal transcription factors regulating development and pathogenicity</article-title><source>Eukaryot Cell</source><year>2010</year><volume>9</volume><issue>4</issue><fpage>480</fpage><lpage>485</lpage><pub-id pub-id-type="doi">10.1128/EC.00333-09</pub-id><pub-id pub-id-type="pmid">20139240</pub-id></element-citation></ref><ref id="CR74"><label>74.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Wright</surname><given-names>DP</given-names></name><name><surname>Johansson</surname><given-names>T</given-names></name><name><surname>Le Quere</surname><given-names>A</given-names></name><name><surname>Söderström</surname><given-names>B</given-names></name><name><surname>Tunlid</surname><given-names>A</given-names></name></person-group><article-title>Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus <italic>Paxillus involutus</italic> in association with birch (<italic>Betula pendula</italic>) seedlings in soil microcosms</article-title><source>New Phytol</source><year>2005</year><volume>167</volume><fpage>579</fpage><lpage>596</lpage><pub-id pub-id-type="doi">10.1111/j.1469-8137.2005.01441.x</pub-id><pub-id pub-id-type="pmid">15998408</pub-id></element-citation></ref><ref id="CR75"><label>75.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Zhang</surname><given-names>Z</given-names></name><name><surname>Li</surname><given-names>H</given-names></name><name><surname>Qin</surname><given-names>G</given-names></name><name><surname>He</surname><given-names>C</given-names></name><name><surname>Li</surname><given-names>B</given-names></name><name><surname>Tian</surname><given-names>S</given-names></name></person-group><article-title>The MADS-Box transcription factor Bcmads1 is required for growth, sclerotia production and pathogenicity of <italic>Botrytis cinerea</italic></article-title><source>Sci Rep</source><year>2016</year><volume>6</volume><fpage>33901</fpage><pub-id pub-id-type="doi">10.1038/srep33901</pub-id><pub-id pub-id-type="pmid">27658442</pub-id></element-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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