A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy
Identifieur interne : 000652 ( Pmc/Checkpoint ); précédent : 000651; suivant : 000653A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy
Auteurs : Nianwu Tang [République populaire de Chine, France] ; Hélène San Clemente [France] ; Sébastien Roy [France] ; Guillaume Bécard [France] ; Bin Zhao [République populaire de Chine] ; Christophe Roux [France]Source :
- Frontiers in Microbiology [ 1664-302X ] ; 2016.
Abstract
Arbuscular mycorrhizal (AM) fungi are a diverse group of soil fungi (Glomeromycota) that form the most ancient mutualistic association termed AM symbiosis with a majority of land plants, improving their nutrition uptake and resistance to stresses. In contrast to their great ecological implications, the knowledge of the molecular biological mechanisms involved is still scant, partly due to the limited genomic resources available. Here, we describe the gene repertoire of a new AM fungus
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DOI: 10.3389/fmicb.2016.00233
PubMed: 26973612
PubMed Central: 4771724
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A Survey of the Gene Repertoire of <italic>Gigaspora rosea</italic> Unravels Conserved Features among Glomeromycota for Obligate Biotrophy</title><author><name sortKey="Tang, Nianwu" sort="Tang, Nianwu" uniqKey="Tang N" first="Nianwu" last="Tang">Nianwu Tang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University</institution><country>Wuhan, China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea></wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="San Clemente, Helene" sort="San Clemente, Helene" uniqKey="San Clemente H" first="Hélène" last="San Clemente">Hélène San Clemente</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Roy, Sebastien" sort="Roy, Sebastien" uniqKey="Roy S" first="Sébastien" last="Roy">Sébastien Roy</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>AGRONUTRITION Laboratoire de Biotechnologies</institution><country>Toulouse, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Zhao, Bin" sort="Zhao, Bin" uniqKey="Zhao B" first="Bin" last="Zhao">Bin Zhao</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University</institution><country>Wuhan, China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Roux, Christophe" sort="Roux, Christophe" uniqKey="Roux C" first="Christophe" last="Roux">Christophe Roux</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26973612</idno><idno type="pmc">4771724</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4771724</idno><idno type="RBID">PMC:4771724</idno><idno type="doi">10.3389/fmicb.2016.00233</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000055</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000055</idno><idno type="wicri:Area/Pmc/Curation">000055</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000055</idno><idno type="wicri:Area/Pmc/Checkpoint">000652</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000652</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A Survey of the Gene Repertoire of <italic>Gigaspora rosea</italic> Unravels Conserved Features among Glomeromycota for Obligate Biotrophy</title><author><name sortKey="Tang, Nianwu" sort="Tang, Nianwu" uniqKey="Tang N" first="Nianwu" last="Tang">Nianwu Tang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University</institution><country>Wuhan, China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea></wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="San Clemente, Helene" sort="San Clemente, Helene" uniqKey="San Clemente H" first="Hélène" last="San Clemente">Hélène San Clemente</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Roy, Sebastien" sort="Roy, Sebastien" uniqKey="Roy S" first="Sébastien" last="Roy">Sébastien Roy</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>AGRONUTRITION Laboratoire de Biotechnologies</institution><country>Toulouse, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Zhao, Bin" sort="Zhao, Bin" uniqKey="Zhao B" first="Bin" last="Zhao">Bin Zhao</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University</institution><country>Wuhan, China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea></wicri:regionArea></affiliation></author><author><name sortKey="Roux, Christophe" sort="Roux, Christophe" uniqKey="Roux C" first="Christophe" last="Roux">Christophe Roux</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea></affiliation></author></analytic><series><title level="j">Frontiers in Microbiology</title><idno type="eISSN">1664-302X</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Arbuscular mycorrhizal (AM) fungi are a diverse group of soil fungi (Glomeromycota) that form the most ancient mutualistic association termed AM symbiosis with a majority of land plants, improving their nutrition uptake and resistance to stresses. In contrast to their great ecological implications, the knowledge of the molecular biological mechanisms involved is still scant, partly due to the limited genomic resources available. Here, we describe the gene repertoire of a new AM fungus <italic>Gigaspora rosea</italic> (Diversisporales). Among the 86332 non-redundant virtual transcripts assembled, 15346 presented similarities with proteins in the Refseq database and 10175 were assigned with GO terms. KOG and Interpro domain annotations clearly showed an enrichment of genes involved in signal transduction in <italic>G. rosea</italic>. KEGG pathway analysis indicates that most primary metabolic processes are active in <italic>G. rosea</italic>. However, as for <italic>Rhizophagus irregularis</italic>, several metabolic genes were not found, including the fatty acid synthase (FAS) gene. This finding supports the hypothesis that AM fungi depend on the lipids produced by their hosts. Furthermore, the presence of a large number of transporters and 100s of secreted proteins, together with the reduced number of plant cell wall degrading enzymes could be interpreted as an evolutionary adaptation to its mutualistic obligate biotrophy. The detection of meiosis-related genes suggests that <italic>G. rosea</italic> might use a cryptic sexual process. Lastly, a phylogeny of basal fungi clearly shows Glomeromycota as a sister clade to Mucoromycotina, not only to the Mucorales or Mortierellales. The characterization of the gene repertoire from an AM fungal species belonging to the order of Diversisporales and its comparison with the gene sets of <italic>R. irregularis</italic> (Glomerales) and <italic>Gigaspora margarita</italic> (Diversisporales), reveal that AM fungi share several features linked to mutualistic obligate biotrophy. This work contributes to lay the foundation for forthcoming studies into the genomics of Diversisporales, and also illuminates the utility of comparing gene repertoires of species from Diversisporales and other clades of Glomeromycota to gain more insights into the genetics and evolution of this fungal group.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Akiyama, K" uniqKey="Akiyama K">K. Akiyama</name></author><author><name sortKey="Matsuzaki, K" uniqKey="Matsuzaki K">K. Matsuzaki</name></author><author><name sortKey="Hayashi, H" uniqKey="Hayashi H">H. Hayashi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Amselem, J" uniqKey="Amselem J">J. Amselem</name></author><author><name sortKey="Cuomo, C A" uniqKey="Cuomo C">C. A. Cuomo</name></author><author><name sortKey="Van Kan, J A L" uniqKey="Van Kan J">J. A. L. van Kan</name></author><author><name sortKey="Viaud, M" uniqKey="Viaud M">M. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Microbiol</journal-id><journal-id journal-id-type="iso-abbrev">Front Microbiol</journal-id><journal-id journal-id-type="publisher-id">Front. Microbiol.</journal-id><journal-title-group><journal-title>Frontiers in Microbiology</journal-title></journal-title-group><issn pub-type="epub">1664-302X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26973612</article-id><article-id pub-id-type="pmc">4771724</article-id><article-id pub-id-type="doi">10.3389/fmicb.2016.00233</article-id><article-categories><subj-group subj-group-type="heading"><subject>Microbiology</subject><subj-group><subject>Original Research</subject></subj-group></subj-group></article-categories><title-group><article-title>A Survey of the Gene Repertoire of <italic>Gigaspora rosea</italic> Unravels Conserved Features among Glomeromycota for Obligate Biotrophy</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Tang</surname><given-names>Nianwu</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/224537/overview"></uri></contrib><contrib contrib-type="author"><name><surname>San Clemente</surname><given-names>Hélène</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/174568/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Roy</surname><given-names>Sébastien</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bécard</surname><given-names>Guillaume</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhao</surname><given-names>Bin</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Roux</surname><given-names>Christophe</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/277139/overview"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University</institution><country>Wuhan, China</country></aff><aff id="aff2"><sup>2</sup><institution>CNRS, Laboratoire de Recherche en Sciences Végétales, UMR, Université Paul Sabatier – Université de Toulouse</institution><country>Castanet Tolosan, France</country></aff><aff id="aff3"><sup>3</sup><institution>AGRONUTRITION Laboratoire de Biotechnologies</institution><country>Toulouse, France</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Andrea Genre, University of Torino, Italy</italic></p></fn><fn fn-type="edited-by"><p>Reviewed by: <italic>Alessandra Salvioli, University of Torino, Italy; Andreas Brachmann, Ludwig-Maximilians-Universität München, Germany</italic></p></fn><corresp id="fn001">*Correspondence: <italic>Bin Zhao, <email xlink:type="simple">binzhao@mail.hzau.edu.cn</email>; Christophe Roux, <email xlink:type="simple">roux@lrsv.ups-tlse.fr</email></italic></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Plant Biotic Interactions, a section of the journal Frontiers in Microbiology</p></fn></author-notes><pub-date pub-type="epub"><day>01</day><month>3</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>7</volume><elocation-id>233</elocation-id><history><date date-type="received"><day>26</day><month>10</month><year>2015</year></date><date date-type="accepted"><day>15</day><month>2</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016 Tang, San Clemente, Roy, Bécard, Zhao and Roux.</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Tang, San Clemente, Roy, Bécard, Zhao and Roux</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Arbuscular mycorrhizal (AM) fungi are a diverse group of soil fungi (Glomeromycota) that form the most ancient mutualistic association termed AM symbiosis with a majority of land plants, improving their nutrition uptake and resistance to stresses. In contrast to their great ecological implications, the knowledge of the molecular biological mechanisms involved is still scant, partly due to the limited genomic resources available. Here, we describe the gene repertoire of a new AM fungus <italic>Gigaspora rosea</italic> (Diversisporales). Among the 86332 non-redundant virtual transcripts assembled, 15346 presented similarities with proteins in the Refseq database and 10175 were assigned with GO terms. KOG and Interpro domain annotations clearly showed an enrichment of genes involved in signal transduction in <italic>G. rosea</italic>. KEGG pathway analysis indicates that most primary metabolic processes are active in <italic>G. rosea</italic>. However, as for <italic>Rhizophagus irregularis</italic>, several metabolic genes were not found, including the fatty acid synthase (FAS) gene. This finding supports the hypothesis that AM fungi depend on the lipids produced by their hosts. Furthermore, the presence of a large number of transporters and 100s of secreted proteins, together with the reduced number of plant cell wall degrading enzymes could be interpreted as an evolutionary adaptation to its mutualistic obligate biotrophy. The detection of meiosis-related genes suggests that <italic>G. rosea</italic> might use a cryptic sexual process. Lastly, a phylogeny of basal fungi clearly shows Glomeromycota as a sister clade to Mucoromycotina, not only to the Mucorales or Mortierellales. The characterization of the gene repertoire from an AM fungal species belonging to the order of Diversisporales and its comparison with the gene sets of <italic>R. irregularis</italic> (Glomerales) and <italic>Gigaspora margarita</italic> (Diversisporales), reveal that AM fungi share several features linked to mutualistic obligate biotrophy. This work contributes to lay the foundation for forthcoming studies into the genomics of Diversisporales, and also illuminates the utility of comparing gene repertoires of species from Diversisporales and other clades of Glomeromycota to gain more insights into the genetics and evolution of this fungal group.</p></abstract><kwd-group><kwd>arbuscular mycorrhizal fungi</kwd><kwd>Glomeromycota</kwd><kwd>obligate biotrophy</kwd><kwd>gene repertoire</kwd><kwd>mRNA sequencing</kwd><kwd>phylogenomics</kwd></kwd-group><funding-group><award-group><funding-source id="cn001">China Scholarship Council<named-content content-type="fundref-id">10.13039/501100004543</named-content></funding-source></award-group></funding-group><counts><fig-count count="4"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="140"></ref-count><page-count count="16"></page-count><word-count count="0"></word-count></counts></article-meta></front></pmc><affiliations><list><country><li>France</li><li>République populaire de Chine</li></country></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Tang, Nianwu" sort="Tang, Nianwu" uniqKey="Tang N" first="Nianwu" last="Tang">Nianwu Tang</name></noRegion><name sortKey="Zhao, Bin" sort="Zhao, Bin" uniqKey="Zhao B" first="Bin" last="Zhao">Bin Zhao</name></country><country name="France"><noRegion><name sortKey="Tang, Nianwu" sort="Tang, Nianwu" uniqKey="Tang N" first="Nianwu" last="Tang">Nianwu Tang</name></noRegion><name sortKey="Becard, Guillaume" sort="Becard, Guillaume" uniqKey="Becard G" first="Guillaume" last="Bécard">Guillaume Bécard</name><name sortKey="Roux, Christophe" sort="Roux, Christophe" uniqKey="Roux C" first="Christophe" last="Roux">Christophe Roux</name><name sortKey="Roy, Sebastien" sort="Roy, Sebastien" uniqKey="Roy S" first="Sébastien" last="Roy">Sébastien Roy</name><name sortKey="San Clemente, Helene" sort="San Clemente, Helene" uniqKey="San Clemente H" first="Hélène" last="San Clemente">Hélène San Clemente</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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