Dual RNA-Sequencing of Eucalyptus nitens during Phytophthora cinnamomi Challenge Reveals Pathogen and Host Factors Influencing Compatibility
Identifieur interne : 000309 ( Pmc/Corpus ); précédent : 000308; suivant : 000310Dual RNA-Sequencing of Eucalyptus nitens during Phytophthora cinnamomi Challenge Reveals Pathogen and Host Factors Influencing Compatibility
Auteurs : Febé E. Meyer ; Louise S. Shuey ; Sitha Naidoo ; Thandekile Mamni ; Dave K. Berger ; Alexander A. Myburg ; Noëlani Van Den Berg ; Sanushka NaidooSource :
- Frontiers in Plant Science [ 1664-462X ] ; 2016.
Abstract
Damage caused by
Url:
DOI: 10.3389/fpls.2016.00191
PubMed: 26973660
PubMed Central: 4773608
Links to Exploration step
PMC:4773608Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Dual RNA-Sequencing of <italic>Eucalyptus nitens</italic> during <italic>Phytophthora cinnamomi</italic> Challenge Reveals Pathogen and Host Factors Influencing Compatibility</title><author><name sortKey="Meyer, Febe E" sort="Meyer, Febe E" uniqKey="Meyer F" first="Febé E." last="Meyer">Febé E. Meyer</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Shuey, Louise S" sort="Shuey, Louise S" uniqKey="Shuey L" first="Louise S." last="Shuey">Louise S. Shuey</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Naidoo, Sitha" sort="Naidoo, Sitha" uniqKey="Naidoo S" first="Sitha" last="Naidoo">Sitha Naidoo</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Mamni, Thandekile" sort="Mamni, Thandekile" uniqKey="Mamni T" first="Thandekile" last="Mamni">Thandekile Mamni</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Berger, Dave K" sort="Berger, Dave K" uniqKey="Berger D" first="Dave K." last="Berger">Dave K. Berger</name><affiliation><nlm:aff id="aff2"><institution>Department of Plant Science, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Myburg, Alexander A" sort="Myburg, Alexander A" uniqKey="Myburg A" first="Alexander A." last="Myburg">Alexander A. Myburg</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Van Den Berg, Noelani" sort="Van Den Berg, Noelani" uniqKey="Van Den Berg N" first="Noëlani" last="Van Den Berg">Noëlani Van Den Berg</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Naidoo, Sanushka" sort="Naidoo, Sanushka" uniqKey="Naidoo S" first="Sanushka" last="Naidoo">Sanushka Naidoo</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26973660</idno><idno type="pmc">4773608</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4773608</idno><idno type="RBID">PMC:4773608</idno><idno type="doi">10.3389/fpls.2016.00191</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000309</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Dual RNA-Sequencing of <italic>Eucalyptus nitens</italic> during <italic>Phytophthora cinnamomi</italic> Challenge Reveals Pathogen and Host Factors Influencing Compatibility</title><author><name sortKey="Meyer, Febe E" sort="Meyer, Febe E" uniqKey="Meyer F" first="Febé E." last="Meyer">Febé E. Meyer</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Shuey, Louise S" sort="Shuey, Louise S" uniqKey="Shuey L" first="Louise S." last="Shuey">Louise S. Shuey</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Naidoo, Sitha" sort="Naidoo, Sitha" uniqKey="Naidoo S" first="Sitha" last="Naidoo">Sitha Naidoo</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Mamni, Thandekile" sort="Mamni, Thandekile" uniqKey="Mamni T" first="Thandekile" last="Mamni">Thandekile Mamni</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Berger, Dave K" sort="Berger, Dave K" uniqKey="Berger D" first="Dave K." last="Berger">Dave K. Berger</name><affiliation><nlm:aff id="aff2"><institution>Department of Plant Science, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Myburg, Alexander A" sort="Myburg, Alexander A" uniqKey="Myburg A" first="Alexander A." last="Myburg">Alexander A. Myburg</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Van Den Berg, Noelani" sort="Van Den Berg, Noelani" uniqKey="Van Den Berg N" first="Noëlani" last="Van Den Berg">Noëlani Van Den Berg</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author><author><name sortKey="Naidoo, Sanushka" sort="Naidoo, Sanushka" uniqKey="Naidoo S" first="Sanushka" last="Naidoo">Sanushka Naidoo</name><affiliation><nlm:aff id="aff1"><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Plant Science</title><idno type="eISSN">1664-462X</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>Damage caused by <italic>Phytophthora cinnamomi</italic> Rands remains an important concern on forest tree species. The pathogen causes root and collar rot, stem cankers, and dieback of various economically important <italic>Eucalyptus</italic> spp. In South Africa, susceptible cold tolerant <italic>Eucalyptus</italic> plantations have been affected by various <italic>Phytophthora</italic> spp. with <italic>P. cinnamomi</italic> considered one of the most virulent. The molecular basis of this compatible interaction is poorly understood. In this study, susceptible <italic>Eucalyptus nitens</italic> plants were stem inoculated with <italic>P. cinnamomi</italic> and tissue was harvested five days post inoculation. Dual RNA-sequencing, a technique which allows the concurrent detection of both pathogen and host transcripts during infection, was performed. Approximately 1% of the reads mapped to the draft genome of <italic>P. cinnamomi</italic> while 78% of the reads mapped to the <italic>Eucalyptus grandis</italic> genome. The highest expressed <italic>P. cinnamomi</italic> gene <italic>in planta</italic> was a putative crinkler effector (<italic>CRN1</italic>). Phylogenetic analysis indicated the high similarity of this <italic>P. cinnamomi CRN1</italic> to that of <italic>Phytophthora infestans</italic>. Some CRN effectors are known to target host nuclei to suppress defense. In the host, over 1400 genes were significantly differentially expressed in comparison to mock inoculated trees, including suites of pathogenesis related (<italic>PR</italic>) genes. In particular, a <italic>PR-9</italic> peroxidase gene with a high similarity to a <italic>Carica papaya PR-9</italic> ortholog previously shown to be suppressed upon infection by <italic>Phytophthora palmivora</italic> was down-regulated two-fold. This <italic>PR-9</italic> gene may represent a cross-species effector target during <italic>P. cinnamomi</italic> infection. This study identified pathogenicity factors, potential manipulation targets, and attempted host defense mechanisms activated by <italic>E. nitens</italic> that contributed to the susceptible outcome of the interaction.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Acharya, K" uniqKey="Acharya K">K. Acharya</name></author><author><name sortKey="Pal, A K" uniqKey="Pal A">A. K. Pal</name></author><author><name sortKey="Gulati, A" uniqKey="Gulati A">A. Gulati</name></author><author><name sortKey="Kumar, S" uniqKey="Kumar S">S. Kumar</name></author><author><name sortKey="Singh, A K" uniqKey="Singh A">A. K. Singh</name></author><author><name sortKey="Ahuja, P S" uniqKey="Ahuja P">P. S. Ahuja</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Adhikari, B N" uniqKey="Adhikari B">B. N. Adhikari</name></author><author><name sortKey="Hamilton, J P" uniqKey="Hamilton J">J. P. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id><journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id><journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id><journal-title-group><journal-title>Frontiers in Plant Science</journal-title></journal-title-group><issn pub-type="epub">1664-462X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26973660</article-id><article-id pub-id-type="pmc">4773608</article-id><article-id pub-id-type="doi">10.3389/fpls.2016.00191</article-id><article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject><subj-group><subject>Original Research</subject></subj-group></subj-group></article-categories><title-group><article-title>Dual RNA-Sequencing of <italic>Eucalyptus nitens</italic> during <italic>Phytophthora cinnamomi</italic> Challenge Reveals Pathogen and Host Factors Influencing Compatibility</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Meyer</surname><given-names>Febé E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn003"><sup>†</sup></xref></contrib><contrib contrib-type="author"><name><surname>Shuey</surname><given-names>Louise S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn003"><sup>†</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/240642/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Naidoo</surname><given-names>Sitha</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Mamni</surname><given-names>Thandekile</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Berger</surname><given-names>Dave K.</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/60723/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Myburg</surname><given-names>Alexander A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/36975/overview"></uri></contrib><contrib contrib-type="author"><name><surname>van den Berg</surname><given-names>Noëlani</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/205576/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Naidoo</surname><given-names>Sanushka</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/67645/overview"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Department of Genetics, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></aff><aff id="aff2"><sup>2</sup><institution>Department of Plant Science, Forestry and Agricultural Biotechnology Institute, Genomics Research Institute, University of Pretoria</institution><country>Pretoria, South Africa</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Giulia De Lorenzo, Sapienza, Università di Roma, Italy</p></fn><fn fn-type="edited-by"><p>Reviewed by: Vijai Kumar Gupta, National University of Ireland, Galway, Ireland; Felice Cervone, Sapienza, Università di Roma, Italy; Carlos Alberto Labate, University of São Paulo, Brazil</p></fn><corresp id="fn001">*Correspondence: Sanushka Naidoo <email xlink:type="simple">sanushka.naidoo@fabi.up.ac.za</email></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Plant Biotic Interactions, a section of the journal Frontiers in Plant Science</p></fn><fn fn-type="other" id="fn003"><p>†These authors have contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>02</day><month>3</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>7</volume><elocation-id>191</elocation-id><history><date date-type="received"><day>26</day><month>5</month><year>2015</year></date><date date-type="accepted"><day>04</day><month>2</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016 Meyer, Shuey, Naidoo, Mamni, Berger, Myburg, van den Berg and Naidoo.</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Meyer, Shuey, Naidoo, Mamni, Berger, Myburg, van den Berg and Naidoo</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>Damage caused by <italic>Phytophthora cinnamomi</italic> Rands remains an important concern on forest tree species. The pathogen causes root and collar rot, stem cankers, and dieback of various economically important <italic>Eucalyptus</italic> spp. In South Africa, susceptible cold tolerant <italic>Eucalyptus</italic> plantations have been affected by various <italic>Phytophthora</italic> spp. with <italic>P. cinnamomi</italic> considered one of the most virulent. The molecular basis of this compatible interaction is poorly understood. In this study, susceptible <italic>Eucalyptus nitens</italic> plants were stem inoculated with <italic>P. cinnamomi</italic> and tissue was harvested five days post inoculation. Dual RNA-sequencing, a technique which allows the concurrent detection of both pathogen and host transcripts during infection, was performed. Approximately 1% of the reads mapped to the draft genome of <italic>P. cinnamomi</italic> while 78% of the reads mapped to the <italic>Eucalyptus grandis</italic> genome. The highest expressed <italic>P. cinnamomi</italic> gene <italic>in planta</italic> was a putative crinkler effector (<italic>CRN1</italic>). Phylogenetic analysis indicated the high similarity of this <italic>P. cinnamomi CRN1</italic> to that of <italic>Phytophthora infestans</italic>. Some CRN effectors are known to target host nuclei to suppress defense. In the host, over 1400 genes were significantly differentially expressed in comparison to mock inoculated trees, including suites of pathogenesis related (<italic>PR</italic>) genes. In particular, a <italic>PR-9</italic> peroxidase gene with a high similarity to a <italic>Carica papaya PR-9</italic> ortholog previously shown to be suppressed upon infection by <italic>Phytophthora palmivora</italic> was down-regulated two-fold. This <italic>PR-9</italic> gene may represent a cross-species effector target during <italic>P. cinnamomi</italic> infection. This study identified pathogenicity factors, potential manipulation targets, and attempted host defense mechanisms activated by <italic>E. nitens</italic> that contributed to the susceptible outcome of the interaction.</p></abstract><kwd-group><kwd>plant defense</kwd><kwd>RNA-seq</kwd><kwd><italic>Eucalyptus nitens</italic></kwd><kwd>pathogenesis related genes</kwd><kwd>crinkler</kwd></kwd-group><funding-group><award-group><funding-source id="cn001">National Research Foundation<named-content content-type="fundref-id">10.13039/501100001321</named-content></funding-source><award-id rid="cn001">76225</award-id></award-group><award-group><funding-source id="cn002">Department of Science and Technology, Republic of South Africa<named-content content-type="fundref-id">10.13039/501100001342</named-content></funding-source></award-group></funding-group><counts><fig-count count="6"></fig-count><table-count count="4"></table-count><equation-count count="0"></equation-count><ref-count count="102"></ref-count><page-count count="15"></page-count><word-count count="10449"></word-count></counts></article-meta></front><body><sec sec-type="intro" id="s1"><title>Introduction</title><p>Species of the Oomycete genus <italic>Phytophthora</italic> are the most economically important pathogens of plants worldwide (Zentmyer, <xref rid="B101" ref-type="bibr">1983</xref>; Erwin and Ribeiro, <xref rid="B27" ref-type="bibr">1996</xref>). Of critical concern to the forestry industry is <italic>Phytophthora cinnamomi</italic> Rands, one of the most pathogenic and damaging species that affects agriculture, forestry, and native forests worldwide (Linde et al., <xref rid="B48" ref-type="bibr">1999</xref>; Brasier, <xref rid="B16" ref-type="bibr">2008</xref>; Hansen, <xref rid="B41" ref-type="bibr">2008</xref>; Oβwald et al., <xref rid="B64" ref-type="bibr">2014</xref>). In <italic>Eucalyptus, P. cinnamomi</italic> has threatened the productivity of plantations (FAO, <xref rid="B31" ref-type="bibr">2007</xref>; Wingfield et al., <xref rid="B96" ref-type="bibr">2011</xref>) and caused extensive damage to native ecosystems including <italic>E. marginata</italic> forests in Western Australia (Podger et al., <xref rid="B65" ref-type="bibr">1967</xref>; Burgess et al., <xref rid="B17" ref-type="bibr">1999</xref>) and native vegetation of the Western Cape of South Africa (Vonbroembsen and Kruger, <xref rid="B92" ref-type="bibr">1985</xref>). Eucalypt plantations contribute significantly to the economy of South Africa (Godsmark, <xref rid="B37" ref-type="bibr">2009</xref>). Susceptible cold-tolerant <italic>Eucalyptus</italic> plantations have been affected by various <italic>Phytophthora</italic> species to such an extent that some valuable species such as <italic>E. fastigata</italic> and <italic>E. fraxinoides</italic> are no longer cultivated (Linde et al., <xref rid="B49" ref-type="bibr">1994</xref>; Wingfield and Kemp, <xref rid="B95" ref-type="bibr">1994</xref>). <italic>Eucalyptus nitens</italic> is considered resistant to <italic>P. cinnamomi</italic> in its native environment but succumbs to the pathogen in plantations (Cahill et al., <xref rid="B19" ref-type="bibr">2008</xref>). <italic>P. cinnamomi</italic>, an introduced stramenopile pathogen (Adl et al., <xref rid="B3" ref-type="bibr">2005</xref>, <xref rid="B4" ref-type="bibr">2012</xref>) severely affected stands of <italic>E. nitens</italic> in South Africa (Maseko, <xref rid="B54" ref-type="bibr">2010</xref>).</p><p>Plant-pathogen interactions in forest systems have not been as well studied at a genomic level as it has for herbaceous crops. The recent availability of the genome sequence of <italic>E. grandis</italic> (Myburg et al., <xref rid="B60" ref-type="bibr">2014</xref>) has provided a valuable resource for transcriptomic studies to dissect defense responses in related <italic>Eucalyptus</italic> species. RNA sequencing (RNA-seq) has contributed knowledge towards several host responses during pathogen challenge (Xu et al., <xref rid="B99" ref-type="bibr">2011</xref>, <xref rid="B98" ref-type="bibr">2012</xref>; Dowen et al., <xref rid="B25" ref-type="bibr">2012</xref>; Martinelli et al., <xref rid="B53" ref-type="bibr">2012</xref>; Savory et al., <xref rid="B74" ref-type="bibr">2012</xref>; Tremblay et al., <xref rid="B90" ref-type="bibr">2012</xref>). Unlike previous probe based methods which require separation of host and pathogen cells, RNA-seq has allowed the study of both host and pathogen transcriptomics simultaneously. This technique, known as dual RNA-seq (reviewed in Westermann et al., <xref rid="B94" ref-type="bibr">2012</xref>) allows the detection of minute amounts of pathogen RNA. It does not require predesigned species specific probes and is more sensitive than the previous methods of microarrays and northern blotting (Kunjeti et al., <xref rid="B45" ref-type="bibr">2012</xref>; Tierney et al., <xref rid="B86" ref-type="bibr">2012</xref>; Westermann et al., <xref rid="B94" ref-type="bibr">2012</xref>; Camilios-Neto et al., <xref rid="B20" ref-type="bibr">2014</xref>; Choi et al., <xref rid="B22" ref-type="bibr">2014</xref>; Hayden et al., <xref rid="B42" ref-type="bibr">2014</xref>). Pathogen RNA-seq data can be further mined for clues to pathogenicity (ability to cause disease) and virulence (degree of damage or pathology) factors based on functional genetics studies conducted in various host-pathogen interactions. The plant-host interactions database provides such data for comparative analysis (Winnenburg et al., <xref rid="B97" ref-type="bibr">2006</xref>).</p><p>An enhanced understanding of the defense response of plants to <italic>P. cinnamomi</italic> will facilitate the production of resistant plants (Eshraghi et al., <xref rid="B28" ref-type="bibr">2014a</xref>). Several RNA-seq host response studies to <italic>Phytophthora</italic> spp. have been undertaken to date (Kunjeti et al., <xref rid="B45" ref-type="bibr">2012</xref>; Ali et al., <xref rid="B6" ref-type="bibr">2014</xref>; Chen et al., <xref rid="B21" ref-type="bibr">2014</xref>). The host responses of raspberry to <italic>P. rubi</italic>, and those of potato tubers to <italic>P. infestans</italic>, were successfully profiled using RNA-seq (Ward and Weber, <xref rid="B93" ref-type="bibr">2012</xref>; Gao et al., <xref rid="B34" ref-type="bibr">2013</xref>). This technique has also been applied to a native forest system, with the response of the oak <italic>Notholithocarpus densiflorus</italic> to <italic>P. ramorum</italic> elucidated (Kunjeti et al., <xref rid="B45" ref-type="bibr">2012</xref>; Ward and Weber, <xref rid="B93" ref-type="bibr">2012</xref>; Gao et al., <xref rid="B34" ref-type="bibr">2013</xref>; Ali et al., <xref rid="B6" ref-type="bibr">2014</xref>; Chen et al., <xref rid="B21" ref-type="bibr">2014</xref>; Hayden et al., <xref rid="B42" ref-type="bibr">2014</xref>).</p><p>The genome sequence of <italic>P. cinnamomi var. cinnamomi</italic> is currently available as a draft assembly of 77.97 Mbp and a sequence read coverage depth of 69.6x (Reeve, 2012, unpublished; JGI Project identity: 1003775). This is an invaluable resource that provides insight into pathogenicity determinants in this species. This has been demonstrated for other <italic>Phytophthora</italic> species sequenced genomes (e.g., <italic>P. infestans, P. sojae, P. ramorum</italic>, reviewed in Jiang and Tyler, <xref rid="B44" ref-type="bibr">2012</xref>).</p><p><italic>Phytophthora</italic> species are able to manipulate their hosts to their own advantage. For example, <italic>P. infestans</italic> manipulates its host to suit its life-style by suppressing the hypersensitive response (HR) in potato during its biotrophic phase, then manipulating the induction of HR during the necrotrophic phase (Bos et al., <xref rid="B15" ref-type="bibr">2010</xref>; Gilroy et al., <xref rid="B36" ref-type="bibr">2011</xref>). This type of manipulation could be a trend in other <italic>Phytophthora</italic> interactions (Belhaj et al., <xref rid="B12" ref-type="bibr">2009</xref>; Porter et al., <xref rid="B66" ref-type="bibr">2009</xref>). Effectors excreted during this interaction are primarily crinklers (CRN), a family of proteins expressed in all plant pathogenic oomycetes, and RxLRs which are confined to only <italic>Phytophthora</italic> species (Stam et al., <xref rid="B81" ref-type="bibr">2013b</xref>; Chen et al., <xref rid="B21" ref-type="bibr">2014</xref>).</p><p>Host defense responses are mediated through different mechanisms, and the timing and degree to which these are activated could determine the outcome of the interaction between a plant and pathogen (Tao et al., <xref rid="B84" ref-type="bibr">2003</xref>). A factor driving compatible interactions has been revealed by several studies to involve a mass down-regulation of defense genes (Schlink et al., <xref rid="B76" ref-type="bibr">2010</xref>). Pathways associated with these genes include the defense hormone salicylic acid (SA) which is associated with biotrophic defense responses, jasmonic acid (JA), and ethylene (ET) which are associated with necrotrophic defense responses, and abscisic acid (ABA) which is associated with abiotic stress as well as pathogen defense (Bari and Jones, <xref rid="B10" ref-type="bibr">2009</xref>). The host responses elicited by <italic>P. cinnamomi</italic> have been studied in different woody species at various levels including anatomical, physiological, biochemical, and molecular levels (recently reviewed in Oβwald et al., <xref rid="B64" ref-type="bibr">2014</xref>). Some of the major findings in these studies highlight the importance of correctly regulated HR and reactive oxygen species (ROS) and synthesis of phenylpropanoid pathway-related substances such as flavonoids, gibberellic acid (GA) and lignin. <italic>PR</italic>-<italic>1</italic> and <italic>PR</italic>-<italic>5</italic> feature in several interactions as possible resistance factors.</p><p>Multiple pathogenesis related (<italic>PR</italic>) gene classes are differentially regulated against <italic>Phytophthora</italic> and are thought to be important for successful defense (Moy et al., <xref rid="B59" ref-type="bibr">2004</xref>; Schlink, <xref rid="B75" ref-type="bibr">2009</xref>; Attard et al., <xref rid="B9" ref-type="bibr">2010</xref>). The over-expression of specific <italic>PR</italic> genes have conferred tolerance against various <italic>Phytophthora</italic> spp. (Alexander et al., <xref rid="B5" ref-type="bibr">1993</xref>; Fagoaga et al., <xref rid="B30" ref-type="bibr">2001</xref>; Sarowar et al., <xref rid="B73" ref-type="bibr">2009</xref>; Pushin et al., <xref rid="B68" ref-type="bibr">2010</xref>; Acharya et al., <xref rid="B1" ref-type="bibr">2013</xref>; He et al., <xref rid="B43" ref-type="bibr">2013</xref>).</p><p>The <italic>E. nitens–P. cinnamomi</italic> interaction provided a novel system to study a compatible host-pathogen interaction using a dual RNA-sequencing approach. The aim of this study was to (i) discover pathogenicity factors produced by <italic>P. cinnamomi</italic> (ii) to determine the <italic>E. nitens</italic> defense response to the pathogen, and (iii) to identify host genes that could potentially be suppressed by the pathogen to promote susceptibility. We observed, among other responses, high expression of a putative <italic>P. cinnamomi</italic> crinkler effector <italic>in planta</italic> and the down-regulation of a <italic>PR</italic>-9 gene, which may represent a common host effector target in <italic>E. nitens</italic>; two factors possibly contributing to the susceptible outcome of the interaction.</p></sec><sec sec-type="methods" id="s2"><title>Methods</title><sec><title>Inoculated plant material</title><p><italic>E. nitens</italic> seedlings were obtained from parents that were part of a third generation commercial breeding program (Sappi Forests Research, Shaw Research Centre, KwaZulu-Natal, South Africa) The criterion for selection was based on wood density gain. An MLRelate analysis, using the microsatellite markers developed by Faria et al. (<xref rid="B32" ref-type="bibr">2010</xref>), determined that the individuals from the Sappi breeding population showed higher relatedness to each other than those within the natural Australian <italic>E. nitens</italic> population (Melissa Reynolds, Forest Molecular Genetics, University of Pretoria). Previous sampling in <italic>E. nitens</italic> stands in South Africa have shown root rot due to <italic>P. cinnamomi</italic> (Maseko, <xref rid="B54" ref-type="bibr">2010</xref>).</p><p>The <italic>E. nitens</italic> seedlings were grown in pine-bark seedling mix until stem thickness was >0.5 cm (~1 year), then stem inoculated with <italic>P. cinnamomi</italic> (CMW26310, Forestry and Agricultural Biotechnology Institute culture collection). A 4 mm cork borer and mycelial plug on cV8 agar [cV8A; modified from Erwin and Ribeiro (<xref rid="B27" ref-type="bibr">1996</xref>): 200 ml/L V8 juice (Campbell Soup Company, Camden, New Jersey), 20 g/L CaCO<sub>3</sub> (Merck), 20 g/L agar)] was used for inoculations. Mock-inoculated plants were treated identically to infected trees, with a sterile cV8 agar plug. Inoculation sites were covered with damp sterile cheesecloth, tinfoil, and Parafilm (Parafilm, Chicago, IL).</p><p>Stems were inoculated at two sites, 10 cm apart. In the attempt to represent the typical responses to <italic>P. cinnamomi</italic> in commercially grown <italic>E. nitens</italic>, for both the mock-inoculated control and inoculated trees, stem tissue was harvested from 18 trees (which consisted of three pooled biological replicates of six trees each) at 5 days post inoculation (dpi). Three centimeters of stem tissue was harvested per inoculation site, with 1.5 cm of stem tissue below and above the center of the site. Harvested material was immediately frozen in liquid nitrogen.</p><p>Since sampling was destructive, nine extra trees were used to observe symptom development for 6 weeks following inoculation. Beneath-bark lesions were measured in other trials to statistically validate the effectivity of inoculation. For these lesions, a Shapiro-Wilk test was performed in GraphPad Prism 6 (Motulsky, <xref rid="B58" ref-type="bibr">1999</xref>) and the non-parametric Mann-Whitney test was used to assess significance at a 95% confidence level.</p></sec><sec><title>Microscopy</title><sec><title>Preparation of plant material</title><p>Approximately 1.5–2 cm of stem tissue surrounding the inoculation site of <italic>P. cinnamomi</italic> inoculated and mock-inoculated <italic>E. nitens</italic> tissue was harvested in triplicate at 24 h post inoculation (hpi), 48 hpi, 96 hpi, and 1 week post inoculation (wpi). The harvested tissue was fixed in formalin-acetic acid-alcohol [FAA; 100 ml/L formalin, 50 ml/L glacial acetic acid, 500 ml/L 95% ethanol]. For confocal microscopy, thin longitudinal- and cross-sections were made of stem tissue away from the immediate vicinity of the inoculation site. These sections were stained in 0.01% Calcofluor white fluorescent brightener 28 (Sigma-Aldrich®).</p></sec><sec><title>Visualization</title><p>Representative stem tissue samples from each time-point were visualized under a Stemi SV6 stereo microscope (Zeiss, Munchen, Germany). Images were captured using an AxioCamMRc digital camera (Zeiss) and Axiovision 4.7 software (Zeiss). The presence of hyphae inside the sampled tissue at various time-points was verified through use of a confocal laser scanning microscope (CLSM 510 Meta, Zeiss). To view Calcofluor-stained tissue, a wavelength of 405 nm was used, and a 543 nm wavelength was used to visualize autofluorescence. LSM Image Browser v4.2.0.121 (Zeiss) was used to view images generated from the confocal microscopy.</p></sec><sec><title>RNA extraction and quality analysis</title><p>RNA was isolated using a modified cetyl-trimethyl-ammonium-bromide (CTAB) method (Naidoo et al., <xref rid="B61" ref-type="bibr">2013</xref>). On-column DNAse treatment with 10 units DNaseI (Fermentas, Ontario, Canada) and RNA purification was performed with the RNeasy® Mini kit (Qiagen, Valencia, California). Quality analysis was done on a 2100 Bioanalyzer (Agilent, Santa Clara, California).</p></sec><sec><title>RNA sequencing</title><p>Approximately 20 μg total RNA for each sample was submitted for sequencing at Beijing Genomics Institute (BGI, Beijing, China). Sequencing of mRNA was performed with random fragmentation of the mRNA and adapter ligation. Fifty bp paired end reads were obtained using an Illumina HiSeq 2000 (Illumina, San Diego, CA).</p></sec></sec><sec><title>Bioinformatic analysis</title><sec><title>Quality analysis and filtering</title><p>Adaptors, low quality reads, and reads with more than 10% unknown nucleotides were removed from the dataset by BGI. The Galaxy platform (Giardine et al., <xref rid="B35" ref-type="bibr">2005</xref>; Blankenberg et al., <xref rid="B14" ref-type="bibr">2010b</xref>; Goecks et al., <xref rid="B38" ref-type="bibr">2010</xref>) was used to analyze and process the RNA-seq reads. FASTQ Groomer (Blankenberg et al., <xref rid="B13" ref-type="bibr">2010a</xref>) and FASTQC (Babraham Bioinformatics, <ext-link ext-link-type="uri" xlink:href="http://www.bioinformatics.babraham.ac.uk/projects/fastqc/">http://www.bioinformatics.babraham.ac.uk/projects/fastqc/</ext-link>) were used to format reads and to assess read quality.</p></sec><sec><title>Mapping and transcript expression analysis of the host</title><p>Mapping to the <italic>E. grandis</italic> v1.1 genome was done with Bowtie (Langmead et al., <xref rid="B46" ref-type="bibr">2009</xref>) and TopHat v1.3.1 (Trapnell et al., <xref rid="B88" ref-type="bibr">2009</xref>), allowing for 2 bp mismatches per 50 bp read and a maximum intron length of 10,000 bp. Mapping statistics were verified using SAMtools flagstat (Li et al., <xref rid="B47" ref-type="bibr">2009</xref>). Assembly of mapped reads and calculation of expression values of predicted <italic>E. grandis</italic> transcripts as fragments per kilobase of transcript per million fragments (FPKM) was performed by Cufflinks (Trapnell et al., <xref rid="B89" ref-type="bibr">2010</xref>). Significant differential expression analysis was done with Cuffdiff (Trapnell et al., <xref rid="B89" ref-type="bibr">2010</xref>), where parameter settings were changed to allow for a minimum alignment count of 1000, a false discovery rate of 0.05, as well as quartile normalization and bias correction. Additional parameter settings were set to an average fragment length of 49 bp and a standard deviation of 10 bp for the fragment lengths.</p></sec><sec><title>Mapping and transcript expression analysis of the pathogen</title><p>Reads from the three uninoculated samples and the three inoculated samples were mapped to the <italic>P. cinnamomi</italic> var <italic>cinnamomi</italic> draft genome downloaded from the Joint Genome Institute (Reeve, 2012, unpublished; JGI Project identity: 1003775). The genome assembly, based on Illumina, 454 and Sanger sequencing, is 77.97 Mbp and the sequence read coverage depth is 69.6x (Grigoriev et al., <xref rid="B39" ref-type="bibr">2012</xref>). Mapping was performed as described above and assembly of reads and FPKM value were generated using Cufflinks. Any genes or transcripts showing an FPKM value above 100 in the control samples were considered conserved eukaryotic genes and removed from further analysis. Remaining genes or transcripts which showed FPKM values >100 in the three inoculated samples with a coefficient of variation < 0.2 were considered further. Approximately 280 genes satisfied this criteria and were subsequently analyzed using the pathogen host interactions (PHI) database (<ext-link ext-link-type="uri" xlink:href="http://www.phi-base.org/">http://www.phi-base.org/</ext-link> Winnenburg et al., <xref rid="B97" ref-type="bibr">2006</xref>) to determine pathogenicity or virulence factors expressed <italic>in planta</italic> using a local BLASTP search in CLCBio main workbench (version 6.1; Qiagen). The database was downloaded in July 2014 and hits with the lowest <italic>e</italic>-value were considered. Selected genes were also subjected to Blast2GO® analysis to annotate the gene models.</p></sec><sec><title>Gene ontology over-representation analysis of host transcripts</title><p>Microsoft Excel 2007 (Microsoft, Redmond, WA) was used to match significantly differentially expressed <italic>E. grandis</italic> v1.1 gene and transcript models to TAIR10 and TAIR9 identifiers based on a reciprocal BLAST analysis. The significantly differentially expressed genes (and transcripts for which the representative gene model was not differentially expressed) with TAIR10 putative orthologs were divided into up- and down-regulated datasets, which were analyzed for gene ontology (GO) over-representation in BiNGO v2.44 (Maere et al., <xref rid="B51" ref-type="bibr">2005</xref>) using the Cytoscape v2.8.3a platform (Shannon et al., <xref rid="B78" ref-type="bibr">2003</xref>). Over-representation was evaluated against the <italic>Arabidopsis thaliana</italic> genome in the categories for “biological processes,” “molecular function,” and “cellular component.” A hypergeometric test with a Benjamini & Hochberg FDR correction of 0.05 was used. Understanding of biological pathways was aided by MapMan v3.5.1R2 (Thimm et al., <xref rid="B85" ref-type="bibr">2004</xref>).</p></sec><sec><title>RT-qPCR</title><p>Genomic contamination in total RNA samples was removed by treating extracted total RNA samples with RNase-free DNaseI enzyme (Qiagen Inc., Valencia, CA). Total RNA samples were then purified using the RNeasy® MinElute Kit (Qiagen Inc.) and subsequently analyzed using a Bio-Rad Experion automated electrophoresis system (Bio-Rad Laboratories, Hercules, CA, USA), to determine RNA integrity. The Improm-IITM Reverse Transcription System (Promega, Wisconsin, USA) was used to synthesize first strand cDNA from purified RNA samples. Primers were designed using Primer Designer 4 v4.20 (Sci Ed Central, Cary, North Carolina, USA). Primer pairs are indicated in Table <xref ref-type="table" rid="T1">1</xref>.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>Primer sequences for <italic>Eucalyptus nitens</italic> RT-qPCR target and reference genes</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Eucalyptus ID<xref ref-type="table-fn" rid="TN1"><sup>*</sup></xref></bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene name</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Forward primer</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Reverse primer</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.B03520</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrWRKY75</italic></td><td valign="top" align="left" rowspan="1" colspan="1">AAGCGCCAGCAGCGGTGGATGAGAA</td><td valign="top" align="left" rowspan="1" colspan="1">TGCAGCCGTGGAACGTGTCAACGGTA</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.F02181</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrLRR-RLK7</italic></td><td valign="top" align="left" rowspan="1" colspan="1">TTGGTGAATCTCTGGCGACTTGAGC</td><td valign="top" align="left" rowspan="1" colspan="1">GACAGATTGACGAGAGCCTCTGGAACT</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.H02533</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrNRT2.5</italic></td><td valign="top" align="left" rowspan="1" colspan="1">TGTCCGAATGGAGCGACAAGGAGAA</td><td valign="top" align="left" rowspan="1" colspan="1">ACACGGTGCACGAGTACATGAACAG</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.I01495</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrPR-3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">GTATTGCTCTCCTAATCC</td><td valign="top" align="left" rowspan="1" colspan="1">CATTGCCCGTAGTTATAG</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.J01100</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrMLO</italic></td><td valign="top" align="left" rowspan="1" colspan="1">GTCAAGAGGTCATTAGAAG</td><td valign="top" align="left" rowspan="1" colspan="1">TAGAAGCAAGAAGATAACG</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.I01779</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrARF</italic></td><td valign="top" align="left" rowspan="1" colspan="1">TGCGTACCGAGTTGTTGAGG</td><td valign="top" align="left" rowspan="1" colspan="1">GTTGCACAGGTGCTCTGGAT</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.B02864</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrFBA</italic></td><td valign="top" align="left" rowspan="1" colspan="1">TGAAGACATGGCAAGGAAGG</td><td valign="top" align="left" rowspan="1" colspan="1">GTACCGAAGTTGCTCCGAAT</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Eucgr.G01186</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>EgrTUB</italic></td><td valign="top" align="left" rowspan="1" colspan="1">TGAGGTCTTCTCGCGCATTG</td><td valign="top" align="left" rowspan="1" colspan="1">AGAGATCTGGCGCAGACAC</td></tr></tbody></table><table-wrap-foot><fn id="TN1"><label>*</label><p><italic>Eucalyptus grandis identities according to <ext-link ext-link-type="uri" xlink:href="http://www.phytozome.net">www.phytozome.net</ext-link></italic>.</p></fn></table-wrap-foot></table-wrap><p>Real-time quantitative reverse transcriptase PCR (RT-qPCR) was conducted according to the Minimum Information for Publication of RT-qPCR Experiments (MIQE) guidelines (Bustin et al., <xref rid="B18" ref-type="bibr">2009</xref>) using a LightCycler® 480 Real-Time PCR system (Roche Diagnostics, GmBh, Basa, Switzerland) following parameters described in Naidoo et al. (<xref rid="B61" ref-type="bibr">2013</xref>). The qBASEplus v1.0 (Biogazelle NV, Belgium) software package was used to perform normalization and relative quantification. Significance was determined using a two-tailed Student's <italic>t</italic>-test in Microsoft® Office Excel 2010.</p></sec><sec><title>Phylogenetic analysis</title><p>Protein sequences were retrieved from GenBank, Phytozome and JGI, and aligned using MUSCLE (Edgar, <xref rid="B26" ref-type="bibr">2004</xref>). RAxML (Stamatakis, <xref rid="B82" ref-type="bibr">2006</xref>) was used to search for the best scoring maximum likelihood tree with rapid bootstrapping, with GAMMA BLOSUM62 as an evolutionary model. A Bayesian inference analysis was conducted in MrBayes 3.2.2 (Ronquist and Huelsenbeck, <xref rid="B72" ref-type="bibr">2003</xref>). Two chains were sampled once every thousand generations out of a total of one million generations. Trees were summarized with a 10% burn-in. All programs used were housed in Geneious software package version 7.1.5.</p></sec></sec></sec><sec sec-type="results" id="s3"><title>Results</title><p><italic>P. cinnamomi</italic> infected tissue for RNA-seq profiling was obtained by inoculating the stems of <italic>E. nitens</italic> seedlings and harvesting at 5 dpi. At this time-point, slight browning was visible around inoculation sites of control plants, whereas lesions of inoculated plants extended to the boundaries of the 3 cm sampled area (Figure <xref ref-type="fig" rid="F1">1A</xref>). At 6 wpi lesion length was pronounced compared to the mock-inoculated controls (Figure <xref ref-type="fig" rid="F1">1B</xref>). At 4 wpi, ~50% of the inoculated plants showed mortality. Lesion length was measured for live plants only. The efficacy of inoculation was verified by the presence of hyphae in stem tissue and lesion development over a 4 day time-course (Figure <xref ref-type="fig" rid="F1">1C</xref>).</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Symptom development in <italic>Eucalyptus nitens</italic> following challenge with <italic>Phytophthora cinnamomi</italic>. (A)</bold> A section of 1.5 cm stem tissue was harvested below and above the site of inoculation at 5 dpi. <bold>(i)</bold> Mock-inoculated and <bold>(ii)</bold> inoculated. <bold>(B)</bold> Lesions on <italic>E. nitens</italic> seedlings 6 wpi with <italic>P. cinnamomi</italic>. The small letters indicate that lesions on inoculated seedlings were significantly larger than the mock-inoculated negative control at <italic>p</italic> < 0.05 using the Mann–Whitney test for non-parametric data. Error bars show standard error based on <italic>n</italic> = 12 replicates. <bold>(C)</bold> Confocal microscopy of a longitudinal stem section showing <italic>P. cinnamomi</italic> hyphae (white arrows) at 4 dpi.</p></caption><graphic xlink:href="fpls-07-00191-g0001"></graphic></fig><sec><title>RNA-sequencing and mapping to <italic>Phytophthora cinnamomi</italic> and <italic>Eucalyptus grandis</italic> genomes</title><p>Approximately 36 million reads were obtained per sample, and reads were mapped to the <italic>E. grandis</italic> genome version 1.1 (Table <xref ref-type="table" rid="T2">2</xref>). In addition to host transcripts, we mapped <italic>P. cinnamomi</italic> transcripts expressed <italic>in planta</italic>, based on the draft <italic>P. cinnamomi</italic> assembly. A low percentage of mapping (0.08%) was observed in the control (mock inoculated) samples, which were considered conserved eukaryotic gene sequences. On average, 1% of the reads mapped to the <italic>P. cinnamomi</italic> genome in the inoculated samples. Approximately 78% of the transcripts derived from both inoculated and mock-inoculated <italic>E. nitens</italic> samples mapped to the <italic>E. grandis</italic> genome (Table <xref ref-type="table" rid="T2">2</xref>). The number of expressed genes and the average FPKM values were similar across the three biological replicates of each treatment which provided confidence that the samples were treated in a consistent manner and the results were comparable across data sets (Table <xref ref-type="table" rid="T2">2</xref>).</p><table-wrap id="T2" position="float"><label>Table 2</label><caption><p><bold>Flagstat and FastQC RNA-seq mapping statistics of <italic>Eucalyptus nitens</italic> reads to the v1.1 <italic>Eucalyptus grandis</italic> and <italic>Phytophthora cinnamomi</italic> var <italic>cinnamomi</italic> genomes</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Sample name</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Total reads mapped to <italic>E. grandis</italic></bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Properly paired to <italic>E. grandis</italic> (%)<xref ref-type="table-fn" rid="TN2"><sup>a</sup></xref></bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Singletons mapped to <italic>E. grandis</italic> (%)<xref ref-type="table-fn" rid="TN3"><sup>b</sup></xref></bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>% GC content</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Expressed genes in host</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Average FPKM in host</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Total reads mapped to pathogen</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>% reads mapped to pathogen</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Control 1</td><td valign="top" align="center" rowspan="1" colspan="1">37444809</td><td valign="top" align="center" rowspan="1" colspan="1">66.44</td><td valign="top" align="center" rowspan="1" colspan="1">10.24</td><td valign="top" align="center" rowspan="1" colspan="1">50</td><td valign="top" align="center" rowspan="1" colspan="1">29024</td><td valign="top" align="center" rowspan="1" colspan="1">493598</td><td valign="top" align="center" rowspan="1" colspan="1">30756</td><td valign="top" align="center" rowspan="1" colspan="1">0.08</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Control 2</td><td valign="top" align="center" rowspan="1" colspan="1">36111678</td><td valign="top" align="center" rowspan="1" colspan="1">68.02</td><td valign="top" align="center" rowspan="1" colspan="1">10.16</td><td valign="top" align="center" rowspan="1" colspan="1">50</td><td valign="top" align="center" rowspan="1" colspan="1">29250</td><td valign="top" align="center" rowspan="1" colspan="1">492972</td><td valign="top" align="center" rowspan="1" colspan="1">29274</td><td valign="top" align="center" rowspan="1" colspan="1">0.08</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Control 3</td><td valign="top" align="center" rowspan="1" colspan="1">37060251</td><td valign="top" align="center" rowspan="1" colspan="1">68.76</td><td valign="top" align="center" rowspan="1" colspan="1">8.90</td><td valign="top" align="center" rowspan="1" colspan="1">49</td><td valign="top" align="center" rowspan="1" colspan="1">29135</td><td valign="top" align="center" rowspan="1" colspan="1">467006</td><td valign="top" align="center" rowspan="1" colspan="1">29116</td><td valign="top" align="center" rowspan="1" colspan="1">0.08</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Inoculated 1</td><td valign="top" align="center" rowspan="1" colspan="1">37234371</td><td valign="top" align="center" rowspan="1" colspan="1">66.13</td><td valign="top" align="center" rowspan="1" colspan="1">11.65</td><td valign="top" align="center" rowspan="1" colspan="1">49</td><td valign="top" align="center" rowspan="1" colspan="1">29429</td><td valign="top" align="center" rowspan="1" colspan="1">471923</td><td valign="top" align="center" rowspan="1" colspan="1">444935</td><td valign="top" align="center" rowspan="1" colspan="1">1.19</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Inoculated 2</td><td valign="top" align="center" rowspan="1" colspan="1">36622434</td><td valign="top" align="center" rowspan="1" colspan="1">67.30</td><td valign="top" align="center" rowspan="1" colspan="1">12.48</td><td valign="top" align="center" rowspan="1" colspan="1">49</td><td valign="top" align="center" rowspan="1" colspan="1">29407</td><td valign="top" align="center" rowspan="1" colspan="1">497171</td><td valign="top" align="center" rowspan="1" colspan="1">552202</td><td valign="top" align="center" rowspan="1" colspan="1">1.51</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Inoculated 3</td><td valign="top" align="center" rowspan="1" colspan="1">36022978</td><td valign="top" align="center" rowspan="1" colspan="1">68.19</td><td valign="top" align="center" rowspan="1" colspan="1">10.18</td><td valign="top" align="center" rowspan="1" colspan="1">49</td><td valign="top" align="center" rowspan="1" colspan="1">29576</td><td valign="top" align="center" rowspan="1" colspan="1">473466</td><td valign="top" align="center" rowspan="1" colspan="1">196534</td><td valign="top" align="center" rowspan="1" colspan="1">0.55</td></tr></tbody></table><table-wrap-foot><fn id="TN2"><label>a</label><p><italic>Number of proper pairs in proportion to the total reads mapped</italic>.</p></fn><fn id="TN3"><label>b</label><p><italic>Number reads where one from a pair in proportion to the total mapped</italic>.</p></fn></table-wrap-foot></table-wrap></sec><sec><title><italic>Phytophthora cinnamomi</italic> genes expressed in planta</title><p>The list of transcripts expressed in the three inoculated <italic>E. nitens</italic> samples with CV < 0.2 are provided as a Supplementary File (Table <xref ref-type="supplementary-material" rid="SM1">S1</xref>). Of these 283 genes, the genes with hits (<italic>E</italic>-value ~0) to the plant host interactions database described as loss in pathogenicity, avirulence determinants, or reduced virulence are indicated in Table <xref ref-type="table" rid="T3">3</xref>. Several of these have homology to transcripts with known roles in pathogenicity and virulence based on functional genetics experiments in other pathogen species. The highest expressed gene was a member of the CRN family protein. The <italic>P. cinnamomi</italic> putative CRN (JGI: Phyci261170) was aligned with other putative and described CRN family members and a maximum likelihood phylogenetic tree describing the relationship was produced. A congruent topology was recovered from Bayesian inference. The closest relationship was to a putative CRN protein from <italic>P. ramorum</italic>. Both the <italic>P. ramorum</italic> and <italic>P. cinammomi</italic> putative CRN proteins are closely related to the better characterized <italic>P. infestans</italic> CRN proteins (Figure <xref ref-type="fig" rid="F2">2</xref>).</p><table-wrap id="T3" position="float"><label>Table 3</label><caption><p><bold><italic>Phytophthora cinnamomi</italic> genes expressed <italic>in planta</italic> implicated in pathogenicity or virulence (<italic>E</italic>-value < 0.01) based on comparison to the plant-host interactions database</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene identity</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Average FPKM</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene ontology</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold><italic>E</italic>-value</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene name</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Knock-out phenotype</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>PHI base accession</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.822.3.1</td><td valign="top" align="center" rowspan="1" colspan="1">1443.83</td><td valign="top" align="left" rowspan="1" colspan="1">gi|301096130|ref|XP_002897163.1|Crinkler (CRN) family protein</td><td valign="top" align="center" rowspan="1" colspan="1">3.85E-91</td><td valign="top" align="left" rowspan="1" colspan="1">crn1</td><td valign="top" align="left" rowspan="1" colspan="1">Effector plant avirulence determinant</td><td valign="top" align="center" rowspan="1" colspan="1">656</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">estExt_fgenesh1_pg.C_680034</td><td valign="top" align="center" rowspan="1" colspan="1">1323.48</td><td valign="top" align="left" rowspan="1" colspan="1">hydrogen-transporting ATPase activity, rotational mechanism</td><td valign="top" align="center" rowspan="1" colspan="1">9.04E-26</td><td valign="top" align="left" rowspan="1" colspan="1">invC</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">645</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">estExt_Genewise1.C_2370044</td><td valign="top" align="center" rowspan="1" colspan="1">1096.91</td><td valign="top" align="left" rowspan="1" colspan="1">DNA binding</td><td valign="top" align="center" rowspan="1" colspan="1">5.16E-11</td><td valign="top" align="left" rowspan="1" colspan="1">GzLam002</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">1533</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.40.157.1</td><td valign="top" align="center" rowspan="1" colspan="1">950</td><td valign="top" align="left" rowspan="1" colspan="1">zinc ion binding, glutathione peroxidase activity, response to oxidative stress</td><td valign="top" align="center" rowspan="1" colspan="1">8.14E-35</td><td valign="top" align="left" rowspan="1" colspan="1">MoHYR1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2356</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">fgenesh1_kg.2_#_22_#_Locus405v1rpkm794.38</td><td valign="top" align="center" rowspan="1" colspan="1">915.58</td><td valign="top" align="left" rowspan="1" colspan="1">protein binding, transcription factor binding, GTP binding, ATP binding</td><td valign="top" align="center" rowspan="1" colspan="1">1.40E-67</td><td valign="top" align="left" rowspan="1" colspan="1">CLPT1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">339</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.76.61.1</td><td valign="top" align="center" rowspan="1" colspan="1">853.95</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, hydrolase activity, ATP binding, ATPase activity, ATPase activity</td><td valign="top" align="center" rowspan="1" colspan="1">7.85E-55</td><td valign="top" align="left" rowspan="1" colspan="1">PMR1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">440</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">estExt_Genewise1.C_610064</td><td valign="top" align="center" rowspan="1" colspan="1">741.59</td><td valign="top" align="left" rowspan="1" colspan="1">protein kinase activity, GTP binding, protein-tyrosine kinase activity</td><td valign="top" align="center" rowspan="1" colspan="1">1.27E-22</td><td valign="top" align="left" rowspan="1" colspan="1">MoSNF1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">1058</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">fgenesh1_kg.16_#_102_#_Locus840v1rpkm311.24</td><td valign="top" align="center" rowspan="1" colspan="1">731.62</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, FAD binding, oxidoreductase activity</td><td valign="top" align="center" rowspan="1" colspan="1">3.59E-04</td><td valign="top" align="left" rowspan="1" colspan="1">ALO1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">197</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">fgenesh1_kg.9_#_117_#_Locus4954v1rpkm35.55</td><td valign="top" align="center" rowspan="1" colspan="1">647.81</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, cofactor binding, oxidoreductase activity</td><td valign="top" align="center" rowspan="1" colspan="1">4.47E-32</td><td valign="top" align="left" rowspan="1" colspan="1">MGG</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">881</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">fgenesh1_pg.124_#_4</td><td valign="top" align="center" rowspan="1" colspan="1">620.76</td><td valign="top" align="left" rowspan="1" colspan="1">FAD binding, oxidoreductase activity, cell redox homeostasis, electron transport</td><td valign="top" align="center" rowspan="1" colspan="1">7.82E-06</td><td valign="top" align="left" rowspan="1" colspan="1">SID1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">1010</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">gm1.2704_g</td><td valign="top" align="center" rowspan="1" colspan="1">421.24</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, ATP binding, metabolism</td><td valign="top" align="center" rowspan="1" colspan="1">0.01</td><td valign="top" align="left" rowspan="1" colspan="1">ACL2</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">2387</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">gm1.12073_g</td><td valign="top" align="center" rowspan="1" colspan="1">324.79</td><td valign="top" align="left" rowspan="1" colspan="1">nucleoside triphosphatase activity, nucleotide binding, hydrolase activity</td><td valign="top" align="left" rowspan="1" colspan="1">2.38E-66</td><td valign="top" align="center" rowspan="1" colspan="1">PEX6</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">226</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">gm1.7056_g</td><td valign="top" align="center" rowspan="1" colspan="1">315.86</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, metabolism</td><td valign="top" align="center" rowspan="1" colspan="1">6.30E-17</td><td valign="top" align="left" rowspan="1" colspan="1">SidI</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2321</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">gm1.272_g</td><td valign="top" align="center" rowspan="1" colspan="1">294.34</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, acetate-CoA ligase activity, AMP binding, etabolism</td><td valign="top" align="center" rowspan="1" colspan="1">3.33E-22</td><td valign="top" align="left" rowspan="1" colspan="1">AKT1</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">133</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.31.72.1</td><td valign="top" align="center" rowspan="1" colspan="1">268.44</td><td valign="top" align="left" rowspan="1" colspan="1">microtubule motor activity, ATP binding, microtubule-based movement</td><td valign="top" align="center" rowspan="1" colspan="1">2.50E-32</td><td valign="top" align="left" rowspan="1" colspan="1">KIN2</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">465</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.1.234.1</td><td valign="top" align="center" rowspan="1" colspan="1">254.89</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, metabolism</td><td valign="top" align="center" rowspan="1" colspan="1">9.49E-12</td><td valign="top" align="left" rowspan="1" colspan="1">SidI</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2321</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.93.22.1</td><td valign="top" align="center" rowspan="1" colspan="1">254.29</td><td valign="top" align="left" rowspan="1" colspan="1">protein binding, protein kinase activity, protein-tyrosine kinase activity</td><td valign="top" align="center" rowspan="1" colspan="1">5.50E-22</td><td valign="top" align="left" rowspan="1" colspan="1">Ste11</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">2484</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.1.500.1</td><td valign="top" align="center" rowspan="1" colspan="1">204.35</td><td valign="top" align="left" rowspan="1" colspan="1">antioxidant activity, oxidoreductase activity</td><td valign="top" align="center" rowspan="1" colspan="1">5.61E-04</td><td valign="top" align="left" rowspan="1" colspan="1">TSA1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">386</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">estExt_Genemark1.C_2810025</td><td valign="top" align="center" rowspan="1" colspan="1">203.63</td><td valign="top" align="left" rowspan="1" colspan="1">electron-transferring-flavoprotein dehydrogenase activity, electron transport</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">SIDA</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">486</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.67.108.1</td><td valign="top" align="center" rowspan="1" colspan="1">199.31</td><td valign="top" align="left" rowspan="1" colspan="1">ATP binding</td><td valign="top" align="center" rowspan="1" colspan="1">1.08E-57</td><td valign="top" align="left" rowspan="1" colspan="1">LHS1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2058</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.82.257.1</td><td valign="top" align="center" rowspan="1" colspan="1">198.02</td><td valign="top" align="left" rowspan="1" colspan="1">ATP binding</td><td valign="top" align="center" rowspan="1" colspan="1">3.65E-13</td><td valign="top" align="left" rowspan="1" colspan="1">LHS1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2058</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.108.166.1</td><td valign="top" align="center" rowspan="1" colspan="1">195.13</td><td valign="top" align="left" rowspan="1" colspan="1">protein kinase activity, protein-tyrosine kinase activity</td><td valign="top" align="center" rowspan="1" colspan="1">2.83E-66</td><td valign="top" align="left" rowspan="1" colspan="1">MoCMK1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2158</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.2.24.1</td><td valign="top" align="center" rowspan="1" colspan="1">187.23</td><td valign="top" align="left" rowspan="1" colspan="1">helicase activity, nucleic acid binding, ATP dependent helicase activity, ATP binding</td><td valign="top" align="center" rowspan="1" colspan="1">9.73E-70</td><td valign="top" align="left" rowspan="1" colspan="1">VAD1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">423</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.184.44.1</td><td valign="top" align="center" rowspan="1" colspan="1">185.29</td><td valign="top" align="left" rowspan="1" colspan="1">protein kinase activity, protein-tyrosine kinase activity, protein serine/threonine kinase activity</td><td valign="top" align="center" rowspan="1" colspan="1">1.67E-51</td><td valign="top" align="left" rowspan="1" colspan="1">SNF1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">188</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">fgenesh1_pg.86_#_13</td><td valign="top" align="center" rowspan="1" colspan="1">184.79</td><td valign="top" align="left" rowspan="1" colspan="1">catalytic activity, aspartic-type endopeptidase activity, metabolism</td><td valign="top" align="center" rowspan="1" colspan="1">1.15E-31</td><td valign="top" align="left" rowspan="1" colspan="1">SidI</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2321</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">MIX7251_264_83</td><td valign="top" align="center" rowspan="1" colspan="1">180.35</td><td valign="top" align="left" rowspan="1" colspan="1">polygalacturonase activity, carbohydrate metabolism</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">Pcipg2</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">2343</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">gm1.8946_g</td><td valign="top" align="center" rowspan="1" colspan="1">164.67</td><td valign="top" align="left" rowspan="1" colspan="1">ATP binding, nucleotide binding, nucleoside triphosphatase activity, tRNA ligase activity</td><td valign="top" align="center" rowspan="1" colspan="1">2.70E-47</td><td valign="top" align="left" rowspan="1" colspan="1">ABC4</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">2067</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.2.738.1</td><td valign="top" align="center" rowspan="1" colspan="1">153.76</td><td valign="top" align="left" rowspan="1" colspan="1">hydrolase activity, cellulose binding, serine-type endopeptidase activity, blood coagulation</td><td valign="top" align="center" rowspan="1" colspan="1">1.21E-46</td><td valign="top" align="left" rowspan="1" colspan="1">CBEL</td><td valign="top" align="left" rowspan="1" colspan="1">Effector plant avirulence determinant</td><td valign="top" align="center" rowspan="1" colspan="1">660</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">fgenesh1_pg.112_#_14</td><td valign="top" align="center" rowspan="1" colspan="1">142.08</td><td valign="top" align="left" rowspan="1" colspan="1">gi|325187184|emb|CCA21725.1|bromodomain containing 2 putative [Albugo laibachii Nc14]</td><td valign="top" align="center" rowspan="1" colspan="1">1.63E-09</td><td valign="top" align="left" rowspan="1" colspan="1">GzBrom002</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">1317</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.11.45.1</td><td valign="top" align="center" rowspan="1" colspan="1">137.55</td><td valign="top" align="left" rowspan="1" colspan="1">phosphotransferase activity, alcohol group as acceptor</td><td valign="top" align="center" rowspan="1" colspan="1">1.02E-31</td><td valign="top" align="left" rowspan="1" colspan="1">VPS34</td><td valign="top" align="left" rowspan="1" colspan="1">Loss of pathogenicity</td><td valign="top" align="center" rowspan="1" colspan="1">195</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">e_gw1.74.48.1</td><td valign="top" align="center" rowspan="1" colspan="1">116.37</td><td valign="top" align="left" rowspan="1" colspan="1">protein binding, transcription factor binding, GTP binding, ATP binding, GTPase activity</td><td valign="top" align="center" rowspan="1" colspan="1">5.62E-40</td><td valign="top" align="left" rowspan="1" colspan="1">CLPT1</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">339</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">estExt_fgenesh1_pg.C_1470005</td><td valign="top" align="center" rowspan="1" colspan="1">110.97</td><td valign="top" align="left" rowspan="1" colspan="1">transporter activity, binding, ATPase activity, ATP binding, transport</td><td valign="top" align="center" rowspan="1" colspan="1">1.15E-26</td><td valign="top" align="left" rowspan="1" colspan="1">MgAtr4</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">310</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">gm1.14921_g</td><td valign="top" align="center" rowspan="1" colspan="1">103.14</td><td valign="top" align="left" rowspan="1" colspan="1">motor activity, ATP binding, myosin</td><td valign="top" align="center" rowspan="1" colspan="1">3.16E-114</td><td valign="top" align="left" rowspan="1" colspan="1">GzWing020</td><td valign="top" align="left" rowspan="1" colspan="1">Reduced virulence</td><td valign="top" align="center" rowspan="1" colspan="1">1648</td></tr></tbody></table></table-wrap><fig id="F2" position="float"><label>Figure 2</label><caption><p><bold>Maximum likelihood phylogenetic tree of the putative <italic>Phytophthora cinnamomi</italic> crinkler (CRN) protein in relation to CRN proteins in other <italic>Phytophthora</italic> species</bold>.</p></caption><graphic xlink:href="fpls-07-00191-g0002"></graphic></fig></sec><sec><title>Differentially expressed genes in <italic>Eucalyptus nitens</italic></title><p>After mapping to the genome, Cuffdiff was used to compare pathogen-inoculated <italic>E. nitens</italic> samples with the mock-inoculated controls. A total of 890 up-regulated and 585 down-regulated gene models were observed at a false discovery rate (FDR) of 0.05. The expression of a sub-set of differentially expressed genes <italic>EgrWRKY75, EgrPR-3, EgrNRT2.5, EgrMLO</italic>, and <italic>EgrLRR-RLK7</italic> were validated using RT-qPCR (Figure <xref ref-type="fig" rid="F3">3</xref>). The tissue for the RT-qPCR validation was sourced from a separate trial that was set up identically to the first trial, with three biological repeats. The expression patterns were comparable to RNA-seq results, with the correlation coefficient between the RNA-seq and the RT-qPCR expression being 0.73.</p><fig id="F3" position="float"><label>Figure 3</label><caption><p><bold>Expression validation of selected genes in <italic>Eucalyptus nitens</italic> under <italic>Phytophthora cinnamomi</italic> inoculated compared to mock inoculated conditions 5 days post inoculation</bold>. Gray bars represent RT-qPCR expression patterns and dark gray bars, RNA-seq expression patterns.</p></caption><graphic xlink:href="fpls-07-00191-g0003"></graphic></fig></sec><sec><title>Over-represented gene ontologies</title><p>Differentially expressed genes with matching TAIR10 IDs were used in BiNGO to test for over-representation against the <italic>A. thaliana</italic> genome as background. In the up-regulated dataset for biological processes, the majority of over-represented GO terms were related to defense (Figure <xref ref-type="fig" rid="F4">4</xref>). Several of the categories involved JA and ET signaling, and there were a few terms related to SA (Figure <xref ref-type="fig" rid="F4">4</xref> and Table <xref ref-type="supplementary-material" rid="SM1">S1</xref>). Phenylpropanoid pathway terms and aromatic compound synthesis related to flavonoid biosynthesis were also found in this dataset (Figure <xref ref-type="fig" rid="F4">4</xref> and Table <xref ref-type="supplementary-material" rid="SM2">S2</xref>). Another prominent term in the up-regulated dataset was response to water deprivation/water stress terms.</p><fig id="F4" position="float"><label>Figure 4</label><caption><p><bold>Over-represented Gene Ontologies in the category biological process for the genes up-regulated in response to <italic>Phytophthora cinnamomi</italic> challenge in <italic>Eucalyptus nitens</italic> at 5 dpi</bold>.</p></caption><graphic xlink:href="fpls-07-00191-g0004"></graphic></fig><p>Over-represented GO terms in the down-regulated dataset for biological processes (Figure <xref ref-type="fig" rid="F5">5</xref>) were predominantly related to growth, cell wall modifications, and cell wall chemistry. The phenylpropanoid pathway terms were related to lignin biosynthesis, as opposed to flavonoid synthesis in the up-regulated dataset (Figure <xref ref-type="fig" rid="F5">5</xref> and Table <xref ref-type="supplementary-material" rid="SM2">S2</xref>). There were minimal biotic stress-related terms, and hormone-related terms in this dataset such as auxin and gibberellin were apparent (Figure <xref ref-type="fig" rid="F5">5</xref> and Table <xref ref-type="supplementary-material" rid="SM1">S1</xref>). Photosynthesis-related terms were also over-represented.</p><fig id="F5" position="float"><label>Figure 5</label><caption><p><bold>Over-represented Gene Ontologies in the category biological process for the genes down-regulated in response to <italic>Phytophthora cinnamomi</italic> challenge in <italic>Eucalyptus nitens</italic> at 5 dpi</bold>.</p></caption><graphic xlink:href="fpls-07-00191-g0005"></graphic></fig><p>One of the noteworthy aspects of the RNA-seq data obtained was that several putative <italic>PR</italic> genes displayed particularly high fold-change values, mostly in the up-regulated dataset. This is summarized in Table <xref ref-type="table" rid="T4">4</xref>. Within the <italic>E. nitens</italic>- <italic>P. cinnamomi</italic> interaction, the most prominent putative <italic>PR</italic> genes were <italic>PR-1, PR-3</italic> (chitinase), and <italic>PR-5</italic> (thaumatin-like and osmotin). These were not only consistently highly up-regulated in inoculated tissue, but there were multiple <italic>E. nitens</italic> putative orthologs per <italic>A. thaliana</italic> gene that are all regulated at similar fold-change levels. Putative <italic>E. nitens</italic> orthologs of <italic>PR-4</italic> (chitin-binding), <italic>PR-8</italic> (chitinase class III), and <italic>PR-12</italic> (defensins) were up-regulated. The <italic>PR-9</italic> (peroxidase) and <italic>PR-10</italic> (ribonuclease-like) classes contained a mix of up- and down-regulated putative orthologs. <italic>PR-14</italic> (lipid transfer proteins) and <italic>PR-15</italic> (oxalate oxidase/germin) putative orthologs were all down-regulated.</p><table-wrap id="T4" position="float"><label>Table 4</label><caption><p><bold>Expression of pathogenesis related genes in response to <italic>Phytophthora cinnamomi</italic> inoculation in <italic>Eucalyptus nitens</italic></bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1"><bold>Gene family</bold></th><th align="left" rowspan="1" colspan="1"><bold>TAIR ID</bold></th><th align="left" rowspan="1" colspan="1"><bold><italic>E. grandis</italic> ID</bold></th><th align="left" rowspan="1" colspan="1"><bold>Description</bold></th><th align="center" rowspan="1" colspan="1"><bold>log<sup>2</sup> expression</bold></th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><italic>PR-1</italic></td><td align="left" rowspan="1" colspan="1">AT2G14580.1</td><td align="left" rowspan="1" colspan="1">Eucgr.D01552</td><td align="left" rowspan="1" colspan="1">Basic pathogenesis-related protein 1</td><td align="center" style="background-color:#da1f26" rowspan="1" colspan="1">4.56</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14580.1</td><td align="left" rowspan="1" colspan="1">Eucgr.G01140</td><td align="left" rowspan="1" colspan="1">Basic pathogenesis-related protein 1</td><td align="center" style="background-color:#da1f26" rowspan="1" colspan="1">4.40</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14580.1</td><td align="left" rowspan="1" colspan="1">Eucgr.G01148</td><td align="left" rowspan="1" colspan="1">Basic pathogenesis-related protein 1</td><td align="center" style="background-color:#da1f26" rowspan="1" colspan="1">4.37</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14580.1</td><td align="left" rowspan="1" colspan="1">Eucgr.D01560</td><td align="left" rowspan="1" colspan="1">Basic pathogenesis-related protein 1</td><td align="center" style="background-color:#da1f26" rowspan="1" colspan="1">4.36</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14580.1</td><td align="left" rowspan="1" colspan="1">Eucgr.G01171</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related gene 1</td><td align="center" style="background-color:#da1f26" rowspan="1" colspan="1">4.31</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14610.1</td><td align="left" rowspan="1" colspan="1">Eucgr.G01134</td><td align="left" rowspan="1" colspan="1">Basic pathogenesis-related protein 1</td><td align="center" style="background-color:#b63625" rowspan="1" colspan="1">3.34</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14610.1</td><td align="left" rowspan="1" colspan="1">Eucgr.G01137</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related gene 1</td><td align="center" style="background-color:#b73a27" rowspan="1" colspan="1">3.24</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14610.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L02505</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related gene 1</td><td align="center" style="background-color:#b63625" rowspan="1" colspan="1">3.14</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G14610.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L01707</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related gene 1</td><td align="center" style="background-color:#b03e26" rowspan="1" colspan="1">3.13</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-3</italic>—Chitinase class I, II, IV, VI, VII</td><td align="left" rowspan="1" colspan="1">AT3G12500.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L00941</td><td align="left" rowspan="1" colspan="1">Basic chitinase</td><td align="center" style="background-color:#c42d27" rowspan="1" colspan="1">4.02</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G12500.1</td><td align="left" rowspan="1" colspan="1">Eucgr.J02519</td><td align="left" rowspan="1" colspan="1">Basic chitinase</td><td align="center" style="background-color:#c42d27" rowspan="1" colspan="1">3.94</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G12500.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L00938</td><td align="left" rowspan="1" colspan="1">Basic chitinase</td><td align="center" style="background-color:#c42d27" rowspan="1" colspan="1">3.93</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G54420.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H00326</td><td align="left" rowspan="1" colspan="1">Homolog of carrot EP3-3 chitinase</td><td align="center" style="background-color:#c42d27" rowspan="1" colspan="1">3.75</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G54420.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H00321</td><td align="left" rowspan="1" colspan="1">Homolog of carrot EP3-3 chitinase</td><td align="center" style="background-color:#c42d27" rowspan="1" colspan="1">3.75</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G12500.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L00939</td><td align="left" rowspan="1" colspan="1">Basic chitinase</td><td align="center" style="background-color:#c42d27" rowspan="1" colspan="1">3.73</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G54420.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H00328</td><td align="left" rowspan="1" colspan="1">Homolog of carrot EP3-3 chitinase</td><td align="center" style="background-color:#bc2f26" rowspan="1" colspan="1">3.57</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G12500.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L00937</td><td align="left" rowspan="1" colspan="1">Basic chitinase</td><td align="center" style="background-color:#bd3427" rowspan="1" colspan="1">3.47</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G12500.1</td><td align="left" rowspan="1" colspan="1">Eucgr.I01495</td><td align="left" rowspan="1" colspan="1">Basic chitinase</td><td align="center" style="background-color:#b14128" rowspan="1" colspan="1">3.11</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G54420.1</td><td align="left" rowspan="1" colspan="1">Eucgr.K02166</td><td align="left" rowspan="1" colspan="1">Homolog of carrot EP3-3 chitinase</td><td align="center" style="background-color:#9a4722" rowspan="1" colspan="1">2.53</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G54420.1</td><td align="left" rowspan="1" colspan="1">Eucgr.K02166</td><td align="left" rowspan="1" colspan="1">Homolog of carrot EP3-3 chitinase</td><td align="center" style="background-color:#8f4f25" rowspan="1" colspan="1">2.21</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G54420.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A00020</td><td align="left" rowspan="1" colspan="1">Homolog of carrot EP3-3 chitinase</td><td align="center" style="background-color:#73602b" rowspan="1" colspan="1">1.43</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G05850.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H00455</td><td align="left" rowspan="1" colspan="1">Chitinase family protein (TAIR 9)</td><td align="center" style="background-color:#2b984c" rowspan="1" colspan="1">−0.75</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G16920.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H04034</td><td align="left" rowspan="1" colspan="1">Chitinase-like protein 2</td><td align="center" style="background-color:#2b984c" rowspan="1" colspan="1">−1.33</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-4</italic>—Chitin-binding</td><td align="left" rowspan="1" colspan="1">AT3G04720.1</td><td align="left" rowspan="1" colspan="1">Eucgr.B02124</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related 4</td><td align="center" style="background-color:#b73426" rowspan="1" colspan="1">3.42</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G04720.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L03258</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related 4</td><td align="center" style="background-color:#b93b28" rowspan="1" colspan="1">3.32</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G04720.1</td><td align="left" rowspan="1" colspan="1">Eucgr.B02122</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related 4</td><td align="center" style="background-color:#ab3a24" rowspan="1" colspan="1">3.06</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-5</italic>—Thaumatin-like and osmotin</td><td align="left" rowspan="1" colspan="1">AT1G20030.2</td><td align="left" rowspan="1" colspan="1">Eucgr.E01382</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">5.42</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G20030.2</td><td align="left" rowspan="1" colspan="1">Eucgr.E01384</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">5.31</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G20030.2</td><td align="left" rowspan="1" colspan="1">Eucgr.E01389</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">5.23</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G20030.2</td><td align="left" rowspan="1" colspan="1">Eucgr.E01385</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">5.13</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H03863</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">5.09</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G20030.2</td><td align="left" rowspan="1" colspan="1">Eucgr.E01381</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">4.96</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H03865</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">4.93</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H03864</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">4.77</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L01962</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#ed1c24" rowspan="1" colspan="1">4.69</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.E00557</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#db1f26" rowspan="1" colspan="1">4.43</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.D01888</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#be3026" rowspan="1" colspan="1">3.57</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.1</td><td align="left" rowspan="1" colspan="1">Eucgr.D01892</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#b63625" rowspan="1" colspan="1">3.34</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.8</td><td align="left" rowspan="1" colspan="1">Eucgr.D01887</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#b43525" rowspan="1" colspan="1">3.31</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11650.9</td><td align="left" rowspan="1" colspan="1">Eucgr.E00560</td><td align="left" rowspan="1" colspan="1">Osmotin 34</td><td align="center" style="background-color:#a83d24" rowspan="1" colspan="1">2.97</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G38280.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A01474</td><td align="left" rowspan="1" colspan="1">PR5-like receptor kinase</td><td align="center" style="background-color:#656a32" rowspan="1" colspan="1">1.03</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G38280.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A01470</td><td align="left" rowspan="1" colspan="1">PR5-like receptor kinase</td><td align="center" style="background-color:#656a32" rowspan="1" colspan="1">0.96</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G38280.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A01478</td><td align="left" rowspan="1" colspan="1">PR5-like receptor kinase</td><td align="center" style="background-color:#656a32" rowspan="1" colspan="1">0.78</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT2G28790.1</td><td align="left" rowspan="1" colspan="1">Eucgr.J02061</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#1aa24a" rowspan="1" colspan="1">−1.18</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G38660.1</td><td align="left" rowspan="1" colspan="1">Eucgr.G01772</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#1aa24a" rowspan="1" colspan="1">−1.33</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G73620.1</td><td align="left" rowspan="1" colspan="1">Eucgr.B00944</td><td align="left" rowspan="1" colspan="1">Pathogenesis-related thaumatin superfam</td><td align="center" style="background-color:#1aa24a" rowspan="1" colspan="1">−1.36</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-8</italic>—Chitinase class III</td><td align="left" rowspan="1" colspan="1">AT5G24090.1</td><td align="left" rowspan="1" colspan="1">Eucgr.E00091</td><td align="left" rowspan="1" colspan="1">Chitinase A</td><td align="center" style="background-color:#954a23" rowspan="1" colspan="1">2.40</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G24090.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L03478</td><td align="left" rowspan="1" colspan="1">Chitinase A</td><td align="center" style="background-color:#765f2b" rowspan="1" colspan="1">1.52</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-9</italic>—Peroxidase</td><td align="left" rowspan="1" colspan="1">AT4G37530.1</td><td align="left" rowspan="1" colspan="1">Eucgr.J02352</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#c12d26" rowspan="1" colspan="1">3.65</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT4G11600.1</td><td align="left" rowspan="1" colspan="1">Eucgr.D01857</td><td align="left" rowspan="1" colspan="1">Glutathione peroxidase 6 (TAIR 9)</td><td align="center" style="background-color:#ab3a24" rowspan="1" colspan="1">3.08</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G71695.1</td><td align="left" rowspan="1" colspan="1">Eucgr.F04198</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#924c23" rowspan="1" colspan="1">2.34</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G05260.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A01385</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#805727" rowspan="1" colspan="1">1.83</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G71695.1</td><td align="left" rowspan="1" colspan="1">Eucgr.F04195</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#75602c" rowspan="1" colspan="1">1.46</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT1G71695.1</td><td align="left" rowspan="1" colspan="1">Eucgr.L02740</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#71632d" rowspan="1" colspan="1">1.39</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G40150.1</td><td align="left" rowspan="1" colspan="1">Eucgr.J02173</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#12a049" rowspan="1" colspan="1">−1.23</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G42180.1</td><td align="left" rowspan="1" colspan="1">Eucgr.F03724</td><td align="left" rowspan="1" colspan="1">Peroxidase superfamily protein</td><td align="center" style="background-color:#0cac4f" rowspan="1" colspan="1">−1.76</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"><bold>AT4G21960.1</bold></td><td align="left" rowspan="1" colspan="1"><bold>Eucgr.E04056</bold></td><td align="left" rowspan="1" colspan="1"><bold>Peroxidase superfamily protein</bold></td><td align="center" style="background-color:#0cac4f" rowspan="1" colspan="1"><bold>−1.85</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-10</italic>—Ribonuclease-like</td><td align="left" rowspan="1" colspan="1">AT1G80780.3</td><td align="left" rowspan="1" colspan="1">Eucgr.F03953</td><td align="left" rowspan="1" colspan="1">Polynucleotidyl transferase, ribonuclease</td><td align="center" style="background-color:#5d6f34" rowspan="1" colspan="1">0.83</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G22250.1</td><td align="left" rowspan="1" colspan="1">Eucgr.J00535</td><td align="left" rowspan="1" colspan="1">Polynucleotidyl transferase, ribonuclease</td><td align="center" style="background-color:#0cac4f" rowspan="1" colspan="1">−1.46</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-12</italic>—Defensins</td><td align="left" rowspan="1" colspan="1">AT4G11393.1</td><td align="left" rowspan="1" colspan="1">Eucgr.K03440</td><td align="left" rowspan="1" colspan="1">Defensin-like (DEFL) family protein</td><td align="center" style="background-color:#a14222" rowspan="1" colspan="1">2.72</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-14</italic>—Lipid transfer proteins</td><td align="left" rowspan="1" colspan="1">AT5G48485.1</td><td align="left" rowspan="1" colspan="1">Eucgr.H00727</td><td align="left" rowspan="1" colspan="1">Bifunctional inhibitor/lipid-transfer protein</td><td align="center" style="background-color:#219648" rowspan="1" colspan="1">−0.85</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G64080.1</td><td align="left" rowspan="1" colspan="1">Eucgr.I02679</td><td align="left" rowspan="1" colspan="1">Bifunctional inhibitor/lipid-transfer protein</td><td align="center" style="background-color:#1d9a49" rowspan="1" colspan="1">−0.95</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT3G18280.1</td><td align="left" rowspan="1" colspan="1">Eucgr.B00824</td><td align="left" rowspan="1" colspan="1">Bifunctional inhibitor/lipid-transfer protein</td><td align="center" style="background-color:#219648" rowspan="1" colspan="1">−1.00</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G59320.1</td><td align="left" rowspan="1" colspan="1">Eucgr.K01283</td><td align="left" rowspan="1" colspan="1">Lipid transfer protein 3</td><td align="center" style="background-color:#0ca14a" rowspan="1" colspan="1">−1.20</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G55460.1</td><td align="left" rowspan="1" colspan="1">Eucgr.F03514</td><td align="left" rowspan="1" colspan="1">Bifunctional inhibitor/lipid-transfer protein</td><td align="center" style="background-color:#0ca14a" rowspan="1" colspan="1">−1.31</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G59320.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A00746</td><td align="left" rowspan="1" colspan="1">Lipid transfer protein 4</td><td align="center" style="background-color:#03aa4d" rowspan="1" colspan="1">−1.60</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G05960.1</td><td align="left" rowspan="1" colspan="1">Eucgr.K03041</td><td align="left" rowspan="1" colspan="1">Bifunctional inhibitor/lipid-transfer protein</td><td align="center" style="background-color:#03aa4d" rowspan="1" colspan="1">−1.66</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">AT5G59320.1</td><td align="left" rowspan="1" colspan="1">Eucgr.K01282</td><td align="left" rowspan="1" colspan="1">Lipid transfer protein 5</td><td align="center" style="background-color:#03aa4d" rowspan="1" colspan="1">−1.76</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>PR-15</italic>—Oxalate oxidases (Germin)</td><td align="left" rowspan="1" colspan="1">AT3G62020.1</td><td align="left" rowspan="1" colspan="1">Eucgr.A00990</td><td align="left" rowspan="1" colspan="1">Germin-like protein 10</td><td align="center" style="background-color:#159f49" rowspan="1" colspan="1">−1.18</td></tr></tbody></table><table-wrap-foot><p><italic>Up and down regulated genes are indicated as a gradient from bright red to bright green</italic>.</p></table-wrap-foot></table-wrap><p>The <italic>E. nitens</italic> putative <italic>PR-9</italic> ortholog (Eucgr.E04056) was down regulated by a 1.85 fold-change on a log<sub>2</sub> scale in the <italic>P. cinnamomi</italic>-inoculated tissue (indicated in bold in Table <xref ref-type="table" rid="T4">4</xref>). The sequence of this ortholog was compared to peroxidase from <italic>Carica papaya</italic> (EL784270) and <italic>A. thaliana</italic>. The amino acid alignment is indicated in Figure <xref ref-type="fig" rid="F6">6</xref>. The <italic>E. nitens PR-9</italic> sequence shared 80% amino acid identity with the <italic>C. papaya PR-9</italic> sequence.</p><fig id="F6" position="float"><label>Figure 6</label><caption><p><bold>Amino acid alignment of the putative PR-9 peroxidase ortholog of <italic>Eucalyptus nitens</italic> (Phytozome: Eucgr.E04056) in comparison to the <italic>Arabidopsis thaliana</italic> (TAIR number AT4G21960) and <italic>Carica papaya</italic> (Genbank: <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="EL784270">EL784270</ext-link>) orthologs</bold>. Light gray highlights conservative amino acid substitutions and dark gray indicates non-conservative substitutions.</p></caption><graphic xlink:href="fpls-07-00191-g0006"></graphic></fig></sec></sec><sec sec-type="discussion" id="s4"><title>Discussion</title><p>The compatible interaction between <italic>E. nitens</italic> and <italic>P. cinnamomi</italic> provided a model system to study the compatible interaction between <italic>Eucalyptus</italic> spp. and <italic>Phytophthora</italic> spp. One year old <italic>E. nitens</italic> plants were stem inoculated using <italic>P. cinnamomi</italic> and pronounced lesions were obtained (Figure <xref ref-type="fig" rid="F1">1</xref>) suggesting that successful infection had occurred. This was corroborated with the presence of hyphae in the stems as early as 48 hpi in some instances and subsequently consistently observed at 5 dpi. In order to gain a better understanding of this compatible pathosystem, a dual RNA sequencing approach, as described previously for other plant-pathogen interactions (Hayden et al., <xref rid="B42" ref-type="bibr">2014</xref>), was undertaken to concurrently detect pathogenicity factors and host responses.</p><p>Analysis of transcripts mapping to the <italic>P. cinnamomi</italic> genome confirmed the presence of ~1% pathogen in the tissue profiled. We obtained 78% mapping of the <italic>E. nitens</italic> transcripts to the <italic>E. grandis</italic> genome which was similar to that obtained in a study by Ward and Weber (<xref rid="B93" ref-type="bibr">2012</xref>) where raspberry transcripts were mapped to the strawberry genome. This substantiates the use of cross-species resources in the event that no such genomic resources are available for the species of interest.</p><p>Table <xref ref-type="table" rid="T3">3</xref> indicates possible determinants expressed <italic>in planta</italic> which may contribute to the susceptible outcome of the interaction. A pathogen transcript encoding a CRN family protein was highly expressed <italic>in planta</italic>. In <italic>Phytophthora</italic> species, the CRNs are a complex family of large proteins and various experiments suggest that some CRNs are able to target host factors to suppress plant defenses (Adhikari et al., <xref rid="B2" ref-type="bibr">2013</xref>). The <italic>P. cinnamomi</italic> CRN is closely related to the CRN1 protein from <italic>P. infestans</italic>, suggesting that it may have the same role as described in <italic>P. infestans</italic>. Torto et al. (<xref rid="B87" ref-type="bibr">2003</xref>) showed that the <italic>P. infestans</italic> CRN1 and CRN2 effectors were expressed during infection of tomato and that CRN1 and CRN2 were able to cause necrosis in tobacco and CRN2 induced PR1a expression in tomato. While some CRN effectors are known to target host nuclei (Stam et al., <xref rid="B80" ref-type="bibr">2013a</xref>) the role in virulence may be diverse in various life stages of <italic>P. infestans</italic> (Resjö et al., <xref rid="B70" ref-type="bibr">2014</xref>). Liu et al. (<xref rid="B50" ref-type="bibr">2011</xref>) described two CRN effectors from <italic>P. sojae</italic> where one induced cell death and the other suppressed cell death in soybean. More recently, it was shown that the two effectors together, or one alone, can suppress host defenses by interacting with catalases and in so doing, modulate the HR and H<sub>2</sub>O<sub>2</sub> levels <italic>in planta</italic> (Zhang et al., <xref rid="B102" ref-type="bibr">2015</xref>). Another well characterized example of an apoplastic effector is that of the <italic>Cellulose Binding, Elicitor, and Lectin-like</italic> (<italic>CBEL</italic>) transcript, which elicits necrosis and defense gene expression in hosts and is necessary for attachment onto plant surfaces (Mateos et al., <xref rid="B55" ref-type="bibr">1997</xref>; Séjalon-Delmas et al., <xref rid="B77" ref-type="bibr">1997</xref>). Further examination of the virulence factors and the host targets they affect, will provide insight into the cause of the host responses observed in <italic>E. nitens</italic>.</p><p>The over-represented GO terms in <italic>E. nitens</italic> challenged with <italic>P. cinnamomi</italic> (Figures <xref ref-type="fig" rid="F4">4</xref>, <xref ref-type="fig" rid="F5">5</xref>) were indicative of a host actively attempting to combat infection, albeit at a late stage of a compatible interaction. We observed differential expression of various defense responses, but highlight two possible factors contributing to susceptibility.</p><p>Some physiological responses to <italic>P. cinnamomi</italic> include the down-regulation of photosynthesis-related terms and up-regulation of water stress terms. Various tree species inoculated with <italic>P. cinnamomi</italic> show declines in stomatal conductance and photosynthesis. In <italic>Eucalyptus sieberi</italic>, this decline is associated with susceptibility, since these factors decreased less severely in resistant <italic>Eucalyptus sideroxylon</italic> (Dempsey et al., <xref rid="B24" ref-type="bibr">2012</xref>). In <italic>Quercus suber</italic>, photosynthesis and stomatal conductance also decreased after inoculation (Medeira et al., <xref rid="B56" ref-type="bibr">2012</xref>). Manter et al. (<xref rid="B52" ref-type="bibr">2007</xref>) noted the prevalence of photosynthetic and stomatal conductance decreases in <italic>Phytophthora</italic>-host interactions. They showed that photosynthetic decline could be caused by elicitins in the absence of water stress. Maintaining adequate photosynthetic levels may assist tolerance or resistance, which is a possible explanation of why lower photosynthetic rates and stomatal conductance is associated with an increase in pathogen (Portz et al., <xref rid="B67" ref-type="bibr">2007</xref>) and lower tolerance to <italic>Phytophthora</italic> spp. (Reeksting et al., <xref rid="B69" ref-type="bibr">2014</xref>).</p><p>Distinct components of the phenylpropanoid pathway are present in both the up- and down-regulated datasets. There are several up-regulated genes with GO annotations associated with flavonoid biosynthesis. Susceptible <italic>Lupinus angustifolius</italic> up-regulated the flavonoid genistein in response to <italic>P. cinnamomi</italic> (Gunning et al., <xref rid="B40" ref-type="bibr">2013</xref>) however, certain <italic>Citrus</italic> flavonoids have an antimicrobial action against <italic>Phytophthora citrophthora</italic> (del Río et al., <xref rid="B23" ref-type="bibr">2004</xref>). In the down-regulated dataset, GO terms associated with lignin synthesis via the phenylpropanoid pathway are over-represented. For lignin synthesis, most genes encoding enzymes involved in biosynthesis of the coniferyl alcohol (G subunit) and sinapyl alcohol (S subunit) are down-regulated, although genes encoding enzymes catalyzing the synthesis of coumaryl alcohol (H subunit) are up-regulated (Table <xref ref-type="supplementary-material" rid="SM2">S2</xref>). Since synthesis of the S and G subunits is possibly suppressed, lignin biosynthesis could be down-regulated in <italic>E. nitens</italic>. Lignin is associated with strengthening of cell-walls and helps prevent penetration by a pathogen (Bechinger et al., <xref rid="B11" ref-type="bibr">1999</xref>), and down-regulation of monolignols can compromise host resistance (Naoumkina et al., <xref rid="B63" ref-type="bibr">2010</xref>). Lignin synthesis plays a role in raspberry responses to challenge with <italic>P. rubi</italic> (Ward and Weber, <xref rid="B93" ref-type="bibr">2012</xref>) and transgenic potato plants with limited phenylpropanoid substrates had increased susceptibility to <italic>P. infestans</italic> (Yao et al., <xref rid="B100" ref-type="bibr">1995</xref>).</p><p>Gene ontology terms pertaining to JA, SA, and ET pathways were over-represented in the up-regulated dataset in <italic>E. nitens</italic>, suggesting that they could play a role in defense signaling for this interaction. Other studies involving hosts inoculated with <italic>Phytophthora</italic> spp. have also shown mixed hormone responses (Attard et al., <xref rid="B9" ref-type="bibr">2010</xref>; Shibata et al., <xref rid="B79" ref-type="bibr">2010</xref>). JA may be needed for successful defense against <italic>P. cinnamomi</italic> in maize, a resistant monocot (Allardyce et al., <xref rid="B8" ref-type="bibr">2013</xref>). Terms related to GA and auxin were over-represented in the down-regulated dataset. Treatment of soybean with GA increased susceptibility to <italic>P. sojae</italic> (Sugano et al., <xref rid="B83" ref-type="bibr">2013</xref>) and it has been proposed that GA influences defense against necrotrophic fungi by repressing resistance (Mengiste, <xref rid="B57" ref-type="bibr">2012</xref>). The role of auxin in defense against <italic>P. cinnamomi</italic> has recently been described (Eshraghi et al., <xref rid="B29" ref-type="bibr">2014b</xref>), where <italic>Arabidopsis</italic> auxin sensitivity and transport mutants were shown to be highly susceptible to the pathogen. Treatment of <italic>L. angustifolius</italic> with an inhibitor of auxin transport increased susceptibility to <italic>P. cinnamomi</italic>.</p><p>Since <italic>PR</italic> genes are markers of defense hormone signaling, the different putative <italic>PR</italic> genes expressed reflect the mix of JA and SA signaling noted in the over-representation analysis.</p><p>Gene models identified as <italic>PR</italic> genes in this dataset are putative orthologs of <italic>A. thaliana PR</italic> genes. For many of these genes, there are multiple differentially expressed <italic>E. grandis</italic> gene models matching to one <italic>A. thaliana</italic> putative ortholog and an expansion of several <italic>PR</italic> genes in <italic>E. grandis</italic> has been noted (Naidoo et al., <xref rid="B62" ref-type="bibr">2014</xref>). Expression of these multiple <italic>PR</italic> gene transcripts in <italic>E. nitens</italic> could indicate that some of the orthologs have slightly different functions and are all used during a defense response.</p><p>Transcription of <italic>PR-1</italic>, chitinase (<italic>PR-3</italic>), chitin-binding protein (<italic>PR-4</italic>), and thaumatin-like protein/osmotin (<italic>PR-5</italic>) putative orthologs appears to be highly up-regulated in <italic>E. nitens</italic> (Table <xref ref-type="table" rid="T4">4</xref>). A <italic>Phytophthora</italic>-resistant potato expresses <italic>PR-1</italic> constitutively (Ali et al., <xref rid="B7" ref-type="bibr">2012</xref>) and constitutive expression of <italic>PR-1</italic> in transgenic tobacco confers resistance to <italic>P. parasitica</italic> (Alexander et al., <xref rid="B5" ref-type="bibr">1993</xref>). Transgenic plants over-expressing <italic>PR-5</italic> genes have been shown to increase resistance to <italic>P. citrophthora</italic> and <italic>P. infestans</italic> (Fagoaga et al., <xref rid="B30" ref-type="bibr">2001</xref>; Pushin et al., <xref rid="B68" ref-type="bibr">2010</xref>; Acharya et al., <xref rid="B1" ref-type="bibr">2013</xref>).</p><p>Peroxidases (PR-9) are potential cross-species <italic>Phytophthora</italic> effector targets, since a certain <italic>C. papaya</italic> peroxidase (EL784270) and its putative orthologs have been suppressed in different hosts upon inoculation with <italic>P. sojae, P. palmivora</italic>, and <italic>P. infestans</italic> (Moy et al., <xref rid="B59" ref-type="bibr">2004</xref>; Restrepo et al., <xref rid="B71" ref-type="bibr">2005</xref>; Porter et al., <xref rid="B66" ref-type="bibr">2009</xref>). An <italic>E. grandis</italic> gene, Eucgr.E04056, is highly similar to the <italic>C. papaya</italic> ortholog, and is also strongly suppressed in the current interaction. Putative <italic>PR-14</italic> and <italic>PR-15</italic> orthologs were down-regulated in <italic>E. nitens</italic> and while these orthologs would have to be characterized further, it is tempting to speculate that their suppression may be driving susceptibility. For example, enhanced resistance to <italic>P. nicotianae</italic> was conferred by a pepper lipid transfer protein over-expressed in tobacco (Sarowar et al., <xref rid="B73" ref-type="bibr">2009</xref>) and <italic>PR-15</italic> may encode for a germin-like oxalate oxidase known to produce hydrogen peroxide that is toxic to pathogens (van Loon et al., <xref rid="B91" ref-type="bibr">2006</xref>; Ferreira et al., <xref rid="B33" ref-type="bibr">2007</xref>).</p></sec><sec sec-type="conclusions" id="s5"><title>Conclusion</title><p>The outcomes of this dual RNA-seq study provided valuable insights into <italic>P. cinnamomi</italic> pathogenicity and virulence factors and <italic>E. nitens</italic> defense mechanisms utilized against <italic>P. cinnamomi</italic>. Several factors may contribute to the compatibility however, we have used further sequence and functional genetics support to motivate that the <italic>P. cinnamomi CRN</italic> and the <italic>E. nitens PR-9</italic> genes are important contributors to the susceptible outcome. Future work involving comparison with a resistant interaction over a time-course is required to provide an indication of host targets manipulated by <italic>P. cinnamomi</italic> and to enhance understanding of the defense pathways required for resistance.</p></sec><sec id="s6"><title>Author contributions</title><p>FM, LS, SiN, and TM performed the experimental work, conducted and interpreted data analyses. SaN conceived the study, obtained funding to support the research. AM provided input into the experimental design and technical aspects of RNA-sequencing and assisted with critical evaluation of the manuscript. FM, LS, and SaN wrote the manuscript with input from DB and NV, who supervised aspects of this research.</p><sec><title>Conflict of interest statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></sec></body><back><ack><p>The authors thank Charles Hefer for creating the TopHat and FastQGroomer pipeline on Galaxy, Melissa Reynolds, and Christy Marais for conducting the relatedness analysis of the plant material, and Eshchar Mizrachi, Burger van Jaarsveld, and Karen van der Merwe for bioinformatics support. This work is based on the research supported in part by the National Research Foundation of South Africa for the grant no. 76225 and 86936; the Forest Molecular Genetics Program by Mondi and Sappi, the Technology and Human Resources for Industry Program (80118), and Department of Science and Technology, The Eucalyptus Genomics Platform: Tree genomics and biotechnology for wood fibre, bioenergy and biomaterials. Any opinion, finding and conclusion or recommendation expressed in this material is that of the author(s) and the NRF does not accept any liability in this regard.</p></ack><sec sec-type="supplementary-material" id="s7"><title>Supplementary material</title><p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="http://journal.frontiersin.org/article/10.3389/fpls.2016.00191">http://journal.frontiersin.org/article/10.3389/fpls.2016.00191</ext-link></p><supplementary-material content-type="local-data" id="SM1"><media xlink:href="Table1.XLSX"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM2"><media xlink:href="Table2.XLSX"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Acharya</surname><given-names>K.</given-names></name><name><surname>Pal</surname><given-names>A. 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