Transcriptome analysis of contrasting resistance to herbivory by Empoasca fabae in two shrub willow species and their hybrid progeny
Identifieur interne : 000005 ( Pmc/Checkpoint ); précédent : 000004; suivant : 000006Transcriptome analysis of contrasting resistance to herbivory by Empoasca fabae in two shrub willow species and their hybrid progeny
Auteurs : Wanyan Wang [États-Unis] ; Craig H. Carlson [États-Unis] ; Lawrence B. Smart [États-Unis] ; John E. Carlson [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2020.
Abstract
Short rotation woody biomass cultivars developed from fast-growing shrub species of willow (
Url:
DOI: 10.1371/journal.pone.0236586
PubMed: 32726362
PubMed Central: 7390382
Affiliations:
- États-Unis
- Pennsylvanie, État de New York
- Ithaca (New York), University Park (Pennsylvanie)
- Université Cornell, Université d'État de Pennsylvanie
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Transcriptome analysis of contrasting resistance to herbivory by <italic>Empoasca fabae</italic> in two shrub willow species and their hybrid progeny</title><author><name sortKey="Wang, Wanyan" sort="Wang, Wanyan" uniqKey="Wang W" first="Wanyan" last="Wang">Wanyan Wang</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">University Park (Pennsylvanie)</settlement></placeName><orgName type="university">Université d'État de Pennsylvanie</orgName></affiliation></author><author><name sortKey="Carlson, Craig H" sort="Carlson, Craig H" uniqKey="Carlson C" first="Craig H." last="Carlson">Craig H. Carlson</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York</wicri:regionArea><placeName><region type="state">État de New York</region><settlement type="city">Ithaca (New York)</settlement></placeName><orgName type="university">Université Cornell</orgName></affiliation></author><author><name sortKey="Smart, Lawrence B" sort="Smart, Lawrence B" uniqKey="Smart L" first="Lawrence B." last="Smart">Lawrence B. Smart</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York</wicri:regionArea><placeName><region type="state">État de New York</region><settlement type="city">Ithaca (New York)</settlement></placeName><orgName type="university">Université Cornell</orgName></affiliation></author><author><name sortKey="Carlson, John E" sort="Carlson, John E" uniqKey="Carlson J" first="John E." last="Carlson">John E. Carlson</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">University Park (Pennsylvanie)</settlement></placeName><orgName type="university">Université d'État de Pennsylvanie</orgName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32726362</idno><idno type="pmc">7390382</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7390382</idno><idno type="RBID">PMC:7390382</idno><idno type="doi">10.1371/journal.pone.0236586</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000A32</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000A32</idno><idno type="wicri:Area/Pmc/Curation">000A32</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000A32</idno><idno type="wicri:Area/Pmc/Checkpoint">000005</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000005</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Transcriptome analysis of contrasting resistance to herbivory by <italic>Empoasca fabae</italic> in two shrub willow species and their hybrid progeny</title><author><name sortKey="Wang, Wanyan" sort="Wang, Wanyan" uniqKey="Wang W" first="Wanyan" last="Wang">Wanyan Wang</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">University Park (Pennsylvanie)</settlement></placeName><orgName type="university">Université d'État de Pennsylvanie</orgName></affiliation></author><author><name sortKey="Carlson, Craig H" sort="Carlson, Craig H" uniqKey="Carlson C" first="Craig H." last="Carlson">Craig H. Carlson</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York</wicri:regionArea><placeName><region type="state">État de New York</region><settlement type="city">Ithaca (New York)</settlement></placeName><orgName type="university">Université Cornell</orgName></affiliation></author><author><name sortKey="Smart, Lawrence B" sort="Smart, Lawrence B" uniqKey="Smart L" first="Lawrence B." last="Smart">Lawrence B. Smart</name><affiliation wicri:level="4"><nlm:aff id="aff002"><addr-line>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York</wicri:regionArea><placeName><region type="state">État de New York</region><settlement type="city">Ithaca (New York)</settlement></placeName><orgName type="university">Université Cornell</orgName></affiliation></author><author><name sortKey="Carlson, John E" sort="Carlson, John E" uniqKey="Carlson J" first="John E." last="Carlson">John E. Carlson</name><affiliation wicri:level="4"><nlm:aff id="aff001"><addr-line>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">University Park (Pennsylvanie)</settlement></placeName><orgName type="university">Université d'État de Pennsylvanie</orgName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Short rotation woody biomass cultivars developed from fast-growing shrub species of willow (<italic>Salix</italic> spp.) have superior properties as perennial energy crops for the Northeast and Midwest US. However, the insect pest potato leafhopper (PLH) <italic>Empoasca fabae</italic> (Harris) can cause serious damage and reduce yield of susceptible genotypes. Currently, the willow cultivars in use display varying levels of susceptibility under PLH infestation. However, genes and markers for resistance to PLH are not yet available for marker-assisted selection in breeding. In this study, transcriptome differences between a resistant genotype 94006 (<italic>S</italic>. <italic>purpurea</italic>) and a susceptible cultivar ‘Jorr’ (<italic>S</italic>. <italic>viminalis</italic>), and their hybrid progeny were determined. Over 600 million RNA-Seq reads were generated and mapped to the <italic>Salix purpurea</italic> reference transcriptome. Gene expression analyses revealed the unique defense mechanism in resistant genotype 94006 that involves PLH-induced secondary cell wall modification. In the susceptible genotypes, genes involved in programed cell death were highly expressed, explaining the necrosis symptoms after PLH feeding. Overall, the discovery of resistance genes and defense mechanisms provides new resources for shrub willow breeding and research in the future.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Volk, Ta" uniqKey="Volk T">TA Volk</name></author><author><name sortKey="Heavey, Jp" uniqKey="Heavey J">JP Heavey</name></author><author><name sortKey="Eisenbies, Mh" uniqKey="Eisenbies M">MH Eisenbies</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stoof, Cr" uniqKey="Stoof C">CR Stoof</name></author><author><name sortKey="Richards, Bk" uniqKey="Richards B">BK Richards</name></author><author><name sortKey="Woodbury, Pb" uniqKey="Woodbury P">PB Woodbury</name></author><author><name sortKey="Fabio, Es" uniqKey="Fabio E">ES Fabio</name></author><author><name sortKey="Brumbach, Ar" uniqKey="Brumbach A">AR Brumbach</name></author><author><name sortKey="Cherney, J" uniqKey="Cherney J">J 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32726362</article-id><article-id pub-id-type="pmc">7390382</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0236586</article-id><article-id pub-id-type="publisher-id">PONE-D-20-05903</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Gene Expression</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Physical Sciences</subject><subj-group><subject>Chemistry</subject><subj-group><subject>Electrochemistry</subject><subj-group><subject>Electrochemical Cells</subject><subj-group><subject>Secondary Cells</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Plant Science</subject><subj-group><subject>Plant Anatomy</subject><subj-group><subject>Leaves</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Biosynthesis</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Computational Biology</subject><subj-group><subject>Genome Analysis</subject><subj-group><subject>Transcriptome Analysis</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Genomics</subject><subj-group><subject>Genome Analysis</subject><subj-group><subject>Transcriptome Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Eukaryota</subject><subj-group><subject>Plants</subject><subj-group><subject>Shrubs</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Plant Physiology</subject><subj-group><subject>Plant Defenses</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Plant Science</subject><subj-group><subject>Plant Physiology</subject><subj-group><subject>Plant Defenses</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Molecular biology</subject><subj-group><subject>Molecular biology techniques</subject><subj-group><subject>Sequencing techniques</subject><subj-group><subject>RNA sequencing</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and analysis methods</subject><subj-group><subject>Molecular biology techniques</subject><subj-group><subject>Sequencing techniques</subject><subj-group><subject>RNA sequencing</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Transcriptome analysis of contrasting resistance to herbivory by <italic>Empoasca fabae</italic> in two shrub willow species and their hybrid progeny</article-title><alt-title alt-title-type="running-head">Transcriptome analysis of insect resistance in shrub willow</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-0332-2702</contrib-id><name><surname>Wang</surname><given-names>Wanyan</given-names></name><role content-type="https://casrai.org/credit/">Formal analysis</role><role content-type="https://casrai.org/credit/">Investigation</role><role content-type="https://casrai.org/credit/">Methodology</role><role content-type="https://casrai.org/credit/">Writing – original draft</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Carlson</surname><given-names>Craig H.</given-names></name><role content-type="https://casrai.org/credit/">Formal analysis</role><role content-type="https://casrai.org/credit/">Investigation</role><role content-type="https://casrai.org/credit/">Methodology</role><role content-type="https://casrai.org/credit/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-7812-7736</contrib-id><name><surname>Smart</surname><given-names>Lawrence B.</given-names></name><role content-type="https://casrai.org/credit/">Conceptualization</role><role content-type="https://casrai.org/credit/">Funding acquisition</role><role content-type="https://casrai.org/credit/">Methodology</role><role content-type="https://casrai.org/credit/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-9129-1867</contrib-id><name><surname>Carlson</surname><given-names>John E.</given-names></name><role content-type="https://casrai.org/credit/">Conceptualization</role><role content-type="https://casrai.org/credit/">Data curation</role><role content-type="https://casrai.org/credit/">Funding acquisition</role><role content-type="https://casrai.org/credit/">Project administration</role><role content-type="https://casrai.org/credit/">Resources</role><role content-type="https://casrai.org/credit/">Supervision</role><role content-type="https://casrai.org/credit/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Horticulture Section, School of Integrative Plant Science, Cornell University, Cornell AgriTech, Geneva, New York, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Heinze</surname><given-names>Berthold</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Austrian Federal Research Centre for Forests BFW, AUSTRIA</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><corresp id="cor001">* E-mail: <email>jec16@psu.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>29</day><month>7</month><year>2020</year></pub-date><pub-date pub-type="collection"><year>2020</year></pub-date><volume>15</volume><issue>7</issue><elocation-id>e0236586</elocation-id><history><date date-type="received"><day>29</day><month>2</month><year>2020</year></date><date date-type="accepted"><day>8</day><month>7</month><year>2020</year></date></history><permissions><copyright-statement>© 2020 Wang et al</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Wang et al</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 <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0236586.pdf"></self-uri><abstract><p>Short rotation woody biomass cultivars developed from fast-growing shrub species of willow (<italic>Salix</italic> spp.) have superior properties as perennial energy crops for the Northeast and Midwest US. However, the insect pest potato leafhopper (PLH) <italic>Empoasca fabae</italic> (Harris) can cause serious damage and reduce yield of susceptible genotypes. Currently, the willow cultivars in use display varying levels of susceptibility under PLH infestation. However, genes and markers for resistance to PLH are not yet available for marker-assisted selection in breeding. In this study, transcriptome differences between a resistant genotype 94006 (<italic>S</italic>. <italic>purpurea</italic>) and a susceptible cultivar ‘Jorr’ (<italic>S</italic>. <italic>viminalis</italic>), and their hybrid progeny were determined. Over 600 million RNA-Seq reads were generated and mapped to the <italic>Salix purpurea</italic> reference transcriptome. Gene expression analyses revealed the unique defense mechanism in resistant genotype 94006 that involves PLH-induced secondary cell wall modification. In the susceptible genotypes, genes involved in programed cell death were highly expressed, explaining the necrosis symptoms after PLH feeding. Overall, the discovery of resistance genes and defense mechanisms provides new resources for shrub willow breeding and research in the future.</p></abstract><funding-group><award-group id="award001"><funding-source><institution>USDA National Institute of Food and Agriculture</institution></funding-source><award-id>2012- 68005-19703</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-9129-1867</contrib-id><name><surname>Carlson</surname><given-names>John E.</given-names></name></principal-award-recipient></award-group><funding-statement>Primary support for this research was provided to LBS and JEC as grant No. 2012-68005-19703 from the USDA Agriculture and Food Research Initiative of the National Institute of Food and Agriculture (<ext-link ext-link-type="uri" xlink:href="https://nifa.usda.gov/grants">https://nifa.usda.gov/grants</ext-link>). Additional support was provided to JEC from through the USDA National Institute of Food and Agriculture Federal Appropriations (<ext-link ext-link-type="uri" xlink:href="https://nifa.usda.gov/nifas-discretionary-and-mandatoryfunding">https://nifa.usda.gov/nifas-discretionary-and-mandatoryfunding</ext-link>) under Project PEN04532 and Accession number 1000326. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="7"></fig-count><table-count count="2"></table-count><page-count count="25"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>Data produced consist of 96 RNA sequence files. All data files have been submitted to the Short Reads Arcvive (SRA) at NCBI (National Center for Biotechnology Information), under BioProject ID PRJNA601117 (<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA601117">https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA601117</ext-link>). The SRA accession numbers for the data files are GSM4263764 - GSM4263859, inclusive.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>Data produced consist of 96 RNA sequence files. All data files have been submitted to the Short Reads Arcvive (SRA) at NCBI (National Center for Biotechnology Information), under BioProject ID PRJNA601117 (<ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA601117">https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA601117</ext-link>). The SRA accession numbers for the data files are GSM4263764 - GSM4263859, inclusive.</p></notes></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Pennsylvanie</li><li>État de New York</li></region><settlement><li>Ithaca (New York)</li><li>University Park (Pennsylvanie)</li></settlement><orgName><li>Université Cornell</li><li>Université d'État de Pennsylvanie</li></orgName></list><tree><country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Wang, Wanyan" sort="Wang, Wanyan" uniqKey="Wang W" first="Wanyan" last="Wang">Wanyan Wang</name></region><name sortKey="Carlson, Craig H" sort="Carlson, Craig H" uniqKey="Carlson C" first="Craig H." last="Carlson">Craig H. Carlson</name><name sortKey="Carlson, John E" sort="Carlson, John E" uniqKey="Carlson J" first="John E." last="Carlson">John E. Carlson</name><name sortKey="Smart, Lawrence B" sort="Smart, Lawrence B" uniqKey="Smart L" first="Lawrence B." last="Smart">Lawrence B. Smart</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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