Depicting the battle between nectarine and Monilinia laxa: the fruit developmental stage dictates the effectiveness of the host defenses and the pathogen's infection strategies.
Identifieur interne : 000187 ( Main/Exploration ); précédent : 000186; suivant : 000188Depicting the battle between nectarine and Monilinia laxa: the fruit developmental stage dictates the effectiveness of the host defenses and the pathogen's infection strategies.
Auteurs : Marta Balsells-Llaurad ; Christian J. Silva [États-Unis] ; Josep Usall ; Núria Vall-Llaura ; Sandra Serrano-Prieto ; Neus Teixid ; Saskia D. Mesquida-Pesci [États-Unis] ; Antonieta De Cal ; Barbara Blanco-Ulate [États-Unis] ; Rosario TorresSource :
- Horticulture research [ 2052-7276 ] ; 2020.
Abstract
Infections by the fungus Monilinia laxa, the main cause of brown rot in Europe, result in considerable losses of stone fruit. Herein, we present a comprehensive transcriptomic approach to unravel strategies deployed by nectarine fruit and M. laxa during their interaction. We used M. laxa-inoculated immature and mature fruit, which was resistant and susceptible to brown rot, respectively, to perform a dual RNA-Seq analysis. In immature fruit, host responses, pathogen biomass, and pathogen transcriptional activity peaked at 14-24 h post inoculation (hpi), at which point M. laxa appeared to switch its transcriptional response to either quiescence or death. Mature fruit experienced an exponential increase in host and pathogen activity beginning at 6 hpi. Functional analyses in both host and pathogen highlighted differences in stage-dependent strategies. For example, in immature fruit, M. laxa unsuccessfully employed carbohydrate-active enzymes (CAZymes) for penetration, which the fruit was able to combat with tightly regulated hormone responses and an oxidative burst that challenged the pathogen's survival at later time points. In contrast, in mature fruit, M. laxa was more dependent on proteolytic effectors than CAZymes, and was able to invest in filamentous growth early during the interaction. Hormone analyses of mature fruit infected with M. laxa indicated that, while jasmonic acid activity was likely useful for defense, high ethylene activity may have promoted susceptibility through the induction of ripening processes. Lastly, we identified M. laxa genes that were highly induced in both quiescent and active infections and may serve as targets for control of brown rot.
DOI: 10.1038/s41438-020-00387-w
PubMed: 33082973
PubMed Central: PMC7527454
Affiliations:
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Silva</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Sciences, University of California, Davis, Davis, CA 95616 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Plant Sciences, University of California, Davis, Davis</wicri:cityArea></affiliation></author><author><name sortKey="Usall, Josep" sort="Usall, Josep" uniqKey="Usall J" first="Josep" last="Usall">Josep Usall</name><affiliation><nlm:affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</nlm:affiliation><wicri:noCountry code="subField">Catalonia Spain</wicri:noCountry></affiliation></author><author><name sortKey="Vall Llaura, Nuria" sort="Vall Llaura, Nuria" uniqKey="Vall Llaura N" first="Núria" last="Vall-Llaura">Núria Vall-Llaura</name><affiliation><nlm:affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</nlm:affiliation><wicri:noCountry code="subField">Catalonia Spain</wicri:noCountry></affiliation></author><author><name sortKey="Serrano Prieto, Sandra" sort="Serrano Prieto, Sandra" uniqKey="Serrano Prieto S" first="Sandra" last="Serrano-Prieto">Sandra Serrano-Prieto</name><affiliation><nlm:affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</nlm:affiliation><wicri:noCountry code="subField">Catalonia Spain</wicri:noCountry></affiliation></author><author><name sortKey="Teixid, Neus" sort="Teixid, Neus" uniqKey="Teixid N" first="Neus" last="Teixid">Neus Teixid</name><affiliation><nlm:affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</nlm:affiliation><wicri:noCountry code="subField">Catalonia Spain</wicri:noCountry></affiliation></author><author><name sortKey="Mesquida Pesci, Saskia D" sort="Mesquida Pesci, Saskia D" uniqKey="Mesquida Pesci S" first="Saskia D" last="Mesquida-Pesci">Saskia D. Mesquida-Pesci</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Sciences, University of California, Davis, Davis, CA 95616 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Plant Sciences, University of California, Davis, Davis</wicri:cityArea></affiliation></author><author><name sortKey="De Cal, Antonieta" sort="De Cal, Antonieta" uniqKey="De Cal A" first="Antonieta" last="De Cal">Antonieta De Cal</name><affiliation><nlm:affiliation>Department of Plant Protection, INIA, Ctra. de La Coruña Km. 7, 28040 Madrid, Community of Madrid Spain.</nlm:affiliation><wicri:noCountry code="subField">Community of Madrid Spain</wicri:noCountry></affiliation></author><author><name sortKey="Blanco Ulate, Barbara" sort="Blanco Ulate, Barbara" uniqKey="Blanco Ulate B" first="Barbara" last="Blanco-Ulate">Barbara Blanco-Ulate</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Sciences, University of California, Davis, Davis, CA 95616 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Plant Sciences, University of California, Davis, Davis</wicri:cityArea></affiliation></author><author><name sortKey="Torres, Rosario" sort="Torres, Rosario" uniqKey="Torres R" first="Rosario" last="Torres">Rosario Torres</name><affiliation><nlm:affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</nlm:affiliation><wicri:noCountry code="subField">Catalonia Spain</wicri:noCountry></affiliation></author></analytic><series><title level="j">Horticulture research</title><idno type="ISSN">2052-7276</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Infections by the fungus <i>Monilinia laxa</i>, the main cause of brown rot in Europe, result in considerable losses of stone fruit. Herein, we present a comprehensive transcriptomic approach to unravel strategies deployed by nectarine fruit and <i>M. laxa</i> during their interaction. We used <i>M. laxa</i>-inoculated immature and mature fruit, which was resistant and susceptible to brown rot, respectively, to perform a dual RNA-Seq analysis. In immature fruit, host responses, pathogen biomass, and pathogen transcriptional activity peaked at 14-24 h post inoculation (hpi), at which point <i>M. laxa</i> appeared to switch its transcriptional response to either quiescence or death. Mature fruit experienced an exponential increase in host and pathogen activity beginning at 6 hpi. Functional analyses in both host and pathogen highlighted differences in stage-dependent strategies. For example, in immature fruit, <i>M. laxa</i> unsuccessfully employed carbohydrate-active enzymes (CAZymes) for penetration, which the fruit was able to combat with tightly regulated hormone responses and an oxidative burst that challenged the pathogen's survival at later time points. In contrast, in mature fruit, <i>M. laxa</i> was more dependent on proteolytic effectors than CAZymes, and was able to invest in filamentous growth early during the interaction. Hormone analyses of mature fruit infected with <i>M. laxa</i> indicated that, while jasmonic acid activity was likely useful for defense, high ethylene activity may have promoted susceptibility through the induction of ripening processes. Lastly, we identified <i>M. laxa</i> genes that were highly induced in both quiescent and active infections and may serve as targets for control of brown rot.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">33082973</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>22</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2052-7276</ISSN><JournalIssue CitedMedium="Print"><Volume>7</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Horticulture research</Title><ISOAbbreviation>Hortic Res</ISOAbbreviation></Journal><ArticleTitle>Depicting the battle between nectarine and <i>Monilinia laxa</i>: the fruit developmental stage dictates the effectiveness of the host defenses and the pathogen's infection strategies.</ArticleTitle><Pagination><MedlinePgn>167</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41438-020-00387-w</ELocationID><Abstract><AbstractText>Infections by the fungus <i>Monilinia laxa</i>, the main cause of brown rot in Europe, result in considerable losses of stone fruit. Herein, we present a comprehensive transcriptomic approach to unravel strategies deployed by nectarine fruit and <i>M. laxa</i> during their interaction. We used <i>M. laxa</i>-inoculated immature and mature fruit, which was resistant and susceptible to brown rot, respectively, to perform a dual RNA-Seq analysis. In immature fruit, host responses, pathogen biomass, and pathogen transcriptional activity peaked at 14-24 h post inoculation (hpi), at which point <i>M. laxa</i> appeared to switch its transcriptional response to either quiescence or death. Mature fruit experienced an exponential increase in host and pathogen activity beginning at 6 hpi. Functional analyses in both host and pathogen highlighted differences in stage-dependent strategies. For example, in immature fruit, <i>M. laxa</i> unsuccessfully employed carbohydrate-active enzymes (CAZymes) for penetration, which the fruit was able to combat with tightly regulated hormone responses and an oxidative burst that challenged the pathogen's survival at later time points. In contrast, in mature fruit, <i>M. laxa</i> was more dependent on proteolytic effectors than CAZymes, and was able to invest in filamentous growth early during the interaction. Hormone analyses of mature fruit infected with <i>M. laxa</i> indicated that, while jasmonic acid activity was likely useful for defense, high ethylene activity may have promoted susceptibility through the induction of ripening processes. Lastly, we identified <i>M. laxa</i> genes that were highly induced in both quiescent and active infections and may serve as targets for control of brown rot.</AbstractText><CopyrightInformation>© The Author(s) 2020.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Balsells-Llauradó</LastName><ForeName>Marta</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</Affiliation><Identifier Source="GRID">grid.8581.4</Identifier><Identifier Source="ISNI">0000 0001 1943 6646</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Silva</LastName><ForeName>Christian J</ForeName><Initials>CJ</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of California, Davis, Davis, CA 95616 USA.</Affiliation><Identifier Source="GRID">grid.27860.3b</Identifier><Identifier Source="ISNI">0000 0004 1936 9684</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Usall</LastName><ForeName>Josep</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</Affiliation><Identifier Source="GRID">grid.8581.4</Identifier><Identifier Source="ISNI">0000 0001 1943 6646</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vall-Llaura</LastName><ForeName>Núria</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</Affiliation><Identifier Source="GRID">grid.8581.4</Identifier><Identifier Source="ISNI">0000 0001 1943 6646</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Serrano-Prieto</LastName><ForeName>Sandra</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</Affiliation><Identifier Source="GRID">grid.8581.4</Identifier><Identifier Source="ISNI">0000 0001 1943 6646</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Teixidó</LastName><ForeName>Neus</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</Affiliation><Identifier Source="GRID">grid.8581.4</Identifier><Identifier Source="ISNI">0000 0001 1943 6646</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mesquida-Pesci</LastName><ForeName>Saskia D</ForeName><Initials>SD</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of California, Davis, Davis, CA 95616 USA.</Affiliation><Identifier Source="GRID">grid.27860.3b</Identifier><Identifier Source="ISNI">0000 0004 1936 9684</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>de Cal</LastName><ForeName>Antonieta</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Plant Protection, INIA, Ctra. de La Coruña Km. 7, 28040 Madrid, Community of Madrid Spain.</Affiliation><Identifier Source="GRID">grid.419190.4</Identifier><Identifier Source="ISNI">0000 0001 2300 669X</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Blanco-Ulate</LastName><ForeName>Barbara</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of California, Davis, Davis, CA 95616 USA.</Affiliation><Identifier Source="GRID">grid.27860.3b</Identifier><Identifier Source="ISNI">0000 0004 1936 9684</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Torres</LastName><ForeName>Rosario</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>IRTA, XaRTA-Postharvest, Edifici Fruitcentre, Parc Científic i Tecnològic Agroalimentari de Lleida, 25003 Lleida, Catalonia Spain.</Affiliation><Identifier Source="GRID">grid.8581.4</Identifier><Identifier Source="ISNI">0000 0001 1943 6646</Identifier></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>01</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Hortic Res</MedlineTA><NlmUniqueID>101655540</NlmUniqueID><ISSNLinking>2052-7276</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Biotic</Keyword><Keyword MajorTopicYN="N">Fungal genetics</Keyword><Keyword 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J" last="Silva">Christian J. 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