Bacillus subtilis PTA-271 Counteracts Botryosphaeria Dieback in Grapevine, Triggering Immune Responses and Detoxification of Fungal Phytotoxins.
Identifieur interne : 000211 ( Main/Exploration ); précédent : 000210; suivant : 000212Bacillus subtilis PTA-271 Counteracts Botryosphaeria Dieback in Grapevine, Triggering Immune Responses and Detoxification of Fungal Phytotoxins.
Auteurs : Patricia Trotel-Aziz [France] ; Eliane Abou-Mansour [Suisse] ; Barbara Courteaux [France] ; Fanja Rabenoelina [France] ; Christophe Clément [France] ; Florence Fontaine [France] ; Aziz Aziz [France]Source :
- Frontiers in plant science [ 1664-462X ] ; 2019.
Abstract
Plant pathogens have evolved various strategies to enter hosts and cause diseases. Particularly Neofusicoccum parvum, a member of Botryosphaeria dieback consortium, can secrete the phytotoxins (-)-terremutin and (R)-mellein during grapevine colonization. The contribution of phytotoxins to Botryosphaeria dieback symptoms still remains unknown. Moreover, there are currently no efficient control strategies of this disease, and agro-environmental concerns have raised increasing interest in biocontrol strategies to limit disease spread in vineyards, especially by using some promising beneficial bacteria. Here, we first examined in planta the biocontrol capacity of Bacillus subtilis PTA-271 against N. parvum Np-Bt67 strain producing both (-)-terremutin and (R)-mellein. We then focused on the direct effects of PTA-271 on pathogen growth and the fate of pure phytotoxins, and explored the capacity of PTA-271 to induce or prime grapevine immunity upon pathogen infection or phytotoxin exposure. Results provided evidence that PTA-271 significantly protects grapevine cuttings against N. parvum and significantly primes the expression of PR2 (encoding a β-1,3-glucanase) and NCED2 (9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis) genes upon pathogen challenge. Using in vitro plantlets, we also showed that PTA-271 triggers the expression of salicylic acid- and jasmonic acid-responsive genes, including GST1 (encoding a glutathione-S-transferase) involved in detoxification process. However, in PTA-271-pretreated plantlets, exogenous (-)-terremutin strongly lowered the expression of most of upregulated genes, except GST1. Data also indicated that PTA-271 can detoxify both (-)-terremutin and (R)-mellein and antagonize N. parvum under in vitro conditions. Our findings highlight (-)-terremutin and (R)-mellein as key aggressive molecules produced by N. parvum that may weaken grapevine immunity to promote Botryosphaeria dieback symptoms. However, PTA-271 can efficiently attenuate Botryosphaeria dieback by enhancing some host immune responses and detoxifying both phytotoxins produced by N. parvum.
DOI: 10.3389/fpls.2019.00025
PubMed: 30733727
PubMed Central: PMC6354549
Affiliations:
- France, Suisse
- Canton de Fribourg, Champagne-Ardenne, Grand Est
- Fribourg, Reims
- Université de Fribourg
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FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Champagne-Ardenne</region><settlement type="city">Reims</settlement></placeName></affiliation></author><author><name sortKey="Abou Mansour, Eliane" sort="Abou Mansour, Eliane" uniqKey="Abou Mansour E" first="Eliane" last="Abou-Mansour">Eliane Abou-Mansour</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Biology, University of Fribourg, Fribourg, Switzerland.</nlm:affiliation><country xml:lang="fr">Suisse</country><wicri:regionArea>Department of Plant Biology, University of Fribourg, Fribourg</wicri:regionArea><orgName type="university">Université de Fribourg</orgName><placeName><settlement type="city">Fribourg</settlement><region nuts="3" type="region">Canton de Fribourg</region></placeName></affiliation></author><author><name sortKey="Courteaux, Barbara" sort="Courteaux, Barbara" uniqKey="Courteaux B" first="Barbara" last="Courteaux">Barbara Courteaux</name><affiliation wicri:level="3"><nlm:affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Champagne-Ardenne</region><settlement type="city">Reims</settlement></placeName></affiliation></author><author><name sortKey="Rabenoelina, Fanja" sort="Rabenoelina, Fanja" uniqKey="Rabenoelina F" first="Fanja" last="Rabenoelina">Fanja Rabenoelina</name><affiliation wicri:level="3"><nlm:affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Champagne-Ardenne</region><settlement type="city">Reims</settlement></placeName></affiliation></author><author><name sortKey="Clement, Christophe" sort="Clement, Christophe" uniqKey="Clement C" first="Christophe" last="Clément">Christophe Clément</name><affiliation wicri:level="3"><nlm:affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Champagne-Ardenne</region><settlement type="city">Reims</settlement></placeName></affiliation></author><author><name sortKey="Fontaine, Florence" sort="Fontaine, Florence" uniqKey="Fontaine F" first="Florence" last="Fontaine">Florence Fontaine</name><affiliation wicri:level="3"><nlm:affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Champagne-Ardenne</region><settlement type="city">Reims</settlement></placeName></affiliation></author><author><name sortKey="Aziz, Aziz" sort="Aziz, Aziz" uniqKey="Aziz A" first="Aziz" last="Aziz">Aziz Aziz</name><affiliation wicri:level="3"><nlm:affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Champagne-Ardenne</region><settlement type="city">Reims</settlement></placeName></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant pathogens have evolved various strategies to enter hosts and cause diseases. Particularly <i>Neofusicoccum parvum</i>, a member of Botryosphaeria dieback consortium, can secrete the phytotoxins (-)-terremutin and (<i>R</i>)-mellein during grapevine colonization. The contribution of phytotoxins to Botryosphaeria dieback symptoms still remains unknown. Moreover, there are currently no efficient control strategies of this disease, and agro-environmental concerns have raised increasing interest in biocontrol strategies to limit disease spread in vineyards, especially by using some promising beneficial bacteria. Here, we first examined <i>in planta</i> the biocontrol capacity of <i>Bacillus subtilis</i> PTA-271 against <i>N. parvum Np</i>-Bt67 strain producing both (-)-terremutin and (<i>R</i>)-mellein. We then focused on the direct effects of PTA-271 on pathogen growth and the fate of pure phytotoxins, and explored the capacity of PTA-271 to induce or prime grapevine immunity upon pathogen infection or phytotoxin exposure. Results provided evidence that PTA-271 significantly protects grapevine cuttings against <i>N. parvum</i> and significantly primes the expression of <i>PR2</i> (encoding a β-1,3-glucanase) and <i>NCED2</i> (9-<i>cis</i>-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis) genes upon pathogen challenge. Using <i>in vitro</i> plantlets, we also showed that PTA-271 triggers the expression of salicylic acid- and jasmonic acid-responsive genes, including <i>GST1</i> (encoding a glutathione-<i>S</i>-transferase) involved in detoxification process. However, in PTA-271-pretreated plantlets, exogenous (-)-terremutin strongly lowered the expression of most of upregulated genes, except <i>GST1</i>. Data also indicated that PTA-271 can detoxify both (-)-terremutin and (<i>R</i>)-mellein and antagonize <i>N. parvum</i> under <i>in vitro</i> conditions. Our findings highlight (-)-terremutin and (<i>R</i>)-mellein as key aggressive molecules produced by <i>N. parvum</i> that may weaken grapevine immunity to promote Botryosphaeria dieback symptoms. However, PTA-271 can efficiently attenuate Botryosphaeria dieback by enhancing some host immune responses and detoxifying both phytotoxins produced by <i>N. parvum</i>.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30733727</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>10</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle><i>Bacillus subtilis</i> PTA-271 Counteracts Botryosphaeria Dieback in Grapevine, Triggering Immune Responses and Detoxification of Fungal Phytotoxins.</ArticleTitle><Pagination><MedlinePgn>25</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2019.00025</ELocationID><Abstract><AbstractText>Plant pathogens have evolved various strategies to enter hosts and cause diseases. Particularly <i>Neofusicoccum parvum</i>, a member of Botryosphaeria dieback consortium, can secrete the phytotoxins (-)-terremutin and (<i>R</i>)-mellein during grapevine colonization. The contribution of phytotoxins to Botryosphaeria dieback symptoms still remains unknown. Moreover, there are currently no efficient control strategies of this disease, and agro-environmental concerns have raised increasing interest in biocontrol strategies to limit disease spread in vineyards, especially by using some promising beneficial bacteria. Here, we first examined <i>in planta</i> the biocontrol capacity of <i>Bacillus subtilis</i> PTA-271 against <i>N. parvum Np</i>-Bt67 strain producing both (-)-terremutin and (<i>R</i>)-mellein. We then focused on the direct effects of PTA-271 on pathogen growth and the fate of pure phytotoxins, and explored the capacity of PTA-271 to induce or prime grapevine immunity upon pathogen infection or phytotoxin exposure. Results provided evidence that PTA-271 significantly protects grapevine cuttings against <i>N. parvum</i> and significantly primes the expression of <i>PR2</i> (encoding a β-1,3-glucanase) and <i>NCED2</i> (9-<i>cis</i>-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis) genes upon pathogen challenge. Using <i>in vitro</i> plantlets, we also showed that PTA-271 triggers the expression of salicylic acid- and jasmonic acid-responsive genes, including <i>GST1</i> (encoding a glutathione-<i>S</i>-transferase) involved in detoxification process. However, in PTA-271-pretreated plantlets, exogenous (-)-terremutin strongly lowered the expression of most of upregulated genes, except <i>GST1</i>. Data also indicated that PTA-271 can detoxify both (-)-terremutin and (<i>R</i>)-mellein and antagonize <i>N. parvum</i> under <i>in vitro</i> conditions. Our findings highlight (-)-terremutin and (<i>R</i>)-mellein as key aggressive molecules produced by <i>N. parvum</i> that may weaken grapevine immunity to promote Botryosphaeria dieback symptoms. However, PTA-271 can efficiently attenuate Botryosphaeria dieback by enhancing some host immune responses and detoxifying both phytotoxins produced by <i>N. parvum</i>.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Trotel-Aziz</LastName><ForeName>Patricia</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abou-Mansour</LastName><ForeName>Eliane</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Plant Biology, University of Fribourg, Fribourg, Switzerland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Courteaux</LastName><ForeName>Barbara</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rabenoelina</LastName><ForeName>Fanja</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Clément</LastName><ForeName>Christophe</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fontaine</LastName><ForeName>Florence</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Aziz</LastName><ForeName>Aziz</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Research Unit EA 4707 RIBP, SFR Condorcet FR CNRS 3417, University of Reims Champagne-Ardenne, Reims, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>01</Month><Day>24</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Bacillus subtilis</Keyword><Keyword MajorTopicYN="N">Botryosphaeria dieback</Keyword><Keyword MajorTopicYN="N">Neofusicoccum parvum</Keyword><Keyword MajorTopicYN="N">biocontrol</Keyword><Keyword MajorTopicYN="N">grapevine</Keyword><Keyword 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|texte= Bacillus subtilis PTA-271 Counteracts Botryosphaeria Dieback in Grapevine, Triggering Immune Responses and Detoxification of Fungal Phytotoxins.
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