Deciphering the Infectious Process of Colletotrichum lupini in Lupin through Transcriptomic and Proteomic Analysis.
Identifieur interne : 000188 ( Main/Exploration ); précédent : 000187; suivant : 000189Deciphering the Infectious Process of Colletotrichum lupini in Lupin through Transcriptomic and Proteomic Analysis.
Auteurs : Guillaume Dubrulle [France] ; Adeline Picot [France] ; Stéphanie Madec [France] ; Erwan Corre [France] ; Audrey Pawtowski [France] ; Riccardo Baroncelli [Espagne] ; Michel Zivy [France] ; Thierry Balliau [France] ; Gaétan Le Floch [France] ; Flora Pensec [France]Source :
- Microorganisms [ 2076-2607 ] ; 2020.
Abstract
The fungal phytopathogen Colletotrichum lupini is responsible for lupin anthracnose, resulting in significant yield losses worldwide. The molecular mechanisms underlying this infectious process are yet to be elucidated. This study proposes to evaluate C. lupini gene expression and protein synthesis during lupin infection, using, respectively, an RNAseq-based transcriptomic approach and a mass spectrometry-based proteomic approach. Patterns of differentially-expressed genes in planta were evaluated from 24 to 84 hours post-inoculation, and compared to in vitro cultures. A total of 897 differentially-expressed genes were identified from C. lupini during interaction with white lupin, of which 520 genes were predicted to have a putative function, including carbohydrate active enzyme, effector, protease or transporter-encoding genes, commonly described as pathogenicity factors for other Colletotrichum species during plant infection, and 377 hypothetical proteins. Simultaneously, a total of 304 proteins produced during the interaction were identified and quantified by mass spectrometry. Taken together, the results highlight that the dynamics of symptoms, gene expression and protein synthesis shared similarities to those of hemibiotrophic pathogens. In addition, a few genes with unknown or poorly-described functions were found to be specifically associated with the early or late stages of infection, suggesting that they may be of importance for pathogenicity. This study, conducted for the first time on a species belonging to the Colletotrichum acutatum species complex, presents an opportunity to deepen functional analyses of the genes involved in the pathogenicity of Colletotrichum spp. during the onset of plant infection.
DOI: 10.3390/microorganisms8101621
PubMed: 33096724
PubMed Central: PMC7589765
Affiliations:
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type="city">Plouzané</settlement></placeName></affiliation></author><author><name sortKey="Picot, Adeline" sort="Picot, Adeline" uniqKey="Picot A" first="Adeline" last="Picot">Adeline Picot</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Plouzané</settlement></placeName></affiliation></author><author><name sortKey="Madec, Stephanie" sort="Madec, Stephanie" uniqKey="Madec S" first="Stéphanie" last="Madec">Stéphanie Madec</name><affiliation wicri:level="3"><nlm:affiliation>CNRS, IRD, Ifremer, LEMAR, Université de Brest, F-29280 Plouzané, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, IRD, Ifremer, LEMAR, Université de Brest, F-29280 Plouzané</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Plouzané</settlement></placeName></affiliation></author><author><name sortKey="Corre, Erwan" sort="Corre, Erwan" uniqKey="Corre E" first="Erwan" last="Corre">Erwan Corre</name><affiliation wicri:level="3"><nlm:affiliation>Station Biologique de Roscoff, FR2424 CNRS Sorbonne Université, Place Georges Teissier, 29680 Roscoff, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Station Biologique de Roscoff, FR2424 CNRS Sorbonne Université, Place Georges Teissier, 29680 Roscoff</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Roscoff</settlement></placeName></affiliation></author><author><name sortKey="Pawtowski, Audrey" sort="Pawtowski, Audrey" uniqKey="Pawtowski A" first="Audrey" last="Pawtowski">Audrey Pawtowski</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Plouzané</settlement></placeName></affiliation></author><author><name sortKey="Baroncelli, Riccardo" sort="Baroncelli, Riccardo" uniqKey="Baroncelli R" first="Riccardo" last="Baroncelli">Riccardo Baroncelli</name><affiliation wicri:level="2"><nlm:affiliation>Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), University of Salamanca, Calle del Duero 12, 37185 Villamayor (Salamanca), Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), University of Salamanca, Calle del Duero 12, 37185 Villamayor (Salamanca)</wicri:regionArea><placeName><region nuts="2" type="communauté">Castille-et-León</region></placeName></affiliation></author><author><name sortKey="Zivy, Michel" sort="Zivy, Michel" uniqKey="Zivy M" first="Michel" last="Zivy">Michel Zivy</name><affiliation wicri:level="3"><nlm:affiliation>INRAE le Moulon, Plateforme PAPPSO, ferme du Moulon, 91190 Gif-sur-Yvette, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE le Moulon, Plateforme PAPPSO, ferme du Moulon, 91190 Gif-sur-Yvette</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Gif-sur-Yvette</settlement></placeName></affiliation></author><author><name sortKey="Balliau, Thierry" sort="Balliau, Thierry" uniqKey="Balliau T" first="Thierry" last="Balliau">Thierry Balliau</name><affiliation wicri:level="3"><nlm:affiliation>INRAE le Moulon, Plateforme PAPPSO, ferme du Moulon, 91190 Gif-sur-Yvette, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRAE le Moulon, Plateforme PAPPSO, ferme du Moulon, 91190 Gif-sur-Yvette</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Gif-sur-Yvette</settlement></placeName></affiliation></author><author><name sortKey="Le Floch, Gaetan" sort="Le Floch, Gaetan" uniqKey="Le Floch G" first="Gaétan" last="Le Floch">Gaétan Le Floch</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Plouzané</settlement></placeName></affiliation></author><author><name sortKey="Pensec, Flora" sort="Pensec, Flora" uniqKey="Pensec F" first="Flora" last="Pensec">Flora Pensec</name><affiliation wicri:level="3"><nlm:affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané</wicri:regionArea><placeName><region type="region" nuts="2">Région Bretagne</region><settlement type="city">Plouzané</settlement></placeName></affiliation></author></analytic><series><title level="j">Microorganisms</title><idno type="ISSN">2076-2607</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">The fungal phytopathogen <i>Colletotrichum lupini</i> is responsible for lupin anthracnose, resulting in significant yield losses worldwide. The molecular mechanisms underlying this infectious process are yet to be elucidated. This study proposes to evaluate <i>C. lupini</i> gene expression and protein synthesis during lupin infection, using, respectively, an RNAseq-based transcriptomic approach and a mass spectrometry-based proteomic approach. Patterns of differentially-expressed genes in planta were evaluated from 24 to 84 hours post-inoculation, and compared to in vitro cultures. A total of 897 differentially-expressed genes were identified from <i>C. lupini</i> during interaction with white lupin, of which 520 genes were predicted to have a putative function, including carbohydrate active enzyme, effector, protease or transporter-encoding genes, commonly described as pathogenicity factors for other <i>Colletotrichum</i> species during plant infection, and 377 hypothetical proteins. Simultaneously, a total of 304 proteins produced during the interaction were identified and quantified by mass spectrometry. Taken together, the results highlight that the dynamics of symptoms, gene expression and protein synthesis shared similarities to those of hemibiotrophic pathogens. In addition, a few genes with unknown or poorly-described functions were found to be specifically associated with the early or late stages of infection, suggesting that they may be of importance for pathogenicity. This study, conducted for the first time on a species belonging to the <i>Colletotrichum acutatum</i> species complex, presents an opportunity to deepen functional analyses of the genes involved in the pathogenicity of <i>Colletotrichum</i> spp. during the onset of plant infection.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">33096724</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>30</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Print">2076-2607</ISSN><JournalIssue CitedMedium="Print"><Volume>8</Volume><Issue>10</Issue><PubDate><Year>2020</Year><Month>Oct</Month><Day>21</Day></PubDate></JournalIssue><Title>Microorganisms</Title><ISOAbbreviation>Microorganisms</ISOAbbreviation></Journal><ArticleTitle>Deciphering the Infectious Process of <i>Colletotrichum lupini</i> in Lupin through Transcriptomic and Proteomic Analysis.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E1621</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/microorganisms8101621</ELocationID><Abstract><AbstractText>The fungal phytopathogen <i>Colletotrichum lupini</i> is responsible for lupin anthracnose, resulting in significant yield losses worldwide. The molecular mechanisms underlying this infectious process are yet to be elucidated. This study proposes to evaluate <i>C. lupini</i> gene expression and protein synthesis during lupin infection, using, respectively, an RNAseq-based transcriptomic approach and a mass spectrometry-based proteomic approach. Patterns of differentially-expressed genes in planta were evaluated from 24 to 84 hours post-inoculation, and compared to in vitro cultures. A total of 897 differentially-expressed genes were identified from <i>C. lupini</i> during interaction with white lupin, of which 520 genes were predicted to have a putative function, including carbohydrate active enzyme, effector, protease or transporter-encoding genes, commonly described as pathogenicity factors for other <i>Colletotrichum</i> species during plant infection, and 377 hypothetical proteins. Simultaneously, a total of 304 proteins produced during the interaction were identified and quantified by mass spectrometry. Taken together, the results highlight that the dynamics of symptoms, gene expression and protein synthesis shared similarities to those of hemibiotrophic pathogens. In addition, a few genes with unknown or poorly-described functions were found to be specifically associated with the early or late stages of infection, suggesting that they may be of importance for pathogenicity. This study, conducted for the first time on a species belonging to the <i>Colletotrichum acutatum</i> species complex, presents an opportunity to deepen functional analyses of the genes involved in the pathogenicity of <i>Colletotrichum</i> spp. during the onset of plant infection.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Dubrulle</LastName><ForeName>Guillaume</ForeName><Initials>G</Initials><Identifier Source="ORCID">0000-0001-8358-2146</Identifier><AffiliationInfo><Affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Picot</LastName><ForeName>Adeline</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Madec</LastName><ForeName>Stéphanie</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>CNRS, IRD, Ifremer, LEMAR, Université de Brest, F-29280 Plouzané, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Corre</LastName><ForeName>Erwan</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0001-6354-2278</Identifier><AffiliationInfo><Affiliation>Station Biologique de Roscoff, FR2424 CNRS Sorbonne Université, Place Georges Teissier, 29680 Roscoff, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pawtowski</LastName><ForeName>Audrey</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baroncelli</LastName><ForeName>Riccardo</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-5878-1159</Identifier><AffiliationInfo><Affiliation>Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), University of Salamanca, Calle del Duero 12, 37185 Villamayor (Salamanca), Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zivy</LastName><ForeName>Michel</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>INRAE le Moulon, Plateforme PAPPSO, ferme du Moulon, 91190 Gif-sur-Yvette, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Balliau</LastName><ForeName>Thierry</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>INRAE le Moulon, Plateforme PAPPSO, ferme du Moulon, 91190 Gif-sur-Yvette, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Le Floch</LastName><ForeName>Gaétan</ForeName><Initials>G</Initials><Identifier Source="ORCID">0000-0001-7413-8852</Identifier><AffiliationInfo><Affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pensec</LastName><ForeName>Flora</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Laboratoire Universitaire de Biodiversité et Écologie Microbienne, ESIAB, Université de Brest, F-29280 Plouzané, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>RBRE160116CR0530019</GrantID><Agency>Région Bretagne et pays de la Loire et FEADER</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>21</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Microorganisms</MedlineTA><NlmUniqueID>101625893</NlmUniqueID><ISSNLinking>2076-2607</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">anthracnose disease</Keyword><Keyword MajorTopicYN="N">pathogenicity factors</Keyword><Keyword MajorTopicYN="N">proteome</Keyword><Keyword MajorTopicYN="N">transcriptome</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>09</Month><Day>25</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>10</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>10</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>24</Day><Hour>1</Hour><Minute>1</Minute></PubMedPubDate><PubMedPubDate 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