The transcription factor CfSte12 of Colletotrichum fructicola is a key regulator of early apple Glomerella leaf spot pathogenesis.
Identifieur interne : 000019 ( Main/Exploration ); précédent : 000018; suivant : 000020The transcription factor CfSte12 of Colletotrichum fructicola is a key regulator of early apple Glomerella leaf spot pathogenesis.
Auteurs : Wenkui Liu [République populaire de Chine] ; Xiaofei Liang [République populaire de Chine] ; Mark L. Gleason [États-Unis] ; Mengyu Cao [République populaire de Chine] ; Rong Zhang [République populaire de Chine] ; Guangyu Sun [République populaire de Chine]Source :
- Applied and environmental microbiology [ 1098-5336 ] ; 2020.
Abstract
Glomerella leaf spot (GLS), caused by Colletotrichum fructicola, is a rapidly emerging disease leading to defoliation, fruit spot and storage fruit rot on apple in China. Little is known about the mechanisms of GLS pathogenesis. Early transcriptome analysis revealed that expression of the zinc finger transcription factor CfSte12 gene in C. fructicola was up-regulated in appressoria and leaf infection. To investigate functions of CfSte12 during pathogenesis, we constructed gene deletion mutants (ΔCfSte12) by homologous recombination. Phenotypic analysis revealed that CfSte12 was involved in pathogenesis of non-wounded apple fruit and leaf, as well as wounded apple fruit. Subsequent histological studies revealed that loss of pathogenicity by ΔCfSte12 on apple leaf was expressed as defects of conidium germination, appressorium development and appressorium-mediated penetration. Further RNA sequencing-based transcriptome comparison revealed that CfSte12 modulates the expression of genes related to appressorium function (e.g. the tetraspanin PLS1, Gas1-like proteins, cutinases, melanin biosynthesis genes) and candidate effectors likely involved in plant interaction. In sum, our results demonstrated that CfSte12 is a key regulator of early apple GLS pathogenesis in C. fructicola Besides, CfSte12 is also needed by sexual development of perithecia and ascospores.Importance Glomerella leaf spot (GLS) is an emerging fungal disease of apple that causes huge economic losses in Asia, North America and South America. The damage inflicted by GLS manifests in rapid necrosis of leaves, severe defoliation and necrotic spot on fruit surface. However, few studies have addressed mechanisms of GLS pathogenesis. In this study, we identified and characterized a key pathogenicity-related transcription factor, CfSte12, of Colletotrichum fructicola that contributes to GLS pathogenesis. We provided evidence that the CfSte12 protein regulates many important pathogenic processes of GLS, including conidium germination, appressorium formation, appressorium-mediated penetration, and colonization. CfSte12 also impacts development of structures needed for sexual reproduction which are vital for the GLS disease cycle. These results revealed a key pathogenicity-related transcription factor CfSte12 in C. fructicola that causing GLS.
DOI: 10.1128/AEM.02212-20
PubMed: 33067192
Affiliations:
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712100</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation></author><author><name sortKey="Liang, Xiaofei" sort="Liang, Xiaofei" uniqKey="Liang X" first="Xiaofei" last="Liang">Xiaofei Liang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China xiaofeiliang@nwsuaf.edu.cn.</nlm:affiliation><country wicri:rule="url">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation></author><author><name sortKey="Gleason, Mark L" sort="Gleason, Mark L" uniqKey="Gleason M" first="Mark L" last="Gleason">Mark L. Gleason</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011</wicri:regionArea><orgName type="university">Université d'État de l'Iowa</orgName><placeName><settlement type="city">Ames (Iowa)</settlement><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Cao, Mengyu" sort="Cao, Mengyu" uniqKey="Cao M" first="Mengyu" last="Cao">Mengyu Cao</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Rong" sort="Zhang, Rong" uniqKey="Zhang R" first="Rong" last="Zhang">Rong Zhang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation></author><author><name sortKey="Sun, Guangyu" sort="Sun, Guangyu" uniqKey="Sun G" first="Guangyu" last="Sun">Guangyu Sun</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China sgy@nwsuaf.edu.cn.</nlm:affiliation><country wicri:rule="url">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100</wicri:regionArea><wicri:noRegion>Shaanxi Province 712100</wicri:noRegion></affiliation></author></analytic><series><title level="j">Applied and environmental microbiology</title><idno type="eISSN">1098-5336</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">Glomerella leaf spot (GLS), caused by <i>Colletotrichum fructicola</i>, is a rapidly emerging disease leading to defoliation, fruit spot and storage fruit rot on apple in China. Little is known about the mechanisms of GLS pathogenesis. Early transcriptome analysis revealed that expression of the zinc finger transcription factor <i>CfSte12</i> gene in <i>C. fructicola</i> was up-regulated in appressoria and leaf infection. To investigate functions of <i>CfSte12</i> during pathogenesis, we constructed gene deletion mutants (Δ<i>CfSte12</i>) by homologous recombination. Phenotypic analysis revealed that CfSte12 was involved in pathogenesis of non-wounded apple fruit and leaf, as well as wounded apple fruit. Subsequent histological studies revealed that loss of pathogenicity by Δ<i>CfSte12</i> on apple leaf was expressed as defects of conidium germination, appressorium development and appressorium-mediated penetration. Further RNA sequencing-based transcriptome comparison revealed that CfSte12 modulates the expression of genes related to appressorium function (e.g. the tetraspanin PLS1, Gas1-like proteins, cutinases, melanin biosynthesis genes) and candidate effectors likely involved in plant interaction. In sum, our results demonstrated that CfSte12 is a key regulator of early apple GLS pathogenesis in <i>C. fructicola</i> Besides, CfSte12 is also needed by sexual development of perithecia and ascospores.<b>Importance</b> Glomerella leaf spot (GLS) is an emerging fungal disease of apple that causes huge economic losses in Asia, North America and South America. The damage inflicted by GLS manifests in rapid necrosis of leaves, severe defoliation and necrotic spot on fruit surface. However, few studies have addressed mechanisms of GLS pathogenesis. In this study, we identified and characterized a key pathogenicity-related transcription factor, CfSte12, of <i>Colletotrichum fructicola</i> that contributes to GLS pathogenesis. We provided evidence that the CfSte12 protein regulates many important pathogenic processes of GLS, including conidium germination, appressorium formation, appressorium-mediated penetration, and colonization. CfSte12 also impacts development of structures needed for sexual reproduction which are vital for the GLS disease cycle. These results revealed a key pathogenicity-related transcription factor CfSte12 in <i>C. fructicola</i> that causing GLS.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33067192</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>17</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1098-5336</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Oct</Month><Day>16</Day></PubDate></JournalIssue><Title>Applied and environmental microbiology</Title><ISOAbbreviation>Appl Environ Microbiol</ISOAbbreviation></Journal><ArticleTitle>The transcription factor CfSte12 of <i>Colletotrichum fructicola</i> is a key regulator of early apple Glomerella leaf spot pathogenesis.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">AEM.02212-20</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/AEM.02212-20</ELocationID><Abstract><AbstractText>Glomerella leaf spot (GLS), caused by <i>Colletotrichum fructicola</i>, is a rapidly emerging disease leading to defoliation, fruit spot and storage fruit rot on apple in China. Little is known about the mechanisms of GLS pathogenesis. Early transcriptome analysis revealed that expression of the zinc finger transcription factor <i>CfSte12</i> gene in <i>C. fructicola</i> was up-regulated in appressoria and leaf infection. To investigate functions of <i>CfSte12</i> during pathogenesis, we constructed gene deletion mutants (Δ<i>CfSte12</i>) by homologous recombination. Phenotypic analysis revealed that CfSte12 was involved in pathogenesis of non-wounded apple fruit and leaf, as well as wounded apple fruit. Subsequent histological studies revealed that loss of pathogenicity by Δ<i>CfSte12</i> on apple leaf was expressed as defects of conidium germination, appressorium development and appressorium-mediated penetration. Further RNA sequencing-based transcriptome comparison revealed that CfSte12 modulates the expression of genes related to appressorium function (e.g. the tetraspanin PLS1, Gas1-like proteins, cutinases, melanin biosynthesis genes) and candidate effectors likely involved in plant interaction. In sum, our results demonstrated that CfSte12 is a key regulator of early apple GLS pathogenesis in <i>C. fructicola</i> Besides, CfSte12 is also needed by sexual development of perithecia and ascospores.<b>Importance</b> Glomerella leaf spot (GLS) is an emerging fungal disease of apple that causes huge economic losses in Asia, North America and South America. The damage inflicted by GLS manifests in rapid necrosis of leaves, severe defoliation and necrotic spot on fruit surface. However, few studies have addressed mechanisms of GLS pathogenesis. In this study, we identified and characterized a key pathogenicity-related transcription factor, CfSte12, of <i>Colletotrichum fructicola</i> that contributes to GLS pathogenesis. We provided evidence that the CfSte12 protein regulates many important pathogenic processes of GLS, including conidium germination, appressorium formation, appressorium-mediated penetration, and colonization. CfSte12 also impacts development of structures needed for sexual reproduction which are vital for the GLS disease cycle. These results revealed a key pathogenicity-related transcription factor CfSte12 in <i>C. fructicola</i> that causing GLS.</AbstractText><CopyrightInformation>Copyright © 2020 American Society for Microbiology.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Wenkui</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liang</LastName><ForeName>Xiaofei</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China xiaofeiliang@nwsuaf.edu.cn.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gleason</LastName><ForeName>Mark L</ForeName><Initials>ML</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cao</LastName><ForeName>Mengyu</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Rong</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Guangyu</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi Province 712100, China sgy@nwsuaf.edu.cn.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Appl Environ Microbiol</MedlineTA><NlmUniqueID>7605801</NlmUniqueID><ISSNLinking>0099-2240</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>17</Day><Hour>5</Hour><Minute>24</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33067192</ArticleId><ArticleId IdType="pii">AEM.02212-20</ArticleId><ArticleId IdType="doi">10.1128/AEM.02212-20</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Iowa</li></region><settlement><li>Ames (Iowa)</li></settlement><orgName><li>Université d'État de l'Iowa</li></orgName></list><tree><country name="République populaire de Chine"><noRegion><name sortKey="Liu, Wenkui" sort="Liu, Wenkui" uniqKey="Liu W" first="Wenkui" last="Liu">Wenkui Liu</name></noRegion><name sortKey="Cao, Mengyu" sort="Cao, Mengyu" uniqKey="Cao M" first="Mengyu" last="Cao">Mengyu Cao</name><name sortKey="Cao, Mengyu" sort="Cao, Mengyu" uniqKey="Cao M" first="Mengyu" last="Cao">Mengyu Cao</name><name sortKey="Liang, Xiaofei" sort="Liang, Xiaofei" uniqKey="Liang X" first="Xiaofei" last="Liang">Xiaofei Liang</name><name sortKey="Liang, Xiaofei" sort="Liang, Xiaofei" uniqKey="Liang X" first="Xiaofei" last="Liang">Xiaofei Liang</name><name sortKey="Liu, Wenkui" sort="Liu, Wenkui" uniqKey="Liu W" first="Wenkui" last="Liu">Wenkui Liu</name><name sortKey="Sun, Guangyu" sort="Sun, Guangyu" uniqKey="Sun G" first="Guangyu" last="Sun">Guangyu Sun</name><name sortKey="Sun, Guangyu" sort="Sun, Guangyu" uniqKey="Sun G" first="Guangyu" last="Sun">Guangyu Sun</name><name sortKey="Zhang, Rong" sort="Zhang, Rong" uniqKey="Zhang R" first="Rong" last="Zhang">Rong Zhang</name><name sortKey="Zhang, Rong" sort="Zhang, Rong" uniqKey="Zhang R" first="Rong" last="Zhang">Rong Zhang</name></country><country name="États-Unis"><region name="Iowa"><name sortKey="Gleason, Mark L" sort="Gleason, Mark L" uniqKey="Gleason M" first="Mark L" last="Gleason">Mark L. 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