Phosphatase-associated protein MoTip41 interacts with the phosphatase MoPpe1 to mediate crosstalk between TOR and cell wall integrity signalling during infection by the rice blast fungus Magnaporthe oryzae.
Identifieur interne : 000070 ( Main/Exploration ); précédent : 000069; suivant : 000071Phosphatase-associated protein MoTip41 interacts with the phosphatase MoPpe1 to mediate crosstalk between TOR and cell wall integrity signalling during infection by the rice blast fungus Magnaporthe oryzae.
Auteurs : Bin Qian [République populaire de Chine] ; Xinyu Liu [République populaire de Chine] ; Ziyuan Ye [République populaire de Chine] ; Qikun Zhou [République populaire de Chine] ; Peng Liu [République populaire de Chine] ; Ziyi Yin [République populaire de Chine] ; Wenhao Wang [République populaire de Chine] ; Xiaobo Zheng [République populaire de Chine] ; Haifeng Zhang [République populaire de Chine] ; Zhengguang Zhang [République populaire de Chine]Source :
- Environmental microbiology [ 1462-2920 ] ; 2020.
Abstract
The type 2A (PP2A) and type 2A-like (PP4 and PP6) serine/threonine phosphatases participate in a variety of cellular processes, such as cell cycle progression, signal transduction and apoptosis. Previously, we reported that the PP6 catalytic subunit MoPpe1, which interacts with and is suppressed by type 2A associated protein of 42 kDa (MoTap42), an essential protein involved in the target of rapamycin (TOR) signalling pathway, has important roles in development, virulence and activation of the cell wall integrity (CWI) pathway in the rice blast fungus Magnaporthe oryzae. Here, we show that Tap42-interacting protein 41 (MoTip41) mediates crosstalk between the TOR and CWI signalling pathways; and participates in the TOR pathway via interaction with MoPpe1, but not MoTap42. The deletion of MoTIP41 resulted in disruption of CWI signalling, autophagy, vegetative growth, appressorium function and plant infection, as well as increased sensitivity to rapamycin. Further investigation revealed that MoTip41 modulates activation of the CWI pathway in response to infection by interfering with the interaction between MoTap42 and MoPpe1. These findings enhance our understanding of how crosstalk between TOR and CWI signalling modulates the development and pathogenicity of M. oryzae.
DOI: 10.1111/1462-2920.15136
PubMed: 32564502
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populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhou, Qikun" sort="Zhou, Qikun" uniqKey="Zhou Q" first="Qikun" last="Zhou">Qikun Zhou</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Yin, Ziyi" sort="Yin, Ziyi" uniqKey="Yin Z" first="Ziyi" last="Yin">Ziyi Yin</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Wenhao" sort="Wang, Wenhao" uniqKey="Wang W" first="Wenhao" last="Wang">Wenhao Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country 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Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32564502</idno><idno type="pmid">32564502</idno><idno type="doi">10.1111/1462-2920.15136</idno><idno type="wicri:Area/Main/Corpus">000058</idno><idno type="wicri:explorRef" 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Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Xinyu" sort="Liu, Xinyu" uniqKey="Liu X" first="Xinyu" last="Liu">Xinyu Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Ye, Ziyuan" sort="Ye, Ziyuan" uniqKey="Ye Z" first="Ziyuan" last="Ye">Ziyuan Ye</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhou, Qikun" sort="Zhou, Qikun" uniqKey="Zhou Q" first="Qikun" last="Zhou">Qikun Zhou</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Peng" sort="Liu, Peng" uniqKey="Liu P" first="Peng" last="Liu">Peng Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Yin, Ziyi" sort="Yin, Ziyi" uniqKey="Yin Z" first="Ziyi" last="Yin">Ziyi Yin</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Wenhao" sort="Wang, Wenhao" uniqKey="Wang W" first="Wenhao" last="Wang">Wenhao Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zheng, Xiaobo" sort="Zheng, Xiaobo" uniqKey="Zheng X" first="Xiaobo" last="Zheng">Xiaobo Zheng</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Haifeng" sort="Zhang, Haifeng" uniqKey="Zhang H" first="Haifeng" last="Zhang">Haifeng Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Zhengguang" sort="Zhang, Zhengguang" uniqKey="Zhang Z" first="Zhengguang" last="Zhang">Zhengguang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author></analytic><series><title level="j">Environmental microbiology</title><idno type="eISSN">1462-2920</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 type 2A (PP2A) and type 2A-like (PP4 and PP6) serine/threonine phosphatases participate in a variety of cellular processes, such as cell cycle progression, signal transduction and apoptosis. Previously, we reported that the PP6 catalytic subunit MoPpe1, which interacts with and is suppressed by type 2A associated protein of 42 kDa (MoTap42), an essential protein involved in the target of rapamycin (TOR) signalling pathway, has important roles in development, virulence and activation of the cell wall integrity (CWI) pathway in the rice blast fungus Magnaporthe oryzae. Here, we show that Tap42-interacting protein 41 (MoTip41) mediates crosstalk between the TOR and CWI signalling pathways; and participates in the TOR pathway via interaction with MoPpe1, but not MoTap42. The deletion of MoTIP41 resulted in disruption of CWI signalling, autophagy, vegetative growth, appressorium function and plant infection, as well as increased sensitivity to rapamycin. Further investigation revealed that MoTip41 modulates activation of the CWI pathway in response to infection by interfering with the interaction between MoTap42 and MoPpe1. These findings enhance our understanding of how crosstalk between TOR and CWI signalling modulates the development and pathogenicity of M. oryzae.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32564502</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>22</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1462-2920</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Jun</Month><Day>20</Day></PubDate></JournalIssue><Title>Environmental microbiology</Title><ISOAbbreviation>Environ Microbiol</ISOAbbreviation></Journal><ArticleTitle>Phosphatase-associated protein MoTip41 interacts with the phosphatase MoPpe1 to mediate crosstalk between TOR and cell wall integrity signalling during infection by the rice blast fungus Magnaporthe oryzae.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/1462-2920.15136</ELocationID><Abstract><AbstractText>The type 2A (PP2A) and type 2A-like (PP4 and PP6) serine/threonine phosphatases participate in a variety of cellular processes, such as cell cycle progression, signal transduction and apoptosis. Previously, we reported that the PP6 catalytic subunit MoPpe1, which interacts with and is suppressed by type 2A associated protein of 42 kDa (MoTap42), an essential protein involved in the target of rapamycin (TOR) signalling pathway, has important roles in development, virulence and activation of the cell wall integrity (CWI) pathway in the rice blast fungus Magnaporthe oryzae. Here, we show that Tap42-interacting protein 41 (MoTip41) mediates crosstalk between the TOR and CWI signalling pathways; and participates in the TOR pathway via interaction with MoPpe1, but not MoTap42. The deletion of MoTIP41 resulted in disruption of CWI signalling, autophagy, vegetative growth, appressorium function and plant infection, as well as increased sensitivity to rapamycin. Further investigation revealed that MoTip41 modulates activation of the CWI pathway in response to infection by interfering with the interaction between MoTap42 and MoPpe1. These findings enhance our understanding of how crosstalk between TOR and CWI signalling modulates the development and pathogenicity of M. oryzae.</AbstractText><CopyrightInformation>© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Qian</LastName><ForeName>Bin</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Xinyu</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ye</LastName><ForeName>Ziyuan</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Qikun</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Peng</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Ziyi</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Wenhao</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zheng</LastName><ForeName>Xiaobo</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Haifeng</ForeName><Initials>H</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7963-9071</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Zhengguang</ForeName><Initials>Z</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-8253-4505</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>KYT201805</GrantID><Agency>Fundamental Research Funds for the Central Universities</Agency><Country></Country></Grant><Grant><GrantID>KYYZ201903</GrantID><Agency>Fundamental Research Funds for the Central Universities</Agency><Country></Country></Grant><Grant><GrantID>KYZ201816</GrantID><Agency>Fundamental Research Funds for the Central Universities</Agency><Country></Country></Grant><Grant><GrantID>2017</GrantID><Agency>Innovation Team Program for Jiangsu Universities</Agency><Country></Country></Grant><Grant><GrantID>31671978</GrantID><Agency>National Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>2016YFD0300700/2016YFD0300706</GrantID><Agency>The National Key Research and Development Program of China</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>20</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Environ Microbiol</MedlineTA><NlmUniqueID>100883692</NlmUniqueID><ISSNLinking>1462-2912</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>12</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>06</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>6</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>6</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>6</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32564502</ArticleId><ArticleId IdType="doi">10.1111/1462-2920.15136</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Beck, T., and Hall, M.N. 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