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Prediction and Characterization of RXLR Effectors in Pythium Species.

Identifieur interne : 000082 ( Main/Exploration ); précédent : 000081; suivant : 000083

Prediction and Characterization of RXLR Effectors in Pythium Species.

Auteurs : Gan Ai [République populaire de Chine] ; Kun Yang [République populaire de Chine] ; Wenwu Ye [République populaire de Chine] ; Yuee Tian [République populaire de Chine] ; Yaxin Du [République populaire de Chine] ; Hai Zhu [République populaire de Chine] ; Tianli Li [République populaire de Chine] ; Qingyue Xia [République populaire de Chine] ; Danyu Shen [République populaire de Chine] ; Hao Peng [États-Unis] ; Maofeng Jing [République populaire de Chine] ; Ai Xia [République populaire de Chine] ; Daolong Dou [République populaire de Chine]

Source :

RBID : pubmed:32330072

Descripteurs français

English descriptors

Abstract

RXLR effectors, a class of secreted proteins that are transferred into host cells to manipulate host immunity, have been reported to widely exist in oomycetes, including those from genera Phytophthora, Hyaloperonospora, Albugo, and Saprolegnia. However, in Pythium species, no RXLR effector has yet been characterized, and the origin and evolution of such virulent effectors are still unknown. Here, we developed a modified regular expression method for de novo identification of RXLRs and characterized 359 putative RXLR effectors in nine Pythium species. Phylogenetic analysis revealed that all oomycetous RXLRs formed a single superfamily, suggesting that they might have a common ancestor. RXLR effectors from Pythium and Phytophthora species exhibited similar sequence features, protein structures, and genome locations. In particular, there were significantly more RXLR proteins in the mosquito biological control agent P. guiyangense than in the other eight Pythium species, and P. guiyangense RXLRs might be the result of gene duplication and genome rearrangement events, as indicated by synteny analysis. Expression pattern analysis of RXLR-encoding genes in the plant pathogen P. ultimum detected transcripts of the majority of the predicted RXLR genes, with some RXLR effectors induced in infection stages and one RXLR showing necrosis-inducing activity. Furthermore, all predicted RXLR genes were cloned from two biocontrol agents, P. oligandrum and P. periplocum, and three of the RXLR genes were found to induce a defense response in Nicotiana benthamiana. Taken together, our findings represent the first evidence of RXLR effectors in Pythium species, providing valuable information on their evolutionary patterns and the mechanisms of their interactions with diverse hosts.

DOI: 10.1094/MPMI-01-20-0010-R
PubMed: 32330072


Affiliations:


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Le document en format XML

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<term>Phytophthora (MeSH)</term>
<term>Pythium (genetics)</term>
<term>Pythium (pathogenicity)</term>
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<term>Famille multigénique (MeSH)</term>
<term>Génome (MeSH)</term>
<term>Phylogenèse (MeSH)</term>
<term>Phytophthora (MeSH)</term>
<term>Pythium (génétique)</term>
<term>Pythium (pathogénicité)</term>
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<div type="abstract" xml:lang="en">RXLR effectors, a class of secreted proteins that are transferred into host cells to manipulate host immunity, have been reported to widely exist in oomycetes, including those from genera
<i>Phytophthora</i>
,
<i>Hyaloperonospora</i>
,
<i>Albugo</i>
, and
<i>Saprolegnia</i>
. However, in
<i>Pythium</i>
species, no RXLR effector has yet been characterized, and the origin and evolution of such virulent effectors are still unknown. Here, we developed a modified regular expression method for de novo identification of RXLRs and characterized 359 putative RXLR effectors in nine
<i>Pythium</i>
species. Phylogenetic analysis revealed that all oomycetous RXLRs formed a single superfamily, suggesting that they might have a common ancestor. RXLR effectors from
<i>Pythium</i>
and
<i>Phytophthora</i>
species exhibited similar sequence features, protein structures, and genome locations. In particular, there were significantly more RXLR proteins in the mosquito biological control agent
<i>P. guiyangense</i>
than in the other eight
<i>Pythium</i>
species, and
<i>P. guiyangense</i>
RXLRs might be the result of gene duplication and genome rearrangement events, as indicated by synteny analysis. Expression pattern analysis of RXLR-encoding genes in the plant pathogen
<i>P. ultimum</i>
detected transcripts of the majority of the predicted
<i>RXLR</i>
genes, with some RXLR effectors induced in infection stages and one RXLR showing necrosis-inducing activity. Furthermore, all predicted
<i>RXLR</i>
genes were cloned from two biocontrol agents,
<i>P. oligandrum</i>
and
<i>P. periplocum</i>
, and three of the
<i>RXLR</i>
genes were found to induce a defense response in
<i>Nicotiana benthamiana</i>
. Taken together, our findings represent the first evidence of RXLR effectors in
<i>Pythium</i>
species, providing valuable information on their evolutionary patterns and the mechanisms of their interactions with diverse hosts.</div>
</front>
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<Day>12</Day>
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<Title>Molecular plant-microbe interactions : MPMI</Title>
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<ArticleTitle>Prediction and Characterization of RXLR Effectors in
<i>Pythium</i>
Species.</ArticleTitle>
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<Abstract>
<AbstractText>RXLR effectors, a class of secreted proteins that are transferred into host cells to manipulate host immunity, have been reported to widely exist in oomycetes, including those from genera
<i>Phytophthora</i>
,
<i>Hyaloperonospora</i>
,
<i>Albugo</i>
, and
<i>Saprolegnia</i>
. However, in
<i>Pythium</i>
species, no RXLR effector has yet been characterized, and the origin and evolution of such virulent effectors are still unknown. Here, we developed a modified regular expression method for de novo identification of RXLRs and characterized 359 putative RXLR effectors in nine
<i>Pythium</i>
species. Phylogenetic analysis revealed that all oomycetous RXLRs formed a single superfamily, suggesting that they might have a common ancestor. RXLR effectors from
<i>Pythium</i>
and
<i>Phytophthora</i>
species exhibited similar sequence features, protein structures, and genome locations. In particular, there were significantly more RXLR proteins in the mosquito biological control agent
<i>P. guiyangense</i>
than in the other eight
<i>Pythium</i>
species, and
<i>P. guiyangense</i>
RXLRs might be the result of gene duplication and genome rearrangement events, as indicated by synteny analysis. Expression pattern analysis of RXLR-encoding genes in the plant pathogen
<i>P. ultimum</i>
detected transcripts of the majority of the predicted
<i>RXLR</i>
genes, with some RXLR effectors induced in infection stages and one RXLR showing necrosis-inducing activity. Furthermore, all predicted
<i>RXLR</i>
genes were cloned from two biocontrol agents,
<i>P. oligandrum</i>
and
<i>P. periplocum</i>
, and three of the
<i>RXLR</i>
genes were found to induce a defense response in
<i>Nicotiana benthamiana</i>
. Taken together, our findings represent the first evidence of RXLR effectors in
<i>Pythium</i>
species, providing valuable information on their evolutionary patterns and the mechanisms of their interactions with diverse hosts.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Ai</LastName>
<ForeName>Gan</ForeName>
<Initials>G</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-2094-5461</Identifier>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yang</LastName>
<ForeName>Kun</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ye</LastName>
<ForeName>Wenwu</ForeName>
<Initials>W</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tian</LastName>
<ForeName>Yuee</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Plant Protection, Henan University of Science and Technology, Luoyang 471000, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Du</LastName>
<ForeName>Yaxin</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhu</LastName>
<ForeName>Hai</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Tianli</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xia</LastName>
<ForeName>Qingyue</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Shen</LastName>
<ForeName>Danyu</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Peng</LastName>
<ForeName>Hao</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-1915-6104</Identifier>
<AffiliationInfo>
<Affiliation>Department of Crop and Soil Sciences, Washington State University, Pullman, WA, U.S.A.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jing</LastName>
<ForeName>Maofeng</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xia</LastName>
<ForeName>Ai</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dou</LastName>
<ForeName>Daolong</ForeName>
<Initials>D</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-5226-6642</Identifier>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>06</Month>
<Day>22</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Mol Plant Microbe Interact</MedlineTA>
<NlmUniqueID>9107902</NlmUniqueID>
<ISSNLinking>0894-0282</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D016678" MajorTopicYN="N">Genome</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005810" MajorTopicYN="Y">Multigene Family</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011775" MajorTopicYN="N">Pythium</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D026801" MajorTopicYN="N">Synteny</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Pythium</Keyword>
<Keyword MajorTopicYN="N">RXLR effector</Keyword>
<Keyword MajorTopicYN="N">gene evolution</Keyword>
<Keyword MajorTopicYN="N">oomycete</Keyword>
<Keyword MajorTopicYN="N">pathogenicity</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="pubmed">
<Year>2020</Year>
<Month>4</Month>
<Day>25</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2020</Year>
<Month>11</Month>
<Day>13</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2020</Year>
<Month>4</Month>
<Day>25</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">32330072</ArticleId>
<ArticleId IdType="doi">10.1094/MPMI-01-20-0010-R</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region>
<li>Washington (État)</li>
</region>
</list>
<tree>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Ai, Gan" sort="Ai, Gan" uniqKey="Ai G" first="Gan" last="Ai">Gan Ai</name>
</noRegion>
<name sortKey="Dou, Daolong" sort="Dou, Daolong" uniqKey="Dou D" first="Daolong" last="Dou">Daolong Dou</name>
<name sortKey="Du, Yaxin" sort="Du, Yaxin" uniqKey="Du Y" first="Yaxin" last="Du">Yaxin Du</name>
<name sortKey="Jing, Maofeng" sort="Jing, Maofeng" uniqKey="Jing M" first="Maofeng" last="Jing">Maofeng Jing</name>
<name sortKey="Li, Tianli" sort="Li, Tianli" uniqKey="Li T" first="Tianli" last="Li">Tianli Li</name>
<name sortKey="Shen, Danyu" sort="Shen, Danyu" uniqKey="Shen D" first="Danyu" last="Shen">Danyu Shen</name>
<name sortKey="Tian, Yuee" sort="Tian, Yuee" uniqKey="Tian Y" first="Yuee" last="Tian">Yuee Tian</name>
<name sortKey="Tian, Yuee" sort="Tian, Yuee" uniqKey="Tian Y" first="Yuee" last="Tian">Yuee Tian</name>
<name sortKey="Xia, Ai" sort="Xia, Ai" uniqKey="Xia A" first="Ai" last="Xia">Ai Xia</name>
<name sortKey="Xia, Qingyue" sort="Xia, Qingyue" uniqKey="Xia Q" first="Qingyue" last="Xia">Qingyue Xia</name>
<name sortKey="Yang, Kun" sort="Yang, Kun" uniqKey="Yang K" first="Kun" last="Yang">Kun Yang</name>
<name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</name>
<name sortKey="Zhu, Hai" sort="Zhu, Hai" uniqKey="Zhu H" first="Hai" last="Zhu">Hai Zhu</name>
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<region name="Washington (État)">
<name sortKey="Peng, Hao" sort="Peng, Hao" uniqKey="Peng H" first="Hao" last="Peng">Hao Peng</name>
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