Genome-wide analysis of NDR1/HIN1-like genes in pepper (Capsicum annuum L.) and functional characterization of CaNHL4 under biotic and abiotic stresses.
Identifieur interne : 000172 ( Main/Corpus ); précédent : 000171; suivant : 000173Genome-wide analysis of NDR1/HIN1-like genes in pepper (Capsicum annuum L.) and functional characterization of CaNHL4 under biotic and abiotic stresses.
Auteurs : Changyun Liu ; Haoren Peang ; Xinyu Li ; Chaolong Liu ; Xing Lv ; Xuefeng Wei ; Aihong Zou ; Jian Zhang ; Guangjin Fan ; Guanhua Ma ; Lisong Ma ; Xianchao SunSource :
- Horticulture research [ 2052-7276 ] ; 2020.
Abstract
Plant NDR1/HIN1-like (NHL) genes play an important role in triggering plant defenses in response to biotic stresses. In this study, we performed a genome-wide identification of the NHL genes in pepper (Capsicum annuum L.) and characterized the functional roles of these CaNHL genes in response to abiotic stresses and infection by different pathogens. Phylogenetic analysis revealed that CaNHLs can be classified into five distinct subgroups, with each group containing generic and specific motifs. Regulatory element analysis showed that the majority of the promoter regions of the identified CaNHLs contain jasmonic acid (JA)-responsive and salicylic acid (SA)-responsive elements, and transcriptomic analysis revealed that CaNHL genes are expressed in all the examined tissues of pepper. The CaNHL1, CaNHL4, CaNHL6, CaNHL10, CaNHL11, and CaNHL12 genes were significantly upregulated under abiotic stress as well as in response to different pathogens, such as TMV, Phytophthora capsici and Pseudomonas syringae. In addition, we found that CaNHL4 localizes to the plasma membrane. CaNHL4-silenced pepper plants display significantly increased susceptibility to TMV, Phytophthora capsici and Pseudomonas syringae, exhibiting reduced expression of JA-related and SA-related genes and reduced ROS production. However, transient overexpression of CaNHL4 in pepper increases the expression of JA-related and SA-related genes, enhances the accumulation of ROS, and inhibits the infection of these three pathogens. Collectively, for the first time, we identified the NHL genes in pepper and demonstrated that CaNHL4 is involved in the production of ROS and that it also regulates the expression of JA-related and SA-related genes in response to different pathogens, suggesting that members of the CaNHL family play an essential role in the disease resistance of pepper.
DOI: 10.1038/s41438-020-0318-0
PubMed: 32528705
PubMed Central: PMC7261774
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Genome-wide analysis of NDR1/HIN1-like genes in pepper (<i>Capsicum annuum</i> L.) and functional characterization of <i>CaNHL4</i> under biotic and abiotic stresses.</title><author><name sortKey="Liu, Changyun" sort="Liu, Changyun" uniqKey="Liu C" first="Changyun" last="Liu">Changyun Liu</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Peang, Haoren" sort="Peang, Haoren" uniqKey="Peang H" first="Haoren" last="Peang">Haoren Peang</name><affiliation><nlm:affiliation>Department of Botany and Plant Biology, Section of Biology, Faculty of Science, University of Geneva, 1211 Geneva 4, Switzerland.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Xinyu" sort="Li, Xinyu" uniqKey="Li X" first="Xinyu" last="Li">Xinyu Li</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Chaolong" sort="Liu, Chaolong" uniqKey="Liu C" first="Chaolong" last="Liu">Chaolong Liu</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Lv, Xing" sort="Lv, Xing" uniqKey="Lv X" first="Xing" last="Lv">Xing Lv</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Wei, Xuefeng" sort="Wei, Xuefeng" uniqKey="Wei X" first="Xuefeng" last="Wei">Xuefeng Wei</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zou, Aihong" sort="Zou, Aihong" uniqKey="Zou A" first="Aihong" last="Zou">Aihong Zou</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zhang, Jian" sort="Zhang, Jian" uniqKey="Zhang J" first="Jian" last="Zhang">Jian Zhang</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Fan, Guangjin" sort="Fan, Guangjin" uniqKey="Fan G" first="Guangjin" last="Fan">Guangjin Fan</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Guanhua" sort="Ma, Guanhua" uniqKey="Ma G" first="Guanhua" last="Ma">Guanhua Ma</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Lisong" sort="Ma, Lisong" uniqKey="Ma L" first="Lisong" last="Ma">Lisong Ma</name><affiliation><nlm:affiliation>State Key Laboratory of North China Crop Improvement and Regulation, College of Plant Protection, Hebei Agricultural University, 071001 Baoding, China.</nlm:affiliation></affiliation></author><author><name sortKey="Sun, Xianchao" sort="Sun, Xianchao" uniqKey="Sun X" first="Xianchao" last="Sun">Xianchao Sun</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32528705</idno><idno type="pmid">32528705</idno><idno type="doi">10.1038/s41438-020-0318-0</idno><idno type="pmc">PMC7261774</idno><idno type="wicri:Area/Main/Corpus">000172</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000172</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Genome-wide analysis of NDR1/HIN1-like genes in pepper (<i>Capsicum annuum</i> L.) and functional characterization of <i>CaNHL4</i> under biotic and abiotic stresses.</title><author><name sortKey="Liu, Changyun" sort="Liu, Changyun" uniqKey="Liu C" first="Changyun" last="Liu">Changyun Liu</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Peang, Haoren" sort="Peang, Haoren" uniqKey="Peang H" first="Haoren" last="Peang">Haoren Peang</name><affiliation><nlm:affiliation>Department of Botany and Plant Biology, Section of Biology, Faculty of Science, University of Geneva, 1211 Geneva 4, Switzerland.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Xinyu" sort="Li, Xinyu" uniqKey="Li X" first="Xinyu" last="Li">Xinyu Li</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Chaolong" sort="Liu, Chaolong" uniqKey="Liu C" first="Chaolong" last="Liu">Chaolong Liu</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Lv, Xing" sort="Lv, Xing" uniqKey="Lv X" first="Xing" last="Lv">Xing Lv</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Wei, Xuefeng" sort="Wei, Xuefeng" uniqKey="Wei X" first="Xuefeng" last="Wei">Xuefeng Wei</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zou, Aihong" sort="Zou, Aihong" uniqKey="Zou A" first="Aihong" last="Zou">Aihong Zou</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zhang, Jian" sort="Zhang, Jian" uniqKey="Zhang J" first="Jian" last="Zhang">Jian Zhang</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Fan, Guangjin" sort="Fan, Guangjin" uniqKey="Fan G" first="Guangjin" last="Fan">Guangjin Fan</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Guanhua" sort="Ma, Guanhua" uniqKey="Ma G" first="Guanhua" last="Ma">Guanhua Ma</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Lisong" sort="Ma, Lisong" uniqKey="Ma L" first="Lisong" last="Ma">Lisong Ma</name><affiliation><nlm:affiliation>State Key Laboratory of North China Crop Improvement and Regulation, College of Plant Protection, Hebei Agricultural University, 071001 Baoding, China.</nlm:affiliation></affiliation></author><author><name sortKey="Sun, Xianchao" sort="Sun, Xianchao" uniqKey="Sun X" first="Xianchao" last="Sun">Xianchao Sun</name><affiliation><nlm:affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Horticulture research</title><idno type="ISSN">2052-7276</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">Plant NDR1/HIN1-like (<i>NHL</i>) genes play an important role in triggering plant defenses in response to biotic stresses. In this study, we performed a genome-wide identification of the <i>NHL</i> genes in pepper (<i>Capsicum annuum</i> L.) and characterized the functional roles of these <i>CaNHL</i> genes in response to abiotic stresses and infection by different pathogens. Phylogenetic analysis revealed that <i>CaNHL</i>s can be classified into five distinct subgroups, with each group containing generic and specific motifs. Regulatory element analysis showed that the majority of the promoter regions of the identified <i>CaNHL</i>s contain jasmonic acid (JA)-responsive and salicylic acid (SA)-responsive elements, and transcriptomic analysis revealed that <i>CaNHL</i> genes are expressed in all the examined tissues of pepper. The <i>CaNHL1</i>, <i>CaNHL4</i>, <i>CaNHL6</i>, <i>CaNHL10</i>, <i>CaNHL11</i>, and <i>CaNHL12</i> genes were significantly upregulated under abiotic stress as well as in response to different pathogens, such as TMV, <i>Phytophthora capsici</i> and <i>Pseudomonas syringae</i>. In addition, we found that CaNHL4 localizes to the plasma membrane. <i>CaNHL4</i>-silenced pepper plants display significantly increased susceptibility to TMV, <i>Phytophthora capsici</i> and <i>Pseudomonas syringae</i>, exhibiting reduced expression of JA-related and SA-related genes and reduced ROS production. However, transient overexpression of <i>CaNHL4</i> in pepper increases the expression of JA-related and SA-related genes, enhances the accumulation of ROS, and inhibits the infection of these three pathogens. Collectively, for the first time, we identified the <i>NHL</i> genes in pepper and demonstrated that <i>CaNHL4</i> is involved in the production of ROS and that it also regulates the expression of JA-related and SA-related genes in response to different pathogens, suggesting that members of the CaNHL family play an essential role in the disease resistance of pepper.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32528705</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2052-7276</ISSN><JournalIssue CitedMedium="Print"><Volume>7</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Horticulture research</Title><ISOAbbreviation>Hortic Res</ISOAbbreviation></Journal><ArticleTitle>Genome-wide analysis of NDR1/HIN1-like genes in pepper (<i>Capsicum annuum</i> L.) and functional characterization of <i>CaNHL4</i> under biotic and abiotic stresses.</ArticleTitle><Pagination><MedlinePgn>93</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41438-020-0318-0</ELocationID><Abstract><AbstractText>Plant NDR1/HIN1-like (<i>NHL</i>) genes play an important role in triggering plant defenses in response to biotic stresses. In this study, we performed a genome-wide identification of the <i>NHL</i> genes in pepper (<i>Capsicum annuum</i> L.) and characterized the functional roles of these <i>CaNHL</i> genes in response to abiotic stresses and infection by different pathogens. Phylogenetic analysis revealed that <i>CaNHL</i>s can be classified into five distinct subgroups, with each group containing generic and specific motifs. Regulatory element analysis showed that the majority of the promoter regions of the identified <i>CaNHL</i>s contain jasmonic acid (JA)-responsive and salicylic acid (SA)-responsive elements, and transcriptomic analysis revealed that <i>CaNHL</i> genes are expressed in all the examined tissues of pepper. The <i>CaNHL1</i>, <i>CaNHL4</i>, <i>CaNHL6</i>, <i>CaNHL10</i>, <i>CaNHL11</i>, and <i>CaNHL12</i> genes were significantly upregulated under abiotic stress as well as in response to different pathogens, such as TMV, <i>Phytophthora capsici</i> and <i>Pseudomonas syringae</i>. In addition, we found that CaNHL4 localizes to the plasma membrane. <i>CaNHL4</i>-silenced pepper plants display significantly increased susceptibility to TMV, <i>Phytophthora capsici</i> and <i>Pseudomonas syringae</i>, exhibiting reduced expression of JA-related and SA-related genes and reduced ROS production. However, transient overexpression of <i>CaNHL4</i> in pepper increases the expression of JA-related and SA-related genes, enhances the accumulation of ROS, and inhibits the infection of these three pathogens. Collectively, for the first time, we identified the <i>NHL</i> genes in pepper and demonstrated that <i>CaNHL4</i> is involved in the production of ROS and that it also regulates the expression of JA-related and SA-related genes in response to different pathogens, suggesting that members of the CaNHL family play an essential role in the disease resistance of pepper.</AbstractText><CopyrightInformation>© The Author(s) 2020.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Changyun</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0003-1683-5101</Identifier><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Peang</LastName><ForeName>Haoren</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Botany and Plant Biology, Section of Biology, Faculty of Science, University of Geneva, 1211 Geneva 4, Switzerland.</Affiliation><Identifier Source="ISNI">0000 0001 2322 4988</Identifier><Identifier Source="GRID">grid.8591.5</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Xinyu</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Chaolong</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lv</LastName><ForeName>Xing</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Xuefeng</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zou</LastName><ForeName>Aihong</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Jian</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fan</LastName><ForeName>Guangjin</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Guanhua</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Lisong</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>State Key Laboratory of North China Crop Improvement and Regulation, College of Plant Protection, Hebei Agricultural University, 071001 Baoding, China.</Affiliation><Identifier Source="ISNI">0000 0001 2291 4530</Identifier><Identifier Source="GRID">grid.274504.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Xianchao</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Laboratory of plant immunity and ecological control of plant disease, College of Plant Protection, Southwest University, 400716 Chongqing, China.</Affiliation><Identifier Source="GRID">grid.263906.8</Identifier></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>01</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Hortic Res</MedlineTA><NlmUniqueID>101655540</NlmUniqueID><ISSNLinking>2052-7276</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Biotic</Keyword><Keyword MajorTopicYN="N">Plant immunity</Keyword></KeywordList><CoiStatement>Conflict of interestThe authors declare that they have no conflict of interest.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>12</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>03</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>04</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>6</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>6</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>6</Month><Day>13</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32528705</ArticleId><ArticleId IdType="doi">10.1038/s41438-020-0318-0</ArticleId><ArticleId IdType="pii">318</ArticleId><ArticleId IdType="pmc">PMC7261774</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Nat Chem Biol. 2009 May;5(5):308-16</Citation><ArticleIdList><ArticleId 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