miR319a/TCP module and DELLA protein regulate trichome initiation synergistically and improve insect defenses in Populus tomentosa.
Identifieur interne : 000003 ( Main/Exploration ); précédent : 000002; suivant : 000004miR319a/TCP module and DELLA protein regulate trichome initiation synergistically and improve insect defenses in Populus tomentosa.
Auteurs : Di Fan [République populaire de Chine] ; Lingyu Ran [République populaire de Chine] ; Jian Hu [République populaire de Chine] ; Xiao Ye [République populaire de Chine] ; Dan Xu [République populaire de Chine] ; Jianqiu Li [République populaire de Chine] ; Huili Su [République populaire de Chine] ; Xianqiang Wang [République populaire de Chine] ; Sha Ren [République populaire de Chine] ; Keming Luo [République populaire de Chine]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
Trichomes are specialized epidermal cells that contribute to plant resistance against herbivores. Their formation is controlled precisely by multiple genetic and environmental signals. Previous studies have shown that microRNA319 (miR319) and gibberellin (GA) signaling are involved in trichome development in Arabidopsis, but little is known about their interaction between these factors. Here we reported that the miR319a/TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) module participates in trichome initiation synergistically with GA signaling in Populus tomentosa. We demonstrated that overexpression of miR319a decreased transcription levels of its targeted TCPs and significantly elevated leaf trichome density in transgenic poplar, resulting in decreasing insect herbivory. Conversely, repressing miR319a by short tandem target mimics (STTM) elevated TCP expression levels and decreased trichome density in transgenic plants. The trichome phenotype of 35S:miR319a plants could be abolished by introducing a miR319a-resistant form of TCP19. Furthermore, the miR319a-targeted TCP19 interacted directly with REPRESSOR OF ga1-3 (RGA), a downstream repressor of GA signaling. TCP19 and RGA synergistically inhibited the GLABROUS1 (GL1)-induced expression of trichome marker gene GLABRA2 (GL2), thereby repressing leaf trichome initiation. Our results provide an insight into the molecular mechanism by which miR319/TCP19 module and GA signaling coordinated regulating trichome initiation in P. tomentosa.
DOI: 10.1111/nph.16585
PubMed: 32270484
Affiliations:
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School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Xianqiang" sort="Wang, Xianqiang" uniqKey="Wang X" first="Xianqiang" last="Wang">Xianqiang Wang</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Ren, Sha" sort="Ren, Sha" uniqKey="Ren S" first="Sha" last="Ren">Sha Ren</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Luo, Keming" sort="Luo, Keming" uniqKey="Luo K" 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wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Ran, Lingyu" sort="Ran, Lingyu" uniqKey="Ran L" first="Lingyu" last="Ran">Lingyu Ran</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Hu, Jian" sort="Hu, Jian" uniqKey="Hu J" first="Jian" last="Hu">Jian Hu</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Ye, Xiao" sort="Ye, Xiao" uniqKey="Ye X" first="Xiao" last="Ye">Xiao Ye</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Xu, Dan" sort="Xu, Dan" uniqKey="Xu D" first="Dan" last="Xu">Dan Xu</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Li, Jianqiu" sort="Li, Jianqiu" uniqKey="Li J" first="Jianqiu" last="Li">Jianqiu Li</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Su, Huili" sort="Su, Huili" uniqKey="Su H" first="Huili" last="Su">Huili Su</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Xianqiang" sort="Wang, Xianqiang" uniqKey="Wang X" first="Xianqiang" last="Wang">Xianqiang Wang</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Ren, Sha" sort="Ren, Sha" uniqKey="Ren S" first="Sha" last="Ren">Sha Ren</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author><author><name sortKey="Luo, Keming" sort="Luo, Keming" uniqKey="Luo K" first="Keming" last="Luo">Keming Luo</name><affiliation wicri:level="1"><nlm:affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715</wicri:regionArea><wicri:noRegion>400715</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</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">Trichomes are specialized epidermal cells that contribute to plant resistance against herbivores. Their formation is controlled precisely by multiple genetic and environmental signals. Previous studies have shown that microRNA319 (miR319) and gibberellin (GA) signaling are involved in trichome development in Arabidopsis, but little is known about their interaction between these factors. Here we reported that the miR319a/TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) module participates in trichome initiation synergistically with GA signaling in Populus tomentosa. We demonstrated that overexpression of miR319a decreased transcription levels of its targeted TCPs and significantly elevated leaf trichome density in transgenic poplar, resulting in decreasing insect herbivory. Conversely, repressing miR319a by short tandem target mimics (STTM) elevated TCP expression levels and decreased trichome density in transgenic plants. The trichome phenotype of 35S:miR319a plants could be abolished by introducing a miR319a-resistant form of TCP19. Furthermore, the miR319a-targeted TCP19 interacted directly with REPRESSOR OF ga1-3 (RGA), a downstream repressor of GA signaling. TCP19 and RGA synergistically inhibited the GLABROUS1 (GL1)-induced expression of trichome marker gene GLABRA2 (GL2), thereby repressing leaf trichome initiation. Our results provide an insight into the molecular mechanism by which miR319/TCP19 module and GA signaling coordinated regulating trichome initiation in P. tomentosa.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32270484</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>23</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><Volume>227</Volume><Issue>3</Issue><PubDate><Year>2020</Year><Month>08</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>miR319a/TCP module and DELLA protein regulate trichome initiation synergistically and improve insect defenses in Populus tomentosa.</ArticleTitle><Pagination><MedlinePgn>867-883</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16585</ELocationID><Abstract><AbstractText>Trichomes are specialized epidermal cells that contribute to plant resistance against herbivores. Their formation is controlled precisely by multiple genetic and environmental signals. Previous studies have shown that microRNA319 (miR319) and gibberellin (GA) signaling are involved in trichome development in Arabidopsis, but little is known about their interaction between these factors. Here we reported that the miR319a/TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) module participates in trichome initiation synergistically with GA signaling in Populus tomentosa. We demonstrated that overexpression of miR319a decreased transcription levels of its targeted TCPs and significantly elevated leaf trichome density in transgenic poplar, resulting in decreasing insect herbivory. Conversely, repressing miR319a by short tandem target mimics (STTM) elevated TCP expression levels and decreased trichome density in transgenic plants. The trichome phenotype of 35S:miR319a plants could be abolished by introducing a miR319a-resistant form of TCP19. Furthermore, the miR319a-targeted TCP19 interacted directly with REPRESSOR OF ga1-3 (RGA), a downstream repressor of GA signaling. TCP19 and RGA synergistically inhibited the GLABROUS1 (GL1)-induced expression of trichome marker gene GLABRA2 (GL2), thereby repressing leaf trichome initiation. Our results provide an insight into the molecular mechanism by which miR319/TCP19 module and GA signaling coordinated regulating trichome initiation in P. tomentosa.</AbstractText><CopyrightInformation>© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Fan</LastName><ForeName>Di</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ran</LastName><ForeName>Lingyu</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hu</LastName><ForeName>Jian</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ye</LastName><ForeName>Xiao</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Dan</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Jianqiu</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Su</LastName><ForeName>Huili</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Xianqiang</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ren</LastName><ForeName>Sha</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Luo</LastName><ForeName>Keming</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0003-4928-7578</Identifier><AffiliationInfo><Affiliation>Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Southwest University, Chongqing, 400715, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>05</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Populus tomentosa
</Keyword><Keyword MajorTopicYN="Y">RGA</Keyword><Keyword MajorTopicYN="Y">TCP</Keyword><Keyword MajorTopicYN="Y">gibberellin</Keyword><Keyword MajorTopicYN="Y">miR319a</Keyword><Keyword MajorTopicYN="Y">trichome</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>02</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>4</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>4</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>4</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32270484</ArticleId><ArticleId IdType="doi">10.1111/nph.16585</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>An L, Zhou Z, Su S, Yan A, Gan Y. 2012. 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