Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway
High temperature (HT) is becoming an increasingly serious factor in limiting crop production with global climate change. During hot seasons, owing to prevailing HT, cultivated tomatoes are prone to exhibiting stigma exsertion, which hampers pollination and causes fruit set failure. However, the unde...
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description | High temperature (HT) is becoming an increasingly serious factor in limiting crop production with global climate change. During hot seasons, owing to prevailing HT, cultivated tomatoes are prone to exhibiting stigma exsertion, which hampers pollination and causes fruit set failure. However, the underlying regulatory mechanisms of the HT‐induced stigma exsertion remain largely unknown. Here, we demonstrate that stigma exsertion induced by HT in cultivated tomato is caused by more seriously shortened stamens than pistils, which is different from the stigma exsertion observed in wild tomato species. Under the HT condition, the different responses of pectin, sugar, expansin, and cyclin cause cell wall remodelling and differentially localized cell division and selective cell enlargement, which further determine the lengths of stamens and pistils. In addition, auxin and jasmonate (JA) are implicated in regulating cell division and cell expansion in stamens and pistils, and exogenous JA instead of auxin treatment can effectively rescue tomato stigma exsertion through regulating the JA/COI1 signalling pathway. Our findings provide a better understanding of stigma exsertions under the HT condition in tomato and uncover a new function of JA in improving plant abiotic stress tolerance.
Stigma exsertion is commonly observed in cultivated tomatoes under elevated temperature conditions, which severely hampers pollination and fruit set. We demonstrate that high temperature (HT)‐induced stigma exsertion in cultivated tomato is caused by more shortened stamens than pistils. The difference of stamen and pistil length changes under HT is attributed to the different responses of pectin, sugar, expansin, and cyclin, which causes cell wall remodelling and differentially localized cell division and selective cell enlargement under the HT condition. The JA/COI1 signalling pathway participates in regulating HT‐induced stigma exsertion. |
doi_str_mv | 10.1111/pce.13444 |
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Stigma exsertion is commonly observed in cultivated tomatoes under elevated temperature conditions, which severely hampers pollination and fruit set. We demonstrate that high temperature (HT)‐induced stigma exsertion in cultivated tomato is caused by more shortened stamens than pistils. The difference of stamen and pistil length changes under HT is attributed to the different responses of pectin, sugar, expansin, and cyclin, which causes cell wall remodelling and differentially localized cell division and selective cell enlargement under the HT condition. The JA/COI1 signalling pathway participates in regulating HT‐induced stigma exsertion.</description><identifier>ISSN: 0140-7791</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.13444</identifier><identifier>PMID: 30203844</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>auxin ; Cell division ; Cell walls ; Climate change ; Crop production ; Cultivation ; cyclin ; Cyclopentanes - metabolism ; Enlargement ; expansin ; Flowers - growth & development ; Flowers - physiology ; Fructose - metabolism ; Fruit cultivation ; Fruit set ; Global climate ; Glucose - metabolism ; heat stress ; High temperature ; Hot Temperature ; Indoleacetic Acids - metabolism ; Jasmonic acid ; Lycopersicon esculentum - growth & development ; Lycopersicon esculentum - metabolism ; Lycopersicon esculentum - physiology ; Oxylipins - metabolism ; Pectin ; Pectins - metabolism ; pistil ; Pistils ; Plant Growth Regulators - metabolism ; Pollination ; Real-Time Polymerase Chain Reaction ; Regulatory mechanisms (biology) ; Self-Fertilization ; Signal Transduction ; Signaling ; stamen ; Stamens ; Stigmas (botany) ; Sucrose - metabolism ; Sugar ; Tomatoes</subject><ispartof>Plant, cell and environment, 2019-04, Vol.42 (4), p.1205-1221</ispartof><rights>2018 John Wiley & Sons Ltd</rights><rights>2018 John Wiley & Sons Ltd.</rights><rights>2019 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3884-288c27cdca663f53ad6b524ba6b072732056652c0eda95dc48e9b5347d3c3eaf3</citedby><cites>FETCH-LOGICAL-c3884-288c27cdca663f53ad6b524ba6b072732056652c0eda95dc48e9b5347d3c3eaf3</cites><orcidid>0000-0002-0116-7561</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpce.13444$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpce.13444$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30203844$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pan, Changtian</creatorcontrib><creatorcontrib>Yang, Dandan</creatorcontrib><creatorcontrib>Zhao, Xiaolin</creatorcontrib><creatorcontrib>Jiao, Chen</creatorcontrib><creatorcontrib>Yan, Yanqiu</creatorcontrib><creatorcontrib>Lamin‐Samu, Anthony Tumbeh</creatorcontrib><creatorcontrib>Wang, Qiaomei</creatorcontrib><creatorcontrib>Xu, Xiangyang</creatorcontrib><creatorcontrib>Fei, Zhangjun</creatorcontrib><creatorcontrib>Lu, Gang</creatorcontrib><title>Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>High temperature (HT) is becoming an increasingly serious factor in limiting crop production with global climate change. During hot seasons, owing to prevailing HT, cultivated tomatoes are prone to exhibiting stigma exsertion, which hampers pollination and causes fruit set failure. However, the underlying regulatory mechanisms of the HT‐induced stigma exsertion remain largely unknown. Here, we demonstrate that stigma exsertion induced by HT in cultivated tomato is caused by more seriously shortened stamens than pistils, which is different from the stigma exsertion observed in wild tomato species. Under the HT condition, the different responses of pectin, sugar, expansin, and cyclin cause cell wall remodelling and differentially localized cell division and selective cell enlargement, which further determine the lengths of stamens and pistils. In addition, auxin and jasmonate (JA) are implicated in regulating cell division and cell expansion in stamens and pistils, and exogenous JA instead of auxin treatment can effectively rescue tomato stigma exsertion through regulating the JA/COI1 signalling pathway. Our findings provide a better understanding of stigma exsertions under the HT condition in tomato and uncover a new function of JA in improving plant abiotic stress tolerance.
Stigma exsertion is commonly observed in cultivated tomatoes under elevated temperature conditions, which severely hampers pollination and fruit set. We demonstrate that high temperature (HT)‐induced stigma exsertion in cultivated tomato is caused by more shortened stamens than pistils. The difference of stamen and pistil length changes under HT is attributed to the different responses of pectin, sugar, expansin, and cyclin, which causes cell wall remodelling and differentially localized cell division and selective cell enlargement under the HT condition. The JA/COI1 signalling pathway participates in regulating HT‐induced stigma exsertion.</description><subject>auxin</subject><subject>Cell division</subject><subject>Cell walls</subject><subject>Climate change</subject><subject>Crop production</subject><subject>Cultivation</subject><subject>cyclin</subject><subject>Cyclopentanes - metabolism</subject><subject>Enlargement</subject><subject>expansin</subject><subject>Flowers - growth & development</subject><subject>Flowers - physiology</subject><subject>Fructose - metabolism</subject><subject>Fruit cultivation</subject><subject>Fruit set</subject><subject>Global climate</subject><subject>Glucose - metabolism</subject><subject>heat stress</subject><subject>High temperature</subject><subject>Hot Temperature</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Jasmonic acid</subject><subject>Lycopersicon esculentum - growth & development</subject><subject>Lycopersicon esculentum - metabolism</subject><subject>Lycopersicon esculentum - physiology</subject><subject>Oxylipins - metabolism</subject><subject>Pectin</subject><subject>Pectins - metabolism</subject><subject>pistil</subject><subject>Pistils</subject><subject>Plant Growth Regulators - metabolism</subject><subject>Pollination</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Regulatory mechanisms (biology)</subject><subject>Self-Fertilization</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>stamen</subject><subject>Stamens</subject><subject>Stigmas (botany)</subject><subject>Sucrose - metabolism</subject><subject>Sugar</subject><subject>Tomatoes</subject><issn>0140-7791</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kMtOwzAQRS0EoqWw4AeQJVYs0voVJ1miqjwkJFiUteU4TuKqeWA7Kvl7DCnsmM1Id46uRgeAa4yWOMyqV3qJKWPsBMwx5XFEEUOnYI4wQ1GSZHgGLpzbIRSCJDsHM4oIoiljc1Btu0b6DjpvqkZC_em09aZroWmLQekC5iOsTVVDr5teW-kHq6FxUDrXKSN9IA7Gh3Ot4U66pmtDBp2pWrnfm7aCvfT1QY6X4KyUe6evjnsB3h822_VT9PL6-Ly-f4kUTVMWkTRVJFGFkpzTMqay4HlMWC55jhKSUIJizmOikC5kFheKpTrLY8qSgiqqZUkX4Hbq7W33MWjnxa4bbHjGCYIzyhDiKQrU3UQp2zlndSl6axppR4GR-FYqglLxozSwN8fGIW908Uf-OgzAagIOZq_H_5vE23ozVX4B74SBMw</recordid><startdate>201904</startdate><enddate>201904</enddate><creator>Pan, Changtian</creator><creator>Yang, Dandan</creator><creator>Zhao, Xiaolin</creator><creator>Jiao, Chen</creator><creator>Yan, Yanqiu</creator><creator>Lamin‐Samu, Anthony Tumbeh</creator><creator>Wang, Qiaomei</creator><creator>Xu, Xiangyang</creator><creator>Fei, Zhangjun</creator><creator>Lu, Gang</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><orcidid>https://orcid.org/0000-0002-0116-7561</orcidid></search><sort><creationdate>201904</creationdate><title>Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway</title><author>Pan, Changtian ; Yang, Dandan ; Zhao, Xiaolin ; Jiao, Chen ; Yan, Yanqiu ; Lamin‐Samu, Anthony Tumbeh ; Wang, Qiaomei ; Xu, Xiangyang ; Fei, Zhangjun ; Lu, Gang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3884-288c27cdca663f53ad6b524ba6b072732056652c0eda95dc48e9b5347d3c3eaf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>auxin</topic><topic>Cell division</topic><topic>Cell walls</topic><topic>Climate change</topic><topic>Crop production</topic><topic>Cultivation</topic><topic>cyclin</topic><topic>Cyclopentanes - metabolism</topic><topic>Enlargement</topic><topic>expansin</topic><topic>Flowers - growth & development</topic><topic>Flowers - physiology</topic><topic>Fructose - metabolism</topic><topic>Fruit cultivation</topic><topic>Fruit set</topic><topic>Global climate</topic><topic>Glucose - metabolism</topic><topic>heat stress</topic><topic>High temperature</topic><topic>Hot Temperature</topic><topic>Indoleacetic Acids - metabolism</topic><topic>Jasmonic acid</topic><topic>Lycopersicon esculentum - growth & development</topic><topic>Lycopersicon esculentum - metabolism</topic><topic>Lycopersicon esculentum - physiology</topic><topic>Oxylipins - metabolism</topic><topic>Pectin</topic><topic>Pectins - metabolism</topic><topic>pistil</topic><topic>Pistils</topic><topic>Plant Growth Regulators - metabolism</topic><topic>Pollination</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>Regulatory mechanisms (biology)</topic><topic>Self-Fertilization</topic><topic>Signal Transduction</topic><topic>Signaling</topic><topic>stamen</topic><topic>Stamens</topic><topic>Stigmas (botany)</topic><topic>Sucrose - metabolism</topic><topic>Sugar</topic><topic>Tomatoes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pan, Changtian</creatorcontrib><creatorcontrib>Yang, Dandan</creatorcontrib><creatorcontrib>Zhao, Xiaolin</creatorcontrib><creatorcontrib>Jiao, Chen</creatorcontrib><creatorcontrib>Yan, Yanqiu</creatorcontrib><creatorcontrib>Lamin‐Samu, Anthony Tumbeh</creatorcontrib><creatorcontrib>Wang, Qiaomei</creatorcontrib><creatorcontrib>Xu, Xiangyang</creatorcontrib><creatorcontrib>Fei, Zhangjun</creatorcontrib><creatorcontrib>Lu, Gang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Environment Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Environment Abstracts</collection><jtitle>Plant, cell and environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pan, Changtian</au><au>Yang, Dandan</au><au>Zhao, Xiaolin</au><au>Jiao, Chen</au><au>Yan, Yanqiu</au><au>Lamin‐Samu, Anthony Tumbeh</au><au>Wang, Qiaomei</au><au>Xu, Xiangyang</au><au>Fei, Zhangjun</au><au>Lu, Gang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway</atitle><jtitle>Plant, cell and environment</jtitle><addtitle>Plant Cell Environ</addtitle><date>2019-04</date><risdate>2019</risdate><volume>42</volume><issue>4</issue><spage>1205</spage><epage>1221</epage><pages>1205-1221</pages><issn>0140-7791</issn><eissn>1365-3040</eissn><abstract>High temperature (HT) is becoming an increasingly serious factor in limiting crop production with global climate change. During hot seasons, owing to prevailing HT, cultivated tomatoes are prone to exhibiting stigma exsertion, which hampers pollination and causes fruit set failure. However, the underlying regulatory mechanisms of the HT‐induced stigma exsertion remain largely unknown. Here, we demonstrate that stigma exsertion induced by HT in cultivated tomato is caused by more seriously shortened stamens than pistils, which is different from the stigma exsertion observed in wild tomato species. Under the HT condition, the different responses of pectin, sugar, expansin, and cyclin cause cell wall remodelling and differentially localized cell division and selective cell enlargement, which further determine the lengths of stamens and pistils. In addition, auxin and jasmonate (JA) are implicated in regulating cell division and cell expansion in stamens and pistils, and exogenous JA instead of auxin treatment can effectively rescue tomato stigma exsertion through regulating the JA/COI1 signalling pathway. Our findings provide a better understanding of stigma exsertions under the HT condition in tomato and uncover a new function of JA in improving plant abiotic stress tolerance.
Stigma exsertion is commonly observed in cultivated tomatoes under elevated temperature conditions, which severely hampers pollination and fruit set. We demonstrate that high temperature (HT)‐induced stigma exsertion in cultivated tomato is caused by more shortened stamens than pistils. The difference of stamen and pistil length changes under HT is attributed to the different responses of pectin, sugar, expansin, and cyclin, which causes cell wall remodelling and differentially localized cell division and selective cell enlargement under the HT condition. The JA/COI1 signalling pathway participates in regulating HT‐induced stigma exsertion.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>30203844</pmid><doi>10.1111/pce.13444</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-0116-7561</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | auxin Cell division Cell walls Climate change Crop production Cultivation cyclin Cyclopentanes - metabolism Enlargement expansin Flowers - growth & development Flowers - physiology Fructose - metabolism Fruit cultivation Fruit set Global climate Glucose - metabolism heat stress High temperature Hot Temperature Indoleacetic Acids - metabolism Jasmonic acid Lycopersicon esculentum - growth & development Lycopersicon esculentum - metabolism Lycopersicon esculentum - physiology Oxylipins - metabolism Pectin Pectins - metabolism pistil Pistils Plant Growth Regulators - metabolism Pollination Real-Time Polymerase Chain Reaction Regulatory mechanisms (biology) Self-Fertilization Signal Transduction Signaling stamen Stamens Stigmas (botany) Sucrose - metabolism Sugar Tomatoes |
title | Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway |
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