Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms
Summary Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown...
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creator | Barro‐Trastoy, Daniela Carrera, Esther Baños, Jorge Palau‐Rodríguez, Julia Ruiz‐Rivero, Omar Tornero, Pablo Alonso, José M. López‐Díaz, Isabel Gómez, María Dolores Pérez‐Amador, Miguel A. |
description | Summary
Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity.
Significance Statement
The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. We provide evidence of two different molecular mechanisms of the interaction between gibberellins and brassinosteroids in ovule initiation in two reference species: in Arabidopsis they act independently, whereas in tomato gibberellins mediate brassinosteroid‐dependent ovule initiation. |
doi_str_mv | 10.1111/tpj.14684 |
format | Article |
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Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity.
Significance Statement
The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. We provide evidence of two different molecular mechanisms of the interaction between gibberellins and brassinosteroids in ovule initiation in two reference species: in Arabidopsis they act independently, whereas in tomato gibberellins mediate brassinosteroid‐dependent ovule initiation.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.14684</identifier><identifier>PMID: 31930587</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biosynthesis ; Brassinosteroids ; Brassinosteroids - metabolism ; Complexity ; Cytokinins ; Flowers & plants ; Gene Expression Regulation, Plant - genetics ; Gene Expression Regulation, Plant - physiology ; Genetic analysis ; Gibberellins ; Gibberellins - metabolism ; hormone interaction ; Hormones ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - metabolism ; Molecular modelling ; ovule ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant species ; Primordia ; reproductive development ; Seeds ; Signal transduction ; Signal Transduction - genetics ; Signal Transduction - physiology ; Solanum lycopersicum ; tomato ; Tomatoes</subject><ispartof>The Plant journal : for cell and molecular biology, 2020-06, Vol.102 (5), p.1026-1041</ispartof><rights>2020 The Authors. The Plant Journal © 2020 John Wiley & Sons Ltd</rights><rights>2020 The Authors. The Plant Journal © 2020 John Wiley & Sons Ltd.</rights><rights>Copyright © 2020 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3884-ff9357d5e79b9b7cda72a3fc71cae6c2326937b959fd687218835628684abbdb3</citedby><cites>FETCH-LOGICAL-c3884-ff9357d5e79b9b7cda72a3fc71cae6c2326937b959fd687218835628684abbdb3</cites><orcidid>0000-0002-3454-7552 ; 0000-0002-8968-436X ; 0000-0001-7087-1571 ; 0000-0001-9445-2056 ; 0000-0003-4518-3544 ; 0000-0001-9755-7726 ; 0000-0001-7069-4376</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%2Ftpj.14684$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.14684$$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/31930587$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Barro‐Trastoy, Daniela</creatorcontrib><creatorcontrib>Carrera, Esther</creatorcontrib><creatorcontrib>Baños, Jorge</creatorcontrib><creatorcontrib>Palau‐Rodríguez, Julia</creatorcontrib><creatorcontrib>Ruiz‐Rivero, Omar</creatorcontrib><creatorcontrib>Tornero, Pablo</creatorcontrib><creatorcontrib>Alonso, José M.</creatorcontrib><creatorcontrib>López‐Díaz, Isabel</creatorcontrib><creatorcontrib>Gómez, María Dolores</creatorcontrib><creatorcontrib>Pérez‐Amador, Miguel A.</creatorcontrib><title>Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity.
Significance Statement
The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. We provide evidence of two different molecular mechanisms of the interaction between gibberellins and brassinosteroids in ovule initiation in two reference species: in Arabidopsis they act independently, whereas in tomato gibberellins mediate brassinosteroid‐dependent ovule initiation.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Biosynthesis</subject><subject>Brassinosteroids</subject><subject>Brassinosteroids - metabolism</subject><subject>Complexity</subject><subject>Cytokinins</subject><subject>Flowers & plants</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Genetic analysis</subject><subject>Gibberellins</subject><subject>Gibberellins - metabolism</subject><subject>hormone interaction</subject><subject>Hormones</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Lycopersicon esculentum - metabolism</subject><subject>Molecular modelling</subject><subject>ovule</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant species</subject><subject>Primordia</subject><subject>reproductive development</subject><subject>Seeds</subject><subject>Signal transduction</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - physiology</subject><subject>Solanum lycopersicum</subject><subject>tomato</subject><subject>Tomatoes</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kctq3TAQhkVpaE7SLvoCRdBNA3Wiiy3J3YWQ3gi0lBS6E5IspzrYlqORE84r5KmrHqddFDqbgZmPfy4_Qi8pOaUlzvK8PaW1UPUTtKFcNBWn_MdTtCGtIJWsKTtERwBbQqjkon6GDjltOWmU3KCHb_5mGUwOccKxx_FuGTwOU8hhrdkdvgnW-uSHIUyAzdRhmwxAmCJkn2LooPA4x9HkuG-fJ2NDF2cI8A7n-4jnwUwZw-xd8PB2Xxrj4F2Zm_Do3U8zBRjhOTrozQD-xWM-Rt_fX15ffKyuvnz4dHF-VTmuVF31fcsb2TVetra10nVGMsN7J6kzXjjGmWi5tG3T9p1QklGleCOYKu8x1naWH6M3q-6c4u3iIesxgCv3mcnHBTTjXBEhmKQFff0Puo1Lmsp2mtVEEiJaVRfqZKVcigDJ93pOYTRppynRvw3SxSC9N6iwrx4VFzv67i_5x5ECnK3AfRj87v9K-vrr51XyFylRnMc</recordid><startdate>202006</startdate><enddate>202006</enddate><creator>Barro‐Trastoy, Daniela</creator><creator>Carrera, Esther</creator><creator>Baños, Jorge</creator><creator>Palau‐Rodríguez, Julia</creator><creator>Ruiz‐Rivero, Omar</creator><creator>Tornero, Pablo</creator><creator>Alonso, José M.</creator><creator>López‐Díaz, Isabel</creator><creator>Gómez, María Dolores</creator><creator>Pérez‐Amador, Miguel A.</creator><general>Blackwell Publishing Ltd</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3454-7552</orcidid><orcidid>https://orcid.org/0000-0002-8968-436X</orcidid><orcidid>https://orcid.org/0000-0001-7087-1571</orcidid><orcidid>https://orcid.org/0000-0001-9445-2056</orcidid><orcidid>https://orcid.org/0000-0003-4518-3544</orcidid><orcidid>https://orcid.org/0000-0001-9755-7726</orcidid><orcidid>https://orcid.org/0000-0001-7069-4376</orcidid></search><sort><creationdate>202006</creationdate><title>Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms</title><author>Barro‐Trastoy, Daniela ; Carrera, Esther ; Baños, Jorge ; Palau‐Rodríguez, Julia ; Ruiz‐Rivero, Omar ; Tornero, Pablo ; Alonso, José M. ; López‐Díaz, Isabel ; Gómez, María Dolores ; Pérez‐Amador, Miguel A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3884-ff9357d5e79b9b7cda72a3fc71cae6c2326937b959fd687218835628684abbdb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Biosynthesis</topic><topic>Brassinosteroids</topic><topic>Brassinosteroids - metabolism</topic><topic>Complexity</topic><topic>Cytokinins</topic><topic>Flowers & plants</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Genetic analysis</topic><topic>Gibberellins</topic><topic>Gibberellins - metabolism</topic><topic>hormone interaction</topic><topic>Hormones</topic><topic>Lycopersicon esculentum - genetics</topic><topic>Lycopersicon esculentum - metabolism</topic><topic>Molecular modelling</topic><topic>ovule</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant species</topic><topic>Primordia</topic><topic>reproductive development</topic><topic>Seeds</topic><topic>Signal transduction</topic><topic>Signal Transduction - genetics</topic><topic>Signal Transduction - physiology</topic><topic>Solanum lycopersicum</topic><topic>tomato</topic><topic>Tomatoes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barro‐Trastoy, Daniela</creatorcontrib><creatorcontrib>Carrera, Esther</creatorcontrib><creatorcontrib>Baños, Jorge</creatorcontrib><creatorcontrib>Palau‐Rodríguez, Julia</creatorcontrib><creatorcontrib>Ruiz‐Rivero, Omar</creatorcontrib><creatorcontrib>Tornero, Pablo</creatorcontrib><creatorcontrib>Alonso, José M.</creatorcontrib><creatorcontrib>López‐Díaz, Isabel</creatorcontrib><creatorcontrib>Gómez, María Dolores</creatorcontrib><creatorcontrib>Pérez‐Amador, Miguel A.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barro‐Trastoy, Daniela</au><au>Carrera, Esther</au><au>Baños, Jorge</au><au>Palau‐Rodríguez, Julia</au><au>Ruiz‐Rivero, Omar</au><au>Tornero, Pablo</au><au>Alonso, José M.</au><au>López‐Díaz, Isabel</au><au>Gómez, María Dolores</au><au>Pérez‐Amador, Miguel A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2020-06</date><risdate>2020</risdate><volume>102</volume><issue>5</issue><spage>1026</spage><epage>1041</epage><pages>1026-1041</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co‐regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity.
Significance Statement
The role of hormone interaction has been clearly established for many plant developmental processes. Research interest is naturally shifting toward the elucidation of the molecular mechanism behind these interactions and determining their level of conservation among the vegetal kingdom. We provide evidence of two different molecular mechanisms of the interaction between gibberellins and brassinosteroids in ovule initiation in two reference species: in Arabidopsis they act independently, whereas in tomato gibberellins mediate brassinosteroid‐dependent ovule initiation.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31930587</pmid><doi>10.1111/tpj.14684</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-3454-7552</orcidid><orcidid>https://orcid.org/0000-0002-8968-436X</orcidid><orcidid>https://orcid.org/0000-0001-7087-1571</orcidid><orcidid>https://orcid.org/0000-0001-9445-2056</orcidid><orcidid>https://orcid.org/0000-0003-4518-3544</orcidid><orcidid>https://orcid.org/0000-0001-9755-7726</orcidid><orcidid>https://orcid.org/0000-0001-7069-4376</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Biosynthesis Brassinosteroids Brassinosteroids - metabolism Complexity Cytokinins Flowers & plants Gene Expression Regulation, Plant - genetics Gene Expression Regulation, Plant - physiology Genetic analysis Gibberellins Gibberellins - metabolism hormone interaction Hormones Lycopersicon esculentum - genetics Lycopersicon esculentum - metabolism Molecular modelling ovule Plant Proteins - genetics Plant Proteins - metabolism Plant species Primordia reproductive development Seeds Signal transduction Signal Transduction - genetics Signal Transduction - physiology Solanum lycopersicum tomato Tomatoes |
title | Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms |
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