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Role of tomato BRANCHED1‐like genes in the control of shoot branching
Summary In angiosperms, shoot branching greatly determines overall plant architecture and affects fundamental aspects of plant life. Branching patterns are determined by genetic pathways conserved widely across angiosperms. In Arabidopsis thaliana (Brassicaceae, Rosidae) BRANCHED1 (BRC1) plays a cen...
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Published in: | The Plant journal : for cell and molecular biology 2011-08, Vol.67 (4), p.701-714 |
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creator | Martín‐Trillo, Mar Grandío, Eduardo González Serra, François Marcel, Fabien Rodríguez‐Buey, María Luisa Schmitz, Gregor Theres, Klaus Bendahmane, Abdelhafid Dopazo, Hernán Cubas, Pilar |
description | Summary
In angiosperms, shoot branching greatly determines overall plant architecture and affects fundamental aspects of plant life. Branching patterns are determined by genetic pathways conserved widely across angiosperms. In Arabidopsis thaliana (Brassicaceae, Rosidae) BRANCHED1 (BRC1) plays a central role in this process, acting locally to arrest axillary bud growth. In tomato (Solanum lycopersicum, Solanaceae, Asteridae) we have identified two BRC1‐like paralogues, SlBRC1a and SlBRC1b. These genes are expressed in arrested axillary buds and both are down‐regulated upon bud activation, although SlBRC1a is transcribed at much lower levels than SlBRC1b. Alternative splicing of SlBRC1a renders two transcripts that encode two BRC1‐like proteins with different C‐t domains due to a 3′‐terminal frameshift. The phenotype of loss‐of‐function lines suggests that SlBRC1b has retained the ancestral role of BRC1 in shoot branch suppression. We have isolated the BRC1a and BRC1b genes of other Solanum species and have studied their evolution rates across the lineages. These studies indicate that, after duplication of an ancestral BRC1‐like gene, BRC1b genes continued to evolve under a strong purifying selection that was consistent with the conserved function of SlBRC1b in shoot branching control. In contrast, the coding sequences of Solanum BRC1a genes have evolved at a higher evolution rate. Branch‐site tests indicate that this difference does not reflect relaxation but rather positive selective pressure for adaptation. |
doi_str_mv | 10.1111/j.1365-313X.2011.04629.x |
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In angiosperms, shoot branching greatly determines overall plant architecture and affects fundamental aspects of plant life. Branching patterns are determined by genetic pathways conserved widely across angiosperms. In Arabidopsis thaliana (Brassicaceae, Rosidae) BRANCHED1 (BRC1) plays a central role in this process, acting locally to arrest axillary bud growth. In tomato (Solanum lycopersicum, Solanaceae, Asteridae) we have identified two BRC1‐like paralogues, SlBRC1a and SlBRC1b. These genes are expressed in arrested axillary buds and both are down‐regulated upon bud activation, although SlBRC1a is transcribed at much lower levels than SlBRC1b. Alternative splicing of SlBRC1a renders two transcripts that encode two BRC1‐like proteins with different C‐t domains due to a 3′‐terminal frameshift. The phenotype of loss‐of‐function lines suggests that SlBRC1b has retained the ancestral role of BRC1 in shoot branch suppression. We have isolated the BRC1a and BRC1b genes of other Solanum species and have studied their evolution rates across the lineages. These studies indicate that, after duplication of an ancestral BRC1‐like gene, BRC1b genes continued to evolve under a strong purifying selection that was consistent with the conserved function of SlBRC1b in shoot branching control. In contrast, the coding sequences of Solanum BRC1a genes have evolved at a higher evolution rate. Branch‐site tests indicate that this difference does not reflect relaxation but rather positive selective pressure for adaptation.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/j.1365-313X.2011.04629.x</identifier><identifier>PMID: 21554455</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Adaptations ; Alternative splicing ; Amino Acid Sequence ; Angiosperms ; Arabidopsis thaliana ; Asteridae ; Biological and medical sciences ; BRANCHED1 ; Brassicaceae ; Buds ; Chromosome Mapping ; duplication ; Evolution ; Evolution, Molecular ; Evolutionary genetics ; Fundamental and applied biological sciences. Psychology ; Gene Duplication ; Gene expression ; Gene Expression Regulation, Plant - physiology ; Genotype & phenotype ; Life Sciences ; Lycopersicon esculentum ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - growth & development ; Lycopersicon esculentum - metabolism ; Lycopersicon esculentum - ultrastructure ; Molecular Sequence Data ; Mutation ; Phenotype ; Phylogeny ; Plant biology ; Plant growth ; Plant Leaves - genetics ; Plant Leaves - growth & development ; Plant Leaves - metabolism ; Plant Leaves - ultrastructure ; Plant physiology and development ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Shoots - genetics ; Plant Shoots - growth & development ; Plant Shoots - metabolism ; Plant Shoots - ultrastructure ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth & development ; Plants, Genetically Modified - metabolism ; Plants, Genetically Modified - ultrastructure ; Point Mutation ; RNA, Messenger - genetics ; Rosidae ; Sequence Alignment ; shoot branching ; Shoots ; Solanaceae ; Solanum ; TCP genes ; tomato ; Tomatoes ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Vegetal Biology</subject><ispartof>The Plant journal : for cell and molecular biology, 2011-08, Vol.67 (4), p.701-714</ispartof><rights>2011 The Authors. The Plant Journal © 2011 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2011 The Authors. The Plant Journal © 2011 Blackwell Publishing Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6639-a854838585cf00b1b9d3bb2df6b0a0ac06b4b162d560e98e20f010c311c82bc43</citedby><cites>FETCH-LOGICAL-c6639-a854838585cf00b1b9d3bb2df6b0a0ac06b4b162d560e98e20f010c311c82bc43</cites><orcidid>0000-0003-3246-868X ; 0000-0002-8134-5961</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24415350$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21554455$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02651258$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Martín‐Trillo, Mar</creatorcontrib><creatorcontrib>Grandío, Eduardo González</creatorcontrib><creatorcontrib>Serra, François</creatorcontrib><creatorcontrib>Marcel, Fabien</creatorcontrib><creatorcontrib>Rodríguez‐Buey, María Luisa</creatorcontrib><creatorcontrib>Schmitz, Gregor</creatorcontrib><creatorcontrib>Theres, Klaus</creatorcontrib><creatorcontrib>Bendahmane, Abdelhafid</creatorcontrib><creatorcontrib>Dopazo, Hernán</creatorcontrib><creatorcontrib>Cubas, Pilar</creatorcontrib><title>Role of tomato BRANCHED1‐like genes in the control of shoot branching</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
In angiosperms, shoot branching greatly determines overall plant architecture and affects fundamental aspects of plant life. Branching patterns are determined by genetic pathways conserved widely across angiosperms. In Arabidopsis thaliana (Brassicaceae, Rosidae) BRANCHED1 (BRC1) plays a central role in this process, acting locally to arrest axillary bud growth. In tomato (Solanum lycopersicum, Solanaceae, Asteridae) we have identified two BRC1‐like paralogues, SlBRC1a and SlBRC1b. These genes are expressed in arrested axillary buds and both are down‐regulated upon bud activation, although SlBRC1a is transcribed at much lower levels than SlBRC1b. Alternative splicing of SlBRC1a renders two transcripts that encode two BRC1‐like proteins with different C‐t domains due to a 3′‐terminal frameshift. The phenotype of loss‐of‐function lines suggests that SlBRC1b has retained the ancestral role of BRC1 in shoot branch suppression. We have isolated the BRC1a and BRC1b genes of other Solanum species and have studied their evolution rates across the lineages. These studies indicate that, after duplication of an ancestral BRC1‐like gene, BRC1b genes continued to evolve under a strong purifying selection that was consistent with the conserved function of SlBRC1b in shoot branching control. In contrast, the coding sequences of Solanum BRC1a genes have evolved at a higher evolution rate. Branch‐site tests indicate that this difference does not reflect relaxation but rather positive selective pressure for adaptation.</description><subject>Adaptations</subject><subject>Alternative splicing</subject><subject>Amino Acid Sequence</subject><subject>Angiosperms</subject><subject>Arabidopsis thaliana</subject><subject>Asteridae</subject><subject>Biological and medical sciences</subject><subject>BRANCHED1</subject><subject>Brassicaceae</subject><subject>Buds</subject><subject>Chromosome Mapping</subject><subject>duplication</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary genetics</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Duplication</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Genotype & phenotype</subject><subject>Life Sciences</subject><subject>Lycopersicon esculentum</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Lycopersicon esculentum - growth & development</subject><subject>Lycopersicon esculentum - metabolism</subject><subject>Lycopersicon esculentum - ultrastructure</subject><subject>Molecular Sequence Data</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Phylogeny</subject><subject>Plant biology</subject><subject>Plant growth</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - growth & development</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - ultrastructure</subject><subject>Plant physiology and development</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Shoots - genetics</subject><subject>Plant Shoots - growth & development</subject><subject>Plant Shoots - metabolism</subject><subject>Plant Shoots - ultrastructure</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth & development</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>Plants, Genetically Modified - ultrastructure</subject><subject>Point Mutation</subject><subject>RNA, Messenger - genetics</subject><subject>Rosidae</subject><subject>Sequence Alignment</subject><subject>shoot branching</subject><subject>Shoots</subject><subject>Solanaceae</subject><subject>Solanum</subject><subject>TCP genes</subject><subject>tomato</subject><subject>Tomatoes</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Vegetal Biology</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqNkc9uEzEQhy1ERUPhFdAKCQGHXWb8L95DDyG0DSgCVBWJm2U73mbDZl3WG2hvPEKfsU-Cl4QgcUD4Ymv8zehnf4RkCAWm9WpVIJMiZ8g-FxQQC-CSlsX1PTLaX9wnIygl5GOO9JA8jHEFgGMm-QNySFEIzoUYkbPz0PgsVFkf1qYP2evzyfvp7OQN3v24beovPrv0rY9Z3Wb90mcutH0XmoGPyxD6zHamdcu6vXxEDirTRP94tx-RT6cnF9NZPv9w9nY6medOSlbmRgmumBJKuArAoi0XzFq6qKQFA8aBtNyipAshwZfKU6gAwTFEp6h1nB2Rl9u5S9Poq65em-5GB1Pr2WSuhxpQKZAK9Q0T-3zLXnXh68bHXq_r6HzTmNaHTdSqZOW4FKgS-eKfJKafK1MkKhP69C90FTZdm96slWIgxlQNKdUWcl2IsfPVPiqCHgzqlR5E6UGUHgzqXwb1dWp9spu_sWu_2Df-VpaAZzvARGeaajBQxz8c5yiYgMQdb7nvdeNv_juAvvj4bjixn0m9s3U</recordid><startdate>201108</startdate><enddate>201108</enddate><creator>Martín‐Trillo, Mar</creator><creator>Grandío, Eduardo González</creator><creator>Serra, François</creator><creator>Marcel, Fabien</creator><creator>Rodríguez‐Buey, María Luisa</creator><creator>Schmitz, Gregor</creator><creator>Theres, Klaus</creator><creator>Bendahmane, Abdelhafid</creator><creator>Dopazo, Hernán</creator><creator>Cubas, Pilar</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><general>Wiley</general><scope>IQODW</scope><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><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-3246-868X</orcidid><orcidid>https://orcid.org/0000-0002-8134-5961</orcidid></search><sort><creationdate>201108</creationdate><title>Role of tomato BRANCHED1‐like genes in the control of shoot branching</title><author>Martín‐Trillo, Mar ; Grandío, Eduardo González ; Serra, François ; Marcel, Fabien ; Rodríguez‐Buey, María Luisa ; Schmitz, Gregor ; Theres, Klaus ; Bendahmane, Abdelhafid ; Dopazo, Hernán ; Cubas, Pilar</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6639-a854838585cf00b1b9d3bb2df6b0a0ac06b4b162d560e98e20f010c311c82bc43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Adaptations</topic><topic>Alternative splicing</topic><topic>Amino Acid Sequence</topic><topic>Angiosperms</topic><topic>Arabidopsis thaliana</topic><topic>Asteridae</topic><topic>Biological and medical sciences</topic><topic>BRANCHED1</topic><topic>Brassicaceae</topic><topic>Buds</topic><topic>Chromosome Mapping</topic><topic>duplication</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Evolutionary genetics</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Duplication</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>Genotype & phenotype</topic><topic>Life Sciences</topic><topic>Lycopersicon esculentum</topic><topic>Lycopersicon esculentum - genetics</topic><topic>Lycopersicon esculentum - growth & development</topic><topic>Lycopersicon esculentum - metabolism</topic><topic>Lycopersicon esculentum - ultrastructure</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Phylogeny</topic><topic>Plant biology</topic><topic>Plant growth</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - growth & development</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - ultrastructure</topic><topic>Plant physiology and development</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Shoots - genetics</topic><topic>Plant Shoots - growth & development</topic><topic>Plant Shoots - metabolism</topic><topic>Plant Shoots - ultrastructure</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - growth & development</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>Plants, Genetically Modified - ultrastructure</topic><topic>Point Mutation</topic><topic>RNA, Messenger - genetics</topic><topic>Rosidae</topic><topic>Sequence Alignment</topic><topic>shoot branching</topic><topic>Shoots</topic><topic>Solanaceae</topic><topic>Solanum</topic><topic>TCP genes</topic><topic>tomato</topic><topic>Tomatoes</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martín‐Trillo, Mar</creatorcontrib><creatorcontrib>Grandío, Eduardo González</creatorcontrib><creatorcontrib>Serra, François</creatorcontrib><creatorcontrib>Marcel, Fabien</creatorcontrib><creatorcontrib>Rodríguez‐Buey, María Luisa</creatorcontrib><creatorcontrib>Schmitz, Gregor</creatorcontrib><creatorcontrib>Theres, Klaus</creatorcontrib><creatorcontrib>Bendahmane, Abdelhafid</creatorcontrib><creatorcontrib>Dopazo, Hernán</creatorcontrib><creatorcontrib>Cubas, Pilar</creatorcontrib><collection>Pascal-Francis</collection><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><collection>Hyper Article en Ligne (HAL)</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Martín‐Trillo, Mar</au><au>Grandío, Eduardo González</au><au>Serra, François</au><au>Marcel, Fabien</au><au>Rodríguez‐Buey, María Luisa</au><au>Schmitz, Gregor</au><au>Theres, Klaus</au><au>Bendahmane, Abdelhafid</au><au>Dopazo, Hernán</au><au>Cubas, Pilar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of tomato BRANCHED1‐like genes in the control of shoot branching</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2011-08</date><risdate>2011</risdate><volume>67</volume><issue>4</issue><spage>701</spage><epage>714</epage><pages>701-714</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
In angiosperms, shoot branching greatly determines overall plant architecture and affects fundamental aspects of plant life. Branching patterns are determined by genetic pathways conserved widely across angiosperms. In Arabidopsis thaliana (Brassicaceae, Rosidae) BRANCHED1 (BRC1) plays a central role in this process, acting locally to arrest axillary bud growth. In tomato (Solanum lycopersicum, Solanaceae, Asteridae) we have identified two BRC1‐like paralogues, SlBRC1a and SlBRC1b. These genes are expressed in arrested axillary buds and both are down‐regulated upon bud activation, although SlBRC1a is transcribed at much lower levels than SlBRC1b. Alternative splicing of SlBRC1a renders two transcripts that encode two BRC1‐like proteins with different C‐t domains due to a 3′‐terminal frameshift. The phenotype of loss‐of‐function lines suggests that SlBRC1b has retained the ancestral role of BRC1 in shoot branch suppression. We have isolated the BRC1a and BRC1b genes of other Solanum species and have studied their evolution rates across the lineages. These studies indicate that, after duplication of an ancestral BRC1‐like gene, BRC1b genes continued to evolve under a strong purifying selection that was consistent with the conserved function of SlBRC1b in shoot branching control. In contrast, the coding sequences of Solanum BRC1a genes have evolved at a higher evolution rate. Branch‐site tests indicate that this difference does not reflect relaxation but rather positive selective pressure for adaptation.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21554455</pmid><doi>10.1111/j.1365-313X.2011.04629.x</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-3246-868X</orcidid><orcidid>https://orcid.org/0000-0002-8134-5961</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adaptations Alternative splicing Amino Acid Sequence Angiosperms Arabidopsis thaliana Asteridae Biological and medical sciences BRANCHED1 Brassicaceae Buds Chromosome Mapping duplication Evolution Evolution, Molecular Evolutionary genetics Fundamental and applied biological sciences. Psychology Gene Duplication Gene expression Gene Expression Regulation, Plant - physiology Genotype & phenotype Life Sciences Lycopersicon esculentum Lycopersicon esculentum - genetics Lycopersicon esculentum - growth & development Lycopersicon esculentum - metabolism Lycopersicon esculentum - ultrastructure Molecular Sequence Data Mutation Phenotype Phylogeny Plant biology Plant growth Plant Leaves - genetics Plant Leaves - growth & development Plant Leaves - metabolism Plant Leaves - ultrastructure Plant physiology and development Plant Proteins - genetics Plant Proteins - metabolism Plant Shoots - genetics Plant Shoots - growth & development Plant Shoots - metabolism Plant Shoots - ultrastructure Plants, Genetically Modified - genetics Plants, Genetically Modified - growth & development Plants, Genetically Modified - metabolism Plants, Genetically Modified - ultrastructure Point Mutation RNA, Messenger - genetics Rosidae Sequence Alignment shoot branching Shoots Solanaceae Solanum TCP genes tomato Tomatoes Transcription Factors - genetics Transcription Factors - metabolism Vegetal Biology |
title | Role of tomato BRANCHED1‐like genes in the control of shoot branching |
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