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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
Main Authors: Martín‐Trillo, Mar, Grandío, Eduardo González, Serra, François, Marcel, Fabien, Rodríguez‐Buey, María Luisa, Schmitz, Gregor, Theres, Klaus, Bendahmane, Abdelhafid, Dopazo, Hernán, Cubas, Pilar
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cited_by cdi_FETCH-LOGICAL-c6639-a854838585cf00b1b9d3bb2df6b0a0ac06b4b162d560e98e20f010c311c82bc43
cites cdi_FETCH-LOGICAL-c6639-a854838585cf00b1b9d3bb2df6b0a0ac06b4b162d560e98e20f010c311c82bc43
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container_title The Plant journal : for cell and molecular biology
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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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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 &amp; phenotype ; Life Sciences ; Lycopersicon esculentum ; Lycopersicon esculentum - genetics ; Lycopersicon esculentum - growth &amp; development ; Lycopersicon esculentum - metabolism ; Lycopersicon esculentum - ultrastructure ; Molecular Sequence Data ; Mutation ; Phenotype ; Phylogeny ; Plant biology ; Plant growth ; Plant Leaves - genetics ; Plant Leaves - growth &amp; development ; Plant Leaves - metabolism ; Plant Leaves - ultrastructure ; Plant physiology and development ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Shoots - genetics ; Plant Shoots - growth &amp; development ; Plant Shoots - metabolism ; Plant Shoots - ultrastructure ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth &amp; 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. 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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. 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Psychology</subject><subject>Gene Duplication</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>Genotype &amp; phenotype</subject><subject>Life Sciences</subject><subject>Lycopersicon esculentum</subject><subject>Lycopersicon esculentum - genetics</subject><subject>Lycopersicon esculentum - growth &amp; 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 &amp; 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 &amp; development</subject><subject>Plant Shoots - metabolism</subject><subject>Plant Shoots - ultrastructure</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth &amp; 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. 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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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ispartof The Plant journal : for cell and molecular biology, 2011-08, Vol.67 (4), p.701-714
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1365-313X
language eng
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source Wiley-Blackwell Read & Publish Collection; EZB Electronic Journals Library
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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