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The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions
Abscisic acid-, stress-, and ripening-induced (ASR) proteins were first described about 15 years ago as accumulating to high levels during plant developmental processes and in response to diverse stresses. Currently, the effects of ASRs on water deficit tolerance and the ways in which their physiolo...
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Published in: | Plant physiology (Bethesda) 2011-10, Vol.157 (2), p.917-936 |
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creator | Virlouvet, Laetitia Jacquemot, Marie-Pierre Gerentes, Denise Corti, Hélène Bouton, Sophie Gilard, Françoise Valot, Benoît Trouverie, Jacques Tcherkez, Guillaume Falque, Matthieu Damerval, Catherine Rogowsky, Peter Perez, Pascual Noctor, Graham Zivy, Michel Coursol, Sylvie |
description | Abscisic acid-, stress-, and ripening-induced (ASR) proteins were first described about 15 years ago as accumulating to high levels during plant developmental processes and in response to diverse stresses. Currently, the effects of ASRs on water deficit tolerance and the ways in which their physiological and biochemical functions lead to this stress tolerance remain poorly understood. Here, we characterized the ASR gene family from maize (Zea mays), which contains nine paralogous genes, and showed that maize ASR1 (ZmASR1) was encoded by one of the most highly expressed paralogs. Ectopic expression of ZmASR1 had a large overall impact on maize yield that was maintained under water-limited stress conditions in the field. Comparative transcriptomic and proteomic analyses of wild-type and ZmASR1 -overexpressing leaves led to the identification of three transcripts and 16 proteins up-or down-regulated by ZmASR1. The majority of them were involved in primary and/or cellular metabolic processes, including branched-chain amino acid (BCAA) biosynthesis. Metabolomic and transcript analyses further indicated that ZmASR1 -overexpressing plants showed a decrease in BCAA compounds and changes in BCAA-related gene expression in comparison with wild-type plants. Interestingly, within-group correlation matrix analysis revealed a close link between 13 decreased metabolites in ZmASR1 -overexpressing leaves, including two A As. Among these 13 metabolites, six were previously shown to be negatively correlated to biomass, suggesting that ZmASR1-dependent regulation of these 13 metabolites might contribute to regulate leaf growth, resulting in improvement in kernel yield. |
doi_str_mv | 10.1104/pp.111.176818 |
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Currently, the effects of ASRs on water deficit tolerance and the ways in which their physiological and biochemical functions lead to this stress tolerance remain poorly understood. Here, we characterized the ASR gene family from maize (Zea mays), which contains nine paralogous genes, and showed that maize ASR1 (ZmASR1) was encoded by one of the most highly expressed paralogs. Ectopic expression of ZmASR1 had a large overall impact on maize yield that was maintained under water-limited stress conditions in the field. Comparative transcriptomic and proteomic analyses of wild-type and ZmASR1 -overexpressing leaves led to the identification of three transcripts and 16 proteins up-or down-regulated by ZmASR1. The majority of them were involved in primary and/or cellular metabolic processes, including branched-chain amino acid (BCAA) biosynthesis. Metabolomic and transcript analyses further indicated that ZmASR1 -overexpressing plants showed a decrease in BCAA compounds and changes in BCAA-related gene expression in comparison with wild-type plants. Interestingly, within-group correlation matrix analysis revealed a close link between 13 decreased metabolites in ZmASR1 -overexpressing leaves, including two A As. Among these 13 metabolites, six were previously shown to be negatively correlated to biomass, suggesting that ZmASR1-dependent regulation of these 13 metabolites might contribute to regulate leaf growth, resulting in improvement in kernel yield.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.111.176818</identifier><identifier>PMID: 21852416</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Amino Acid Sequence ; Amino acids ; Amino Acids, Branched-Chain - metabolism ; Biological and medical sciences ; Biosynthesis ; Branched chain amino acids ; Corn ; Dehydration ; ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Plant ; Genes ; Leaves ; Life Sciences ; Molecular Sequence Data ; Multigene Family ; Plant Leaves - physiology ; Plant physiology and development ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants ; Protein metabolism ; Proteins ; Proteomics ; Seeds - growth & development ; Stress, Physiological ; Vegetal Biology ; Water ; Zea mays - genetics</subject><ispartof>Plant physiology (Bethesda), 2011-10, Vol.157 (2), p.917-936</ispartof><rights>2011 American Society of Plant Biologists</rights><rights>2015 INIST-CNRS</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-c417t-6fbc1ffae1e8b66255d78e8094e3e5ab1e6e384b0a590dba1d95d54830d99c6b3</citedby><cites>FETCH-LOGICAL-c417t-6fbc1ffae1e8b66255d78e8094e3e5ab1e6e384b0a590dba1d95d54830d99c6b3</cites><orcidid>0000-0002-6444-858X ; 0000-0001-8689-310X ; 0000-0002-7317-4971 ; 0000-0002-3931-0263 ; 0000-0002-3339-956X ; 0000-0001-9314-1555 ; 0000-0002-6629-2400 ; 0000-0002-1450-896X ; 0000-0003-4822-3783</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41435701$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41435701$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24595642$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21852416$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02647863$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Virlouvet, Laetitia</creatorcontrib><creatorcontrib>Jacquemot, Marie-Pierre</creatorcontrib><creatorcontrib>Gerentes, Denise</creatorcontrib><creatorcontrib>Corti, Hélène</creatorcontrib><creatorcontrib>Bouton, Sophie</creatorcontrib><creatorcontrib>Gilard, Françoise</creatorcontrib><creatorcontrib>Valot, Benoît</creatorcontrib><creatorcontrib>Trouverie, Jacques</creatorcontrib><creatorcontrib>Tcherkez, Guillaume</creatorcontrib><creatorcontrib>Falque, Matthieu</creatorcontrib><creatorcontrib>Damerval, Catherine</creatorcontrib><creatorcontrib>Rogowsky, Peter</creatorcontrib><creatorcontrib>Perez, Pascual</creatorcontrib><creatorcontrib>Noctor, Graham</creatorcontrib><creatorcontrib>Zivy, Michel</creatorcontrib><creatorcontrib>Coursol, Sylvie</creatorcontrib><title>The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Abscisic acid-, stress-, and ripening-induced (ASR) proteins were first described about 15 years ago as accumulating to high levels during plant developmental processes and in response to diverse stresses. Currently, the effects of ASRs on water deficit tolerance and the ways in which their physiological and biochemical functions lead to this stress tolerance remain poorly understood. Here, we characterized the ASR gene family from maize (Zea mays), which contains nine paralogous genes, and showed that maize ASR1 (ZmASR1) was encoded by one of the most highly expressed paralogs. Ectopic expression of ZmASR1 had a large overall impact on maize yield that was maintained under water-limited stress conditions in the field. Comparative transcriptomic and proteomic analyses of wild-type and ZmASR1 -overexpressing leaves led to the identification of three transcripts and 16 proteins up-or down-regulated by ZmASR1. The majority of them were involved in primary and/or cellular metabolic processes, including branched-chain amino acid (BCAA) biosynthesis. Metabolomic and transcript analyses further indicated that ZmASR1 -overexpressing plants showed a decrease in BCAA compounds and changes in BCAA-related gene expression in comparison with wild-type plants. Interestingly, within-group correlation matrix analysis revealed a close link between 13 decreased metabolites in ZmASR1 -overexpressing leaves, including two A As. Among these 13 metabolites, six were previously shown to be negatively correlated to biomass, suggesting that ZmASR1-dependent regulation of these 13 metabolites might contribute to regulate leaf growth, resulting in improvement in kernel yield.</description><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Amino Acids, Branched-Chain - metabolism</subject><subject>Biological and medical sciences</subject><subject>Biosynthesis</subject><subject>Branched chain amino acids</subject><subject>Corn</subject><subject>Dehydration</subject><subject>ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>Leaves</subject><subject>Life Sciences</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Plant Leaves - physiology</subject><subject>Plant physiology and development</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants</subject><subject>Protein metabolism</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Seeds - growth & development</subject><subject>Stress, Physiological</subject><subject>Vegetal Biology</subject><subject>Water</subject><subject>Zea mays - genetics</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNpF0UGL1DAUB_AgijuuHj0quYh46JrXJml67A7qLo4ouiJ6KWnzymRpk5q0wvoF_Npm6Dgewgt5v7zD-xPyFNgFAOOvpylVuIBSKlD3yAZEkWe54Oo-2TCW7kyp6ow8ivGWMQYF8IfkLAclcg5yQ_7c7JH-GOsvn4F-Cn5G6-i164cFXYeRXgbtuj2abLvXqVOP1nlad9bQS-vjnZv3GG2k2hn6IYE5nUjfY3A40O8WB0PTr9T5jXRxBgP9pmcM2c6OdkZDt94ZO1vv4mPyoNdDxCfHek6-vn1zs73Kdh_fXW_rXdZxKOdM9m0Hfa8RULVS5kKYUqFiFccChW4BJRaKt0yLiplWg6mEScsomKmqTrbFOXm1zt3roZmCHXW4a7y2zVW9aw5vLJe8VLL4Bcm-XO0U_M8F49yMNnY4DNqhX2KjKinyshRlktkqu-BjDNifRgNrDjE105QqNGtMyT8_Tl7aEc1J_8slgRdHoGOnh_4Qg43_HReVkDxP7tnqbuPsw6nPgReiTGn_Ba4kpAQ</recordid><startdate>20111001</startdate><enddate>20111001</enddate><creator>Virlouvet, Laetitia</creator><creator>Jacquemot, Marie-Pierre</creator><creator>Gerentes, Denise</creator><creator>Corti, Hélène</creator><creator>Bouton, Sophie</creator><creator>Gilard, Françoise</creator><creator>Valot, Benoît</creator><creator>Trouverie, Jacques</creator><creator>Tcherkez, Guillaume</creator><creator>Falque, Matthieu</creator><creator>Damerval, Catherine</creator><creator>Rogowsky, Peter</creator><creator>Perez, Pascual</creator><creator>Noctor, Graham</creator><creator>Zivy, Michel</creator><creator>Coursol, Sylvie</creator><general>American Society of Plant Biologists</general><general>Oxford University Press ; American Society of Plant Biologists</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>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-6444-858X</orcidid><orcidid>https://orcid.org/0000-0001-8689-310X</orcidid><orcidid>https://orcid.org/0000-0002-7317-4971</orcidid><orcidid>https://orcid.org/0000-0002-3931-0263</orcidid><orcidid>https://orcid.org/0000-0002-3339-956X</orcidid><orcidid>https://orcid.org/0000-0001-9314-1555</orcidid><orcidid>https://orcid.org/0000-0002-6629-2400</orcidid><orcidid>https://orcid.org/0000-0002-1450-896X</orcidid><orcidid>https://orcid.org/0000-0003-4822-3783</orcidid></search><sort><creationdate>20111001</creationdate><title>The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions</title><author>Virlouvet, Laetitia ; Jacquemot, Marie-Pierre ; Gerentes, Denise ; Corti, Hélène ; Bouton, Sophie ; Gilard, Françoise ; Valot, Benoît ; Trouverie, Jacques ; Tcherkez, Guillaume ; Falque, Matthieu ; Damerval, Catherine ; Rogowsky, Peter ; Perez, Pascual ; Noctor, Graham ; Zivy, Michel ; Coursol, Sylvie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c417t-6fbc1ffae1e8b66255d78e8094e3e5ab1e6e384b0a590dba1d95d54830d99c6b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Amino Acid Sequence</topic><topic>Amino acids</topic><topic>Amino Acids, Branched-Chain - metabolism</topic><topic>Biological and medical sciences</topic><topic>Biosynthesis</topic><topic>Branched chain amino acids</topic><topic>Corn</topic><topic>Dehydration</topic><topic>ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>Leaves</topic><topic>Life Sciences</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family</topic><topic>Plant Leaves - physiology</topic><topic>Plant physiology and development</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants</topic><topic>Protein metabolism</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Seeds - growth & development</topic><topic>Stress, Physiological</topic><topic>Vegetal Biology</topic><topic>Water</topic><topic>Zea mays - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Virlouvet, Laetitia</creatorcontrib><creatorcontrib>Jacquemot, Marie-Pierre</creatorcontrib><creatorcontrib>Gerentes, Denise</creatorcontrib><creatorcontrib>Corti, Hélène</creatorcontrib><creatorcontrib>Bouton, Sophie</creatorcontrib><creatorcontrib>Gilard, Françoise</creatorcontrib><creatorcontrib>Valot, Benoît</creatorcontrib><creatorcontrib>Trouverie, Jacques</creatorcontrib><creatorcontrib>Tcherkez, Guillaume</creatorcontrib><creatorcontrib>Falque, Matthieu</creatorcontrib><creatorcontrib>Damerval, Catherine</creatorcontrib><creatorcontrib>Rogowsky, Peter</creatorcontrib><creatorcontrib>Perez, Pascual</creatorcontrib><creatorcontrib>Noctor, Graham</creatorcontrib><creatorcontrib>Zivy, Michel</creatorcontrib><creatorcontrib>Coursol, Sylvie</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>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Virlouvet, Laetitia</au><au>Jacquemot, Marie-Pierre</au><au>Gerentes, Denise</au><au>Corti, Hélène</au><au>Bouton, Sophie</au><au>Gilard, Françoise</au><au>Valot, Benoît</au><au>Trouverie, Jacques</au><au>Tcherkez, Guillaume</au><au>Falque, Matthieu</au><au>Damerval, Catherine</au><au>Rogowsky, Peter</au><au>Perez, Pascual</au><au>Noctor, Graham</au><au>Zivy, Michel</au><au>Coursol, Sylvie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2011-10-01</date><risdate>2011</risdate><volume>157</volume><issue>2</issue><spage>917</spage><epage>936</epage><pages>917-936</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Abscisic acid-, stress-, and ripening-induced (ASR) proteins were first described about 15 years ago as accumulating to high levels during plant developmental processes and in response to diverse stresses. Currently, the effects of ASRs on water deficit tolerance and the ways in which their physiological and biochemical functions lead to this stress tolerance remain poorly understood. Here, we characterized the ASR gene family from maize (Zea mays), which contains nine paralogous genes, and showed that maize ASR1 (ZmASR1) was encoded by one of the most highly expressed paralogs. Ectopic expression of ZmASR1 had a large overall impact on maize yield that was maintained under water-limited stress conditions in the field. Comparative transcriptomic and proteomic analyses of wild-type and ZmASR1 -overexpressing leaves led to the identification of three transcripts and 16 proteins up-or down-regulated by ZmASR1. The majority of them were involved in primary and/or cellular metabolic processes, including branched-chain amino acid (BCAA) biosynthesis. Metabolomic and transcript analyses further indicated that ZmASR1 -overexpressing plants showed a decrease in BCAA compounds and changes in BCAA-related gene expression in comparison with wild-type plants. Interestingly, within-group correlation matrix analysis revealed a close link between 13 decreased metabolites in ZmASR1 -overexpressing leaves, including two A As. Among these 13 metabolites, six were previously shown to be negatively correlated to biomass, suggesting that ZmASR1-dependent regulation of these 13 metabolites might contribute to regulate leaf growth, resulting in improvement in kernel yield.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>21852416</pmid><doi>10.1104/pp.111.176818</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-6444-858X</orcidid><orcidid>https://orcid.org/0000-0001-8689-310X</orcidid><orcidid>https://orcid.org/0000-0002-7317-4971</orcidid><orcidid>https://orcid.org/0000-0002-3931-0263</orcidid><orcidid>https://orcid.org/0000-0002-3339-956X</orcidid><orcidid>https://orcid.org/0000-0001-9314-1555</orcidid><orcidid>https://orcid.org/0000-0002-6629-2400</orcidid><orcidid>https://orcid.org/0000-0002-1450-896X</orcidid><orcidid>https://orcid.org/0000-0003-4822-3783</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Amino acids Amino Acids, Branched-Chain - metabolism Biological and medical sciences Biosynthesis Branched chain amino acids Corn Dehydration ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Plant Genes Leaves Life Sciences Molecular Sequence Data Multigene Family Plant Leaves - physiology Plant physiology and development Plant Proteins - genetics Plant Proteins - metabolism Plants Protein metabolism Proteins Proteomics Seeds - growth & development Stress, Physiological Vegetal Biology Water Zea mays - genetics |
title | The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions |
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