Overexpression of thioredoxin m in chloroplasts alters carbon and nitrogen partitioning in tobacco
Abstract In plants, there is a complex interaction between carbon (C) and nitrogen (N) metabolism, and its coordination is fundamental for plant growth and development. Here, we studied the influence of thioredoxin (Trx) m on C and N partitioning using tobacco plants overexpressing Trx m from the ch...
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Veröffentlicht in: | Journal of experimental botany 2021-06, Vol.72 (13), p.4949-4964 |
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creator | Ancín, María Larraya, Luis Florez-Sarasa, Igor Bénard, Camille Fernández-San Millán, Alicia Veramendi, Jon Gibon, Yves Fernie, Alisdair R Aranjuelo, Iker Farran, Inmaculada |
description | Abstract
In plants, there is a complex interaction between carbon (C) and nitrogen (N) metabolism, and its coordination is fundamental for plant growth and development. Here, we studied the influence of thioredoxin (Trx) m on C and N partitioning using tobacco plants overexpressing Trx m from the chloroplast genome. The transgenic plants showed altered metabolism of C (lower leaf starch and soluble sugar accumulation) and N (with higher amounts of amino acids and soluble protein), which pointed to an activation of N metabolism at the expense of carbohydrates. To further delineate the effect of Trx m overexpression, metabolomic and enzymatic analyses were performed on these plants. These results showed an up-regulation of the glutamine synthetase–glutamate synthase pathway; specifically tobacco plants overexpressing Trx m displayed increased activity and stability of glutamine synthetase. Moreover, higher photorespiration and nitrate accumulation were observed in these plants relative to untransformed control plants, indicating that overexpression of Trx m favors the photorespiratory N cycle rather than primary nitrate assimilation. Taken together, our results reveal the importance of Trx m as a molecular mediator of N metabolism in plant chloroplasts.
Thioredoxin m overexpression modulates carbon and nitrogen partitioning in plants by regulating the photorespiratory nitrogen cycle, where an increase of activity and stability of glutamine synthetase was shown. |
doi_str_mv | 10.1093/jxb/erab193 |
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In plants, there is a complex interaction between carbon (C) and nitrogen (N) metabolism, and its coordination is fundamental for plant growth and development. Here, we studied the influence of thioredoxin (Trx) m on C and N partitioning using tobacco plants overexpressing Trx m from the chloroplast genome. The transgenic plants showed altered metabolism of C (lower leaf starch and soluble sugar accumulation) and N (with higher amounts of amino acids and soluble protein), which pointed to an activation of N metabolism at the expense of carbohydrates. To further delineate the effect of Trx m overexpression, metabolomic and enzymatic analyses were performed on these plants. These results showed an up-regulation of the glutamine synthetase–glutamate synthase pathway; specifically tobacco plants overexpressing Trx m displayed increased activity and stability of glutamine synthetase. Moreover, higher photorespiration and nitrate accumulation were observed in these plants relative to untransformed control plants, indicating that overexpression of Trx m favors the photorespiratory N cycle rather than primary nitrate assimilation. Taken together, our results reveal the importance of Trx m as a molecular mediator of N metabolism in plant chloroplasts.
Thioredoxin m overexpression modulates carbon and nitrogen partitioning in plants by regulating the photorespiratory nitrogen cycle, where an increase of activity and stability of glutamine synthetase was shown.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erab193</identifier><identifier>PMID: 33963398</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Carbon - metabolism ; Chloroplast Thioredoxins - metabolism ; Chloroplasts - metabolism ; Gene Expression Regulation, Plant ; Life Sciences & Biomedicine ; Nicotiana - genetics ; Nicotiana - metabolism ; Nitrogen - metabolism ; Plant Sciences ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - metabolism ; Research Papers ; Science & Technology</subject><ispartof>Journal of experimental botany, 2021-06, Vol.72 (13), p.4949-4964</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>10</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000670994100027</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c412t-257017c0ef4d6aeadf7ee25434d516847f889076bce3e8676623e9928eef7d13</citedby><cites>FETCH-LOGICAL-c412t-257017c0ef4d6aeadf7ee25434d516847f889076bce3e8676623e9928eef7d13</cites><orcidid>0000-0001-9000-335X ; 0000-0002-3385-2432 ; 0000-0002-7834-6058 ; 0000-0002-6707-2901 ; 0000-0002-8231-5043 ; 0000-0002-1862-7931 ; 0000-0001-8161-1089 ; 0000-0002-3214-213X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,1585,27929,27930,39263</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33963398$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gutiérrez, Rodrigo</contributor><creatorcontrib>Ancín, María</creatorcontrib><creatorcontrib>Larraya, Luis</creatorcontrib><creatorcontrib>Florez-Sarasa, Igor</creatorcontrib><creatorcontrib>Bénard, Camille</creatorcontrib><creatorcontrib>Fernández-San Millán, Alicia</creatorcontrib><creatorcontrib>Veramendi, Jon</creatorcontrib><creatorcontrib>Gibon, Yves</creatorcontrib><creatorcontrib>Fernie, Alisdair R</creatorcontrib><creatorcontrib>Aranjuelo, Iker</creatorcontrib><creatorcontrib>Farran, Inmaculada</creatorcontrib><title>Overexpression of thioredoxin m in chloroplasts alters carbon and nitrogen partitioning in tobacco</title><title>Journal of experimental botany</title><addtitle>J EXP BOT</addtitle><addtitle>J Exp Bot</addtitle><description>Abstract
In plants, there is a complex interaction between carbon (C) and nitrogen (N) metabolism, and its coordination is fundamental for plant growth and development. Here, we studied the influence of thioredoxin (Trx) m on C and N partitioning using tobacco plants overexpressing Trx m from the chloroplast genome. The transgenic plants showed altered metabolism of C (lower leaf starch and soluble sugar accumulation) and N (with higher amounts of amino acids and soluble protein), which pointed to an activation of N metabolism at the expense of carbohydrates. To further delineate the effect of Trx m overexpression, metabolomic and enzymatic analyses were performed on these plants. These results showed an up-regulation of the glutamine synthetase–glutamate synthase pathway; specifically tobacco plants overexpressing Trx m displayed increased activity and stability of glutamine synthetase. Moreover, higher photorespiration and nitrate accumulation were observed in these plants relative to untransformed control plants, indicating that overexpression of Trx m favors the photorespiratory N cycle rather than primary nitrate assimilation. Taken together, our results reveal the importance of Trx m as a molecular mediator of N metabolism in plant chloroplasts.
Thioredoxin m overexpression modulates carbon and nitrogen partitioning in plants by regulating the photorespiratory nitrogen cycle, where an increase of activity and stability of glutamine synthetase was shown.</description><subject>Carbon - metabolism</subject><subject>Chloroplast Thioredoxins - metabolism</subject><subject>Chloroplasts - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Life Sciences & Biomedicine</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - metabolism</subject><subject>Nitrogen - metabolism</subject><subject>Plant Sciences</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>Research Papers</subject><subject>Science & Technology</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><recordid>eNqNkc2LFDEQxYMo7rh68i59EmFpNx-dr4sgg6vCwl72HtLp6pksPUmbpNfxvzfDjKNexEMqgfrVy6MeQq8Jfk-wZtcP-_4aku2JZk_QinQCt7Rj5ClaYUxpizWXF-hFzg8YY445f44uGNOiHrVC_d0jJNjPCXL2MTRxbMrWxwRD3PvQ7Jpa3HaKKc6TzSU3diqQcuNs6ituw9AEX1LcQGhmm4ovVcWHzWGuxN46F1-iZ6OdMrw63Zfo_ubT_fpLe3v3-ev6423rOkJLS7nERDoMYzcIC3YYJQDlHesGToTq5KiUxlL0DhgoIYWgDLSmCmCUA2GX6MNRdl76HQwOQkl2MnPyO5t-mGi9-bsT_NZs4qNRlGjcsSrw7iSQ4rcFcjE7nx1Mkw0Ql2wor2vlSlFe0asj6lLMOcF4_oZgcwjF1FDMKZRKv_nT2Zn9lUIF1BH4Dn0cs_MQHJyxGpuQWOuO1BeVa1_sYcnruITy28n_jFb67ZGOy_xPyz8BMM66GQ</recordid><startdate>20210622</startdate><enddate>20210622</enddate><creator>Ancín, María</creator><creator>Larraya, Luis</creator><creator>Florez-Sarasa, Igor</creator><creator>Bénard, Camille</creator><creator>Fernández-San Millán, Alicia</creator><creator>Veramendi, Jon</creator><creator>Gibon, Yves</creator><creator>Fernie, Alisdair R</creator><creator>Aranjuelo, Iker</creator><creator>Farran, Inmaculada</creator><general>Oxford University Press</general><general>Oxford Univ Press</general><scope>TOX</scope><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</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>5PM</scope><orcidid>https://orcid.org/0000-0001-9000-335X</orcidid><orcidid>https://orcid.org/0000-0002-3385-2432</orcidid><orcidid>https://orcid.org/0000-0002-7834-6058</orcidid><orcidid>https://orcid.org/0000-0002-6707-2901</orcidid><orcidid>https://orcid.org/0000-0002-8231-5043</orcidid><orcidid>https://orcid.org/0000-0002-1862-7931</orcidid><orcidid>https://orcid.org/0000-0001-8161-1089</orcidid><orcidid>https://orcid.org/0000-0002-3214-213X</orcidid></search><sort><creationdate>20210622</creationdate><title>Overexpression of thioredoxin m in chloroplasts alters carbon and nitrogen partitioning in tobacco</title><author>Ancín, María ; Larraya, Luis ; Florez-Sarasa, Igor ; Bénard, Camille ; Fernández-San Millán, Alicia ; Veramendi, Jon ; Gibon, Yves ; Fernie, Alisdair R ; Aranjuelo, Iker ; Farran, Inmaculada</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-257017c0ef4d6aeadf7ee25434d516847f889076bce3e8676623e9928eef7d13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Carbon - metabolism</topic><topic>Chloroplast Thioredoxins - metabolism</topic><topic>Chloroplasts - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Life Sciences & Biomedicine</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - metabolism</topic><topic>Nitrogen - metabolism</topic><topic>Plant Sciences</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>Research Papers</topic><topic>Science & Technology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ancín, María</creatorcontrib><creatorcontrib>Larraya, Luis</creatorcontrib><creatorcontrib>Florez-Sarasa, Igor</creatorcontrib><creatorcontrib>Bénard, Camille</creatorcontrib><creatorcontrib>Fernández-San Millán, Alicia</creatorcontrib><creatorcontrib>Veramendi, Jon</creatorcontrib><creatorcontrib>Gibon, Yves</creatorcontrib><creatorcontrib>Fernie, Alisdair R</creatorcontrib><creatorcontrib>Aranjuelo, Iker</creatorcontrib><creatorcontrib>Farran, Inmaculada</creatorcontrib><collection>Oxford University Press Open Access</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Web of Science - Science Citation Index Expanded - 2021</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>PubMed Central (Full Participant titles)</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ancín, María</au><au>Larraya, Luis</au><au>Florez-Sarasa, Igor</au><au>Bénard, Camille</au><au>Fernández-San Millán, Alicia</au><au>Veramendi, Jon</au><au>Gibon, Yves</au><au>Fernie, Alisdair R</au><au>Aranjuelo, Iker</au><au>Farran, Inmaculada</au><au>Gutiérrez, Rodrigo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Overexpression of thioredoxin m in chloroplasts alters carbon and nitrogen partitioning in tobacco</atitle><jtitle>Journal of experimental botany</jtitle><stitle>J EXP BOT</stitle><addtitle>J Exp Bot</addtitle><date>2021-06-22</date><risdate>2021</risdate><volume>72</volume><issue>13</issue><spage>4949</spage><epage>4964</epage><pages>4949-4964</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Abstract
In plants, there is a complex interaction between carbon (C) and nitrogen (N) metabolism, and its coordination is fundamental for plant growth and development. Here, we studied the influence of thioredoxin (Trx) m on C and N partitioning using tobacco plants overexpressing Trx m from the chloroplast genome. The transgenic plants showed altered metabolism of C (lower leaf starch and soluble sugar accumulation) and N (with higher amounts of amino acids and soluble protein), which pointed to an activation of N metabolism at the expense of carbohydrates. To further delineate the effect of Trx m overexpression, metabolomic and enzymatic analyses were performed on these plants. These results showed an up-regulation of the glutamine synthetase–glutamate synthase pathway; specifically tobacco plants overexpressing Trx m displayed increased activity and stability of glutamine synthetase. Moreover, higher photorespiration and nitrate accumulation were observed in these plants relative to untransformed control plants, indicating that overexpression of Trx m favors the photorespiratory N cycle rather than primary nitrate assimilation. Taken together, our results reveal the importance of Trx m as a molecular mediator of N metabolism in plant chloroplasts.
Thioredoxin m overexpression modulates carbon and nitrogen partitioning in plants by regulating the photorespiratory nitrogen cycle, where an increase of activity and stability of glutamine synthetase was shown.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>33963398</pmid><doi>10.1093/jxb/erab193</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-9000-335X</orcidid><orcidid>https://orcid.org/0000-0002-3385-2432</orcidid><orcidid>https://orcid.org/0000-0002-7834-6058</orcidid><orcidid>https://orcid.org/0000-0002-6707-2901</orcidid><orcidid>https://orcid.org/0000-0002-8231-5043</orcidid><orcidid>https://orcid.org/0000-0002-1862-7931</orcidid><orcidid>https://orcid.org/0000-0001-8161-1089</orcidid><orcidid>https://orcid.org/0000-0002-3214-213X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Carbon - metabolism Chloroplast Thioredoxins - metabolism Chloroplasts - metabolism Gene Expression Regulation, Plant Life Sciences & Biomedicine Nicotiana - genetics Nicotiana - metabolism Nitrogen - metabolism Plant Sciences Plants, Genetically Modified - genetics Plants, Genetically Modified - metabolism Research Papers Science & Technology |
title | Overexpression of thioredoxin m in chloroplasts alters carbon and nitrogen partitioning in tobacco |
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