An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants
Plants are challenged by a large number of environmental stresses that reduce productivity and even cause death. Both chloroplasts and mitochondria produce reactive oxygen species under normal conditions; however, stress causes an imbalance in these species that leads to deviations from normal cellu...
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description | Plants are challenged by a large number of environmental stresses that reduce productivity and even cause death. Both chloroplasts and mitochondria produce reactive oxygen species under normal conditions; however, stress causes an imbalance in these species that leads to deviations from normal cellular conditions and a variety of toxic effects. Mitochondria have uncoupling proteins (UCPs) that uncouple electron transport from ATP synthesis. There is evidence that UCPs play a role in alleviating stress caused by reactive oxygen species overproduction. However, direct evidence that UCPs protect plants from abiotic stress is lacking.
Tolerances to salt and water deficit were analyzed in transgenic tobacco plants that overexpress a UCP (AtUCP1) from Arabidopsis thaliana. Seeds of AtUCP1 transgenic lines germinated faster, and adult plants showed better responses to drought and salt stress than wild-type (WT) plants. These phenotypes correlated with increased water retention and higher gas exchange parameters in transgenic plants that overexpress AtUCP1. WT plants exhibited increased respiration under stress, while transgenic plants were only slightly affected. Furthermore, the transgenic plants showed reduced accumulation of hydrogen peroxide in stressed leaves compared with WT plants.
Higher levels of AtUCP1 improved tolerance to multiple abiotic stresses, and this protection was correlated with lower oxidative stress. Our data support previous assumptions that UCPs reduce the imbalance of reactive oxygen species. Our data also suggest that UCPs may play a role in stomatal closure, which agrees with other evidence of a direct relationship between these proteins and photosynthesis. Manipulation of the UCP protein expression in mitochondria is a new avenue for crop improvement and may lead to crops with greater tolerance for challenging environmental conditions. |
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Tolerances to salt and water deficit were analyzed in transgenic tobacco plants that overexpress a UCP (AtUCP1) from Arabidopsis thaliana. Seeds of AtUCP1 transgenic lines germinated faster, and adult plants showed better responses to drought and salt stress than wild-type (WT) plants. These phenotypes correlated with increased water retention and higher gas exchange parameters in transgenic plants that overexpress AtUCP1. WT plants exhibited increased respiration under stress, while transgenic plants were only slightly affected. Furthermore, the transgenic plants showed reduced accumulation of hydrogen peroxide in stressed leaves compared with WT plants.
Higher levels of AtUCP1 improved tolerance to multiple abiotic stresses, and this protection was correlated with lower oxidative stress. Our data support previous assumptions that UCPs reduce the imbalance of reactive oxygen species. Our data also suggest that UCPs may play a role in stomatal closure, which agrees with other evidence of a direct relationship between these proteins and photosynthesis. Manipulation of the UCP protein expression in mitochondria is a new avenue for crop improvement and may lead to crops with greater tolerance for challenging environmental conditions.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0023776</identifier><identifier>PMID: 21912606</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abiotic stress ; Agriculture ; Analysis ; Antioxidants ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis Proteins - genetics ; Arabidopsis thaliana ; Biology ; Carbon ; Chloroplasts ; Crop improvement ; Crops ; Crops, Agricultural - genetics ; Crops, Agricultural - metabolism ; Crops, Agricultural - physiology ; Dehydrogenases ; Drought ; Droughts ; Electron transport ; Environmental conditions ; Environmental stress ; Flowers & plants ; Gas exchange ; Genetic engineering ; Genetically modified plants ; Germination ; Germination - genetics ; Geum urbanum ; Hydrogen ; Hydrogen peroxide ; Ion Channels - genetics ; Leaves ; Metabolism ; Mitochondria ; Mitochondrial Proteins - genetics ; Nicotiana - genetics ; Nicotiana - metabolism ; Nicotiana - physiology ; Oxidative stress ; Oxygen ; Phenotype ; Phenotypes ; Photoreceptors ; Photosynthesis ; Physiology ; Plant biochemistry ; Plant growth ; Plant mitochondria ; Plant protection ; Plant sciences ; Plants, Genetically Modified ; Proteins ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Respiration ; Salinity tolerance ; Salt Tolerance - genetics ; Salts ; Seeds ; Stomata ; Stress, Physiological - genetics ; Tobacco ; Tolerances ; Toxicity ; Transgenic plants ; Uncoupling Protein 1 ; Water deficit</subject><ispartof>PloS one, 2011-08, Vol.6 (8), p.e23776</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Begcy et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Begcy et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c691t-998cbb9d14314a0d85d81ccfffb393e6d57ba0f8412bc90654d8fb69e0c9af593</citedby><cites>FETCH-LOGICAL-c691t-998cbb9d14314a0d85d81ccfffb393e6d57ba0f8412bc90654d8fb69e0c9af593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3166057/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3166057/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21912606$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Shirihai, Orian S.</contributor><creatorcontrib>Begcy, Kevin</creatorcontrib><creatorcontrib>Mariano, Eduardo D</creatorcontrib><creatorcontrib>Mattiello, Lucia</creatorcontrib><creatorcontrib>Nunes, Alessandra V</creatorcontrib><creatorcontrib>Mazzafera, Paulo</creatorcontrib><creatorcontrib>Maia, Ivan G</creatorcontrib><creatorcontrib>Menossi, Marcelo</creatorcontrib><title>An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Plants are challenged by a large number of environmental stresses that reduce productivity and even cause death. Both chloroplasts and mitochondria produce reactive oxygen species under normal conditions; however, stress causes an imbalance in these species that leads to deviations from normal cellular conditions and a variety of toxic effects. Mitochondria have uncoupling proteins (UCPs) that uncouple electron transport from ATP synthesis. There is evidence that UCPs play a role in alleviating stress caused by reactive oxygen species overproduction. However, direct evidence that UCPs protect plants from abiotic stress is lacking.
Tolerances to salt and water deficit were analyzed in transgenic tobacco plants that overexpress a UCP (AtUCP1) from Arabidopsis thaliana. Seeds of AtUCP1 transgenic lines germinated faster, and adult plants showed better responses to drought and salt stress than wild-type (WT) plants. These phenotypes correlated with increased water retention and higher gas exchange parameters in transgenic plants that overexpress AtUCP1. WT plants exhibited increased respiration under stress, while transgenic plants were only slightly affected. Furthermore, the transgenic plants showed reduced accumulation of hydrogen peroxide in stressed leaves compared with WT plants.
Higher levels of AtUCP1 improved tolerance to multiple abiotic stresses, and this protection was correlated with lower oxidative stress. Our data support previous assumptions that UCPs reduce the imbalance of reactive oxygen species. Our data also suggest that UCPs may play a role in stomatal closure, which agrees with other evidence of a direct relationship between these proteins and photosynthesis. Manipulation of the UCP protein expression in mitochondria is a new avenue for crop improvement and may lead to crops with greater tolerance for challenging environmental conditions.</description><subject>Abiotic stress</subject><subject>Agriculture</subject><subject>Analysis</subject><subject>Antioxidants</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis thaliana</subject><subject>Biology</subject><subject>Carbon</subject><subject>Chloroplasts</subject><subject>Crop improvement</subject><subject>Crops</subject><subject>Crops, Agricultural - genetics</subject><subject>Crops, Agricultural - metabolism</subject><subject>Crops, Agricultural - physiology</subject><subject>Dehydrogenases</subject><subject>Drought</subject><subject>Droughts</subject><subject>Electron transport</subject><subject>Environmental conditions</subject><subject>Environmental stress</subject><subject>Flowers & plants</subject><subject>Gas exchange</subject><subject>Genetic engineering</subject><subject>Genetically modified plants</subject><subject>Germination</subject><subject>Germination - genetics</subject><subject>Geum urbanum</subject><subject>Hydrogen</subject><subject>Hydrogen peroxide</subject><subject>Ion Channels - genetics</subject><subject>Leaves</subject><subject>Metabolism</subject><subject>Mitochondria</subject><subject>Mitochondrial Proteins - genetics</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - metabolism</subject><subject>Nicotiana - physiology</subject><subject>Oxidative stress</subject><subject>Oxygen</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Photoreceptors</subject><subject>Photosynthesis</subject><subject>Physiology</subject><subject>Plant biochemistry</subject><subject>Plant growth</subject><subject>Plant mitochondria</subject><subject>Plant protection</subject><subject>Plant sciences</subject><subject>Plants, Genetically Modified</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Respiration</subject><subject>Salinity tolerance</subject><subject>Salt Tolerance - genetics</subject><subject>Salts</subject><subject>Seeds</subject><subject>Stomata</subject><subject>Stress, Physiological - genetics</subject><subject>Tobacco</subject><subject>Tolerances</subject><subject>Toxicity</subject><subject>Transgenic plants</subject><subject>Uncoupling Protein 1</subject><subject>Water deficit</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNkluL1DAYhoso7rr6D0QDguDFjDm0aXMjDIuHgYUFT7chzaGTJZPUJBX335txussUFCQXCV-e7_3Cm7eqniO4RqRFb2_CFL1w6zF4vYYQk7alD6pzxAheUQzJw5PzWfUkpRsIG9JR-rg6w4ghTCE9r243Hmyi6K0KY7IJ7G0Oche8ilY4MHkZptFZP4AxhqytBzJ4o2MCOTgdhZe6nICKYRp2GQivQBIug5SjTgkUPhcoDdpbWcBeSBnA6ITP6Wn1yAiX9LN5v6i-fXj_9fLT6ur64_Zyc7WSlKG8YqyTfc8UqgmqBVRdozokpTGmJ4xoqpq2F9B0NcK9ZJA2tepMT5mGkgnTMHJRvTzqji4kPruWOCKwg7htG1yI7ZFQQdzwMdq9iLc8CMv_FEIcuIjZSqe5JMVTRZq2LhMl0qyjmDGsa9pgCclh2rt52tTvtZLaFwPcQnR54-2OD-EnJ4hS2LRF4NUsEMOPSaf8jyfP1CDKq6w3oYjJvU2Sb-qWdh0iuC7U-i9UWUrvbflIbWypLxreLBoKk_WvPIgpJb798vn_2evvS_b1CbvTJSK7FNyUbfBpCdZHUMaQUtTm3jkE-SH2d27wQ-z5HPvS9uLU9fumu5yT303P_1o</recordid><startdate>20110830</startdate><enddate>20110830</enddate><creator>Begcy, Kevin</creator><creator>Mariano, Eduardo D</creator><creator>Mattiello, Lucia</creator><creator>Nunes, Alessandra V</creator><creator>Mazzafera, Paulo</creator><creator>Maia, Ivan G</creator><creator>Menossi, Marcelo</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20110830</creationdate><title>An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants</title><author>Begcy, Kevin ; Mariano, Eduardo D ; Mattiello, Lucia ; Nunes, Alessandra V ; Mazzafera, Paulo ; Maia, Ivan G ; Menossi, Marcelo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c691t-998cbb9d14314a0d85d81ccfffb393e6d57ba0f8412bc90654d8fb69e0c9af593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Abiotic stress</topic><topic>Agriculture</topic><topic>Analysis</topic><topic>Antioxidants</topic><topic>Arabidopsis</topic><topic>Arabidopsis - 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Both chloroplasts and mitochondria produce reactive oxygen species under normal conditions; however, stress causes an imbalance in these species that leads to deviations from normal cellular conditions and a variety of toxic effects. Mitochondria have uncoupling proteins (UCPs) that uncouple electron transport from ATP synthesis. There is evidence that UCPs play a role in alleviating stress caused by reactive oxygen species overproduction. However, direct evidence that UCPs protect plants from abiotic stress is lacking.
Tolerances to salt and water deficit were analyzed in transgenic tobacco plants that overexpress a UCP (AtUCP1) from Arabidopsis thaliana. Seeds of AtUCP1 transgenic lines germinated faster, and adult plants showed better responses to drought and salt stress than wild-type (WT) plants. These phenotypes correlated with increased water retention and higher gas exchange parameters in transgenic plants that overexpress AtUCP1. WT plants exhibited increased respiration under stress, while transgenic plants were only slightly affected. Furthermore, the transgenic plants showed reduced accumulation of hydrogen peroxide in stressed leaves compared with WT plants.
Higher levels of AtUCP1 improved tolerance to multiple abiotic stresses, and this protection was correlated with lower oxidative stress. Our data support previous assumptions that UCPs reduce the imbalance of reactive oxygen species. Our data also suggest that UCPs may play a role in stomatal closure, which agrees with other evidence of a direct relationship between these proteins and photosynthesis. Manipulation of the UCP protein expression in mitochondria is a new avenue for crop improvement and may lead to crops with greater tolerance for challenging environmental conditions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21912606</pmid><doi>10.1371/journal.pone.0023776</doi><tpages>e23776</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Abiotic stress Agriculture Analysis Antioxidants Arabidopsis Arabidopsis - genetics Arabidopsis Proteins - genetics Arabidopsis thaliana Biology Carbon Chloroplasts Crop improvement Crops Crops, Agricultural - genetics Crops, Agricultural - metabolism Crops, Agricultural - physiology Dehydrogenases Drought Droughts Electron transport Environmental conditions Environmental stress Flowers & plants Gas exchange Genetic engineering Genetically modified plants Germination Germination - genetics Geum urbanum Hydrogen Hydrogen peroxide Ion Channels - genetics Leaves Metabolism Mitochondria Mitochondrial Proteins - genetics Nicotiana - genetics Nicotiana - metabolism Nicotiana - physiology Oxidative stress Oxygen Phenotype Phenotypes Photoreceptors Photosynthesis Physiology Plant biochemistry Plant growth Plant mitochondria Plant protection Plant sciences Plants, Genetically Modified Proteins Reactive oxygen species Reactive Oxygen Species - metabolism Respiration Salinity tolerance Salt Tolerance - genetics Salts Seeds Stomata Stress, Physiological - genetics Tobacco Tolerances Toxicity Transgenic plants Uncoupling Protein 1 Water deficit |
title | An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-20T20%3A02%3A09IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=An%20Arabidopsis%20mitochondrial%20uncoupling%20protein%20confers%20tolerance%20to%20drought%20and%20salt%20stress%20in%20transgenic%20tobacco%20plants&rft.jtitle=PloS%20one&rft.au=Begcy,%20Kevin&rft.date=2011-08-30&rft.volume=6&rft.issue=8&rft.spage=e23776&rft.pages=e23776-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0023776&rft_dat=%3Cgale_plos_%3EA476881324%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1308027752&rft_id=info:pmid/21912606&rft_galeid=A476881324&rft_doaj_id=oai_doaj_org_article_c3193d3574f84c1e9862992e4652c039&rfr_iscdi=true |