Energy costs of salt tolerance in crop plants
Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would m...
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Veröffentlicht in: | The New phytologist 2020-02, Vol.225 (3), p.1072-1090 |
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creator | Munns, Rana Day, David A. Fricke, Wieland Watt, Michelle Arsova, Borjana Barkla, Bronwyn J. Bose, Jayakumar Byrt, Caitlin S. Chen, Zhong-Hua Foster, Kylie J. Gilliham, Matthew Henderson, Sam W. Jenkins, Colin L. D. Kronzucker, Herbert J. Miklavcic, Stanley J. Plett, Darren Roy, Stuart J. Shabala, Sergey Shelden, Megan C. Soole, Kathleen L. Taylor, Nicolas L. Tester, Mark Wege, Stefanie Wegner, Lars H. Tyerman, Stephen D. |
description | Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion up take are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H⁺ -ATPase also is a critical component. One proposed leak, that of Na⁺ influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na⁺ and Cl⁻ concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. This modelling approach will inform experimentation and allow a quantitative assess ment of the energy costs of Na Cl tolerance to guide breeding and engineering of molecular components. |
doi_str_mv | 10.1111/nph.15864 |
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D. ; Kronzucker, Herbert J. ; Miklavcic, Stanley J. ; Plett, Darren ; Roy, Stuart J. ; Shabala, Sergey ; Shelden, Megan C. ; Soole, Kathleen L. ; Taylor, Nicolas L. ; Tester, Mark ; Wege, Stefanie ; Wegner, Lars H. ; Tyerman, Stephen D.</creator><creatorcontrib>Munns, Rana ; Day, David A. ; Fricke, Wieland ; Watt, Michelle ; Arsova, Borjana ; Barkla, Bronwyn J. ; Bose, Jayakumar ; Byrt, Caitlin S. ; Chen, Zhong-Hua ; Foster, Kylie J. ; Gilliham, Matthew ; Henderson, Sam W. ; Jenkins, Colin L. D. ; Kronzucker, Herbert J. ; Miklavcic, Stanley J. ; Plett, Darren ; Roy, Stuart J. ; Shabala, Sergey ; Shelden, Megan C. ; Soole, Kathleen L. ; Taylor, Nicolas L. ; Tester, Mark ; Wege, Stefanie ; Wegner, Lars H. ; Tyerman, Stephen D.</creatorcontrib><description>Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion up take are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H⁺ -ATPase also is a critical component. One proposed leak, that of Na⁺ influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na⁺ and Cl⁻ concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. This modelling approach will inform experimentation and allow a quantitative assess ment of the energy costs of Na Cl tolerance to guide breeding and engineering of molecular components.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.15864</identifier><identifier>PMID: 31004496</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Agricultural economics ; barley and wheat ; Biological Transport ; Breeding ; Cations ; Cell Respiration ; Channels ; Chloroplasts ; Computer architecture ; Cost assessments ; Costs ; Coupling (molecular) ; Critical components ; Crops, Agricultural - physiology ; Energy ; Energy conservation ; Energy costs ; Energy efficiency ; Energy Metabolism ; Energy requirements ; Experimentation ; Ion channels ; Leaves ; membrane transport ; Membranes ; Mitochondria ; Modelling ; photosynthesis ; Plant Roots - anatomy & histology ; respiration ; root anatomy ; Salinity ; Salinity effects ; Salinity tolerance ; Salt tolerance ; Salt Tolerance - physiology ; Sodium ; sodium and chloride transport ; Sodium chloride ; Tansley review ; Uptake ; Vacuoles ; Water flow</subject><ispartof>The New phytologist, 2020-02, Vol.225 (3), p.1072-1090</ispartof><rights>2019 The Authors © 2019 New Phytologist Trust</rights><rights>2019 The Authors. New Phytologist © 2019 New Phytologist Trust</rights><rights>2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</rights><rights>Copyright © 2020 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4764-9445c49f7a71a8e2ede79438fe3d30b56f125d264397c18ca2e6d00e3b61a9213</citedby><cites>FETCH-LOGICAL-c4764-9445c49f7a71a8e2ede79438fe3d30b56f125d264397c18ca2e6d00e3b61a9213</cites><orcidid>0000-0002-9347-8948 ; 0000-0002-4691-8023 ; 0000-0003-0666-3078 ; 0000-0002-7232-5889 ; 0000-0001-8549-2873 ; 0000-0003-2004-5217 ; 0000-0002-7203-3763 ; 0000-0003-0411-9431 ; 0000-0002-9358-0029 ; 0000-0001-7967-2173 ; 0000-0002-0566-2009 ; 0000-0003-2345-8981 ; 0000-0002-9551-8755 ; 0000-0003-2455-1643 ; 0000-0002-9263-8436 ; 0000-0002-0565-2951 ; 0000-0002-1514-1389 ; 0000-0001-7843-0957 ; 0000-0003-2651-3915 ; 0000-0003-3019-1891 ; 0000-0002-5085-8801 ; 0000-0002-8837-3404 ; 0000-0002-7531-320X ; 0000-0002-2361-246X ; 0000-0002-7519-2698</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26928245$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26928245$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,777,781,800,1412,1428,27905,27906,45555,45556,46390,46814,57998,58231</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31004496$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Munns, Rana</creatorcontrib><creatorcontrib>Day, David A.</creatorcontrib><creatorcontrib>Fricke, Wieland</creatorcontrib><creatorcontrib>Watt, Michelle</creatorcontrib><creatorcontrib>Arsova, Borjana</creatorcontrib><creatorcontrib>Barkla, Bronwyn J.</creatorcontrib><creatorcontrib>Bose, Jayakumar</creatorcontrib><creatorcontrib>Byrt, Caitlin S.</creatorcontrib><creatorcontrib>Chen, Zhong-Hua</creatorcontrib><creatorcontrib>Foster, Kylie J.</creatorcontrib><creatorcontrib>Gilliham, Matthew</creatorcontrib><creatorcontrib>Henderson, Sam W.</creatorcontrib><creatorcontrib>Jenkins, Colin L. D.</creatorcontrib><creatorcontrib>Kronzucker, Herbert J.</creatorcontrib><creatorcontrib>Miklavcic, Stanley J.</creatorcontrib><creatorcontrib>Plett, Darren</creatorcontrib><creatorcontrib>Roy, Stuart J.</creatorcontrib><creatorcontrib>Shabala, Sergey</creatorcontrib><creatorcontrib>Shelden, Megan C.</creatorcontrib><creatorcontrib>Soole, Kathleen L.</creatorcontrib><creatorcontrib>Taylor, Nicolas L.</creatorcontrib><creatorcontrib>Tester, Mark</creatorcontrib><creatorcontrib>Wege, Stefanie</creatorcontrib><creatorcontrib>Wegner, Lars H.</creatorcontrib><creatorcontrib>Tyerman, Stephen D.</creatorcontrib><title>Energy costs of salt tolerance in crop plants</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion up take are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H⁺ -ATPase also is a critical component. One proposed leak, that of Na⁺ influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na⁺ and Cl⁻ concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. This modelling approach will inform experimentation and allow a quantitative assess ment of the energy costs of Na Cl tolerance to guide breeding and engineering of molecular components.</description><subject>Agricultural economics</subject><subject>barley and wheat</subject><subject>Biological Transport</subject><subject>Breeding</subject><subject>Cations</subject><subject>Cell Respiration</subject><subject>Channels</subject><subject>Chloroplasts</subject><subject>Computer architecture</subject><subject>Cost assessments</subject><subject>Costs</subject><subject>Coupling (molecular)</subject><subject>Critical components</subject><subject>Crops, Agricultural - physiology</subject><subject>Energy</subject><subject>Energy conservation</subject><subject>Energy costs</subject><subject>Energy efficiency</subject><subject>Energy Metabolism</subject><subject>Energy requirements</subject><subject>Experimentation</subject><subject>Ion channels</subject><subject>Leaves</subject><subject>membrane transport</subject><subject>Membranes</subject><subject>Mitochondria</subject><subject>Modelling</subject><subject>photosynthesis</subject><subject>Plant Roots - anatomy & histology</subject><subject>respiration</subject><subject>root anatomy</subject><subject>Salinity</subject><subject>Salinity effects</subject><subject>Salinity tolerance</subject><subject>Salt tolerance</subject><subject>Salt Tolerance - physiology</subject><subject>Sodium</subject><subject>sodium and chloride transport</subject><subject>Sodium chloride</subject><subject>Tansley review</subject><subject>Uptake</subject><subject>Vacuoles</subject><subject>Water flow</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kE1PAjEURRujEUQX_gBNE1cuBvr9sTQExYSoC03cNaXTUcgwHdshhH_v4AA73-Ztzj3v5QJwjdEQtzOq6u8h5kqwE9DHTOhMYSpPQR8hojLBxGcPXKS0RAhpLsg56FGMEGNa9EE2qXz82kIXUpNgKGCyZQObUPpoK-fhooIuhhrWpa2adAnOClsmf7XfA_DxOHkfT7PZ69Pz-GGWOSYFyzRj3DFdSCuxVZ743EvNqCo8zSmac1FgwnMiGNXSYeUs8SJHyNO5wFYTTAfgrvPWMfysfWrMMqxj1Z40hFIsMad6R913VPthStEXpo6LlY1bg5HZFWPaYsxfMS17uzeu5yufH8lDEy0w6oDNovTb_03m5W16UN50iWVqQjwmiNBEEcbpL7pOdA4</recordid><startdate>202002</startdate><enddate>202002</enddate><creator>Munns, Rana</creator><creator>Day, David A.</creator><creator>Fricke, Wieland</creator><creator>Watt, Michelle</creator><creator>Arsova, Borjana</creator><creator>Barkla, Bronwyn J.</creator><creator>Bose, Jayakumar</creator><creator>Byrt, Caitlin S.</creator><creator>Chen, Zhong-Hua</creator><creator>Foster, Kylie J.</creator><creator>Gilliham, Matthew</creator><creator>Henderson, Sam W.</creator><creator>Jenkins, Colin L. 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D. ; Kronzucker, Herbert J. ; Miklavcic, Stanley J. ; Plett, Darren ; Roy, Stuart J. ; Shabala, Sergey ; Shelden, Megan C. ; Soole, Kathleen L. ; Taylor, Nicolas L. ; Tester, Mark ; Wege, Stefanie ; Wegner, Lars H. ; Tyerman, Stephen D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4764-9445c49f7a71a8e2ede79438fe3d30b56f125d264397c18ca2e6d00e3b61a9213</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Agricultural economics</topic><topic>barley and wheat</topic><topic>Biological Transport</topic><topic>Breeding</topic><topic>Cations</topic><topic>Cell Respiration</topic><topic>Channels</topic><topic>Chloroplasts</topic><topic>Computer architecture</topic><topic>Cost assessments</topic><topic>Costs</topic><topic>Coupling (molecular)</topic><topic>Critical components</topic><topic>Crops, Agricultural - physiology</topic><topic>Energy</topic><topic>Energy conservation</topic><topic>Energy costs</topic><topic>Energy efficiency</topic><topic>Energy Metabolism</topic><topic>Energy requirements</topic><topic>Experimentation</topic><topic>Ion channels</topic><topic>Leaves</topic><topic>membrane transport</topic><topic>Membranes</topic><topic>Mitochondria</topic><topic>Modelling</topic><topic>photosynthesis</topic><topic>Plant Roots - anatomy & histology</topic><topic>respiration</topic><topic>root anatomy</topic><topic>Salinity</topic><topic>Salinity effects</topic><topic>Salinity tolerance</topic><topic>Salt tolerance</topic><topic>Salt Tolerance - physiology</topic><topic>Sodium</topic><topic>sodium and chloride transport</topic><topic>Sodium chloride</topic><topic>Tansley review</topic><topic>Uptake</topic><topic>Vacuoles</topic><topic>Water flow</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Munns, Rana</creatorcontrib><creatorcontrib>Day, David A.</creatorcontrib><creatorcontrib>Fricke, Wieland</creatorcontrib><creatorcontrib>Watt, Michelle</creatorcontrib><creatorcontrib>Arsova, Borjana</creatorcontrib><creatorcontrib>Barkla, Bronwyn J.</creatorcontrib><creatorcontrib>Bose, Jayakumar</creatorcontrib><creatorcontrib>Byrt, Caitlin S.</creatorcontrib><creatorcontrib>Chen, Zhong-Hua</creatorcontrib><creatorcontrib>Foster, Kylie J.</creatorcontrib><creatorcontrib>Gilliham, Matthew</creatorcontrib><creatorcontrib>Henderson, Sam W.</creatorcontrib><creatorcontrib>Jenkins, Colin L. 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Different sources of energy, and modifications of root system architecture that would maximize water vs ion up take are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H⁺ -ATPase also is a critical component. One proposed leak, that of Na⁺ influx across the plasma membrane through certain aquaporin channels, might be coupled to water flow, thus conserving energy. For the tonoplast, control of two types of cation channels is required for energy efficiency. Transporters controlling the Na⁺ and Cl⁻ concentrations in mitochondria and chloroplasts are largely unknown and could be a major energy cost. The complexity of the system will require a sophisticated modelling approach to identify critical transporters, apoplastic barriers and root structures. 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recordid | cdi_proquest_journals_2331715391 |
source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Jstor Complete Legacy; Wiley Free Content |
subjects | Agricultural economics barley and wheat Biological Transport Breeding Cations Cell Respiration Channels Chloroplasts Computer architecture Cost assessments Costs Coupling (molecular) Critical components Crops, Agricultural - physiology Energy Energy conservation Energy costs Energy efficiency Energy Metabolism Energy requirements Experimentation Ion channels Leaves membrane transport Membranes Mitochondria Modelling photosynthesis Plant Roots - anatomy & histology respiration root anatomy Salinity Salinity effects Salinity tolerance Salt tolerance Salt Tolerance - physiology Sodium sodium and chloride transport Sodium chloride Tansley review Uptake Vacuoles Water flow |
title | Energy costs of salt tolerance in crop plants |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-18T20%3A09%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Energy%20costs%20of%20salt%20tolerance%20in%20crop%20plants&rft.jtitle=The%20New%20phytologist&rft.au=Munns,%20Rana&rft.date=2020-02&rft.volume=225&rft.issue=3&rft.spage=1072&rft.epage=1090&rft.pages=1072-1090&rft.issn=0028-646X&rft.eissn=1469-8137&rft_id=info:doi/10.1111/nph.15864&rft_dat=%3Cjstor_proqu%3E26928245%3C/jstor_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2331715391&rft_id=info:pmid/31004496&rft_jstor_id=26928245&rfr_iscdi=true |