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Nitrate modulates the physiological tolerance responses of the halophytic species Sarcocornia fruticosa to copper excess
Coexistence impact of pollutants of different nature on halophytes tolerance to metal excess has not been thoroughly examined, and plant functional responses described so far do not follow a clear pattern. Using the Cu-tolerant halophyte Sarcocornia fruticosa as a model species, we conducted a green...
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Published in: | Plant physiology and biochemistry 2024-05, Vol.210, p.108569-108569, Article 108569 |
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creator | Valle-Romero, Pedro Castellanos, Eloy Manuel Luque, Carlos J. Flores-Duarte, Noris J. Romano-Rodríguez, Elena Redondo-Gómez, Susana Rodríguez-Llorente, Ignacio D. Pajuelo, Eloísa Mateos-Naranjo, Enrique |
description | Coexistence impact of pollutants of different nature on halophytes tolerance to metal excess has not been thoroughly examined, and plant functional responses described so far do not follow a clear pattern. Using the Cu-tolerant halophyte Sarcocornia fruticosa as a model species, we conducted a greenhouse experiment to evaluate the impact of two concentration of copper (0 and 12 mM CuSO4) in combination with three nitrate levels (2, 14 and 50 mM KNO3) on plant growth, photosynthetic apparatus performance and ROS-scavenging enzymes system. The results revealed that S. fruticosa was able to grow adequately even when exposed to high concentrations of copper and nitrate. This response was linked to the plant capacity to uptake and retain a large amount of copper in its roots (up to 1500 mg kg−1 Cu), preventing its transport to aerial parts. This control of translocation was further magnified with nitrate concentration increment. Likewise, although Cu excess impaired S. fruticosa carbon assimilation capacity, the plant was able to downregulate its light-harvesting complexes function, as indicated its lowers ETR values, especially at 12 mM Cu + 50 mM NO3. This downregulation would contribute to avoid excess energy absorption and transformation. In addition, this strategy of avoiding excess energy was accompanied by the upregulation of all ROS-scavenging enzymes, a response that was further enhanced by the increase in nitrate concentration. Therefore, we conclude that the coexistence of nitrate would favor S. fruticosa tolerance to copper excess, and this effect is mediated by the combined activation of several tolerance mechanisms.
•Role of nitrate on the Cu tolerance of the halophytic S. fruticosa remain unknown.•Nitrate reduces Cu excess impact on photosynthetic apparatus yield under Cu stress.•Nitrate had a positive effect on photosystem light harvest energy efficiency.•Nitrate contribute to maintain plant water use efficiency.•Enzyme oxidative machinery was modulated by nitrate presence. |
doi_str_mv | 10.1016/j.plaphy.2024.108569 |
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•Role of nitrate on the Cu tolerance of the halophytic S. fruticosa remain unknown.•Nitrate reduces Cu excess impact on photosynthetic apparatus yield under Cu stress.•Nitrate had a positive effect on photosystem light harvest energy efficiency.•Nitrate contribute to maintain plant water use efficiency.•Enzyme oxidative machinery was modulated by nitrate presence.</description><identifier>ISSN: 0981-9428</identifier><identifier>EISSN: 1873-2690</identifier><identifier>DOI: 10.1016/j.plaphy.2024.108569</identifier><identifier>PMID: 38552261</identifier><language>eng</language><publisher>France: Elsevier Masson SAS</publisher><subject>Aizoaceae - drug effects ; Aizoaceae - metabolism ; Aizoaceae - physiology ; Antioxidant activity ; Copper ; Copper - metabolism ; Copper - toxicity ; Halophyte ; Nitrate ; Nitrates - metabolism ; Nitrates - pharmacology ; Photosynthesis ; Photosynthesis - drug effects ; Plant Roots - drug effects ; Plant Roots - metabolism ; Reactive Oxygen Species - metabolism ; Salt-Tolerant Plants - drug effects ; Salt-Tolerant Plants - metabolism ; Sarcocornia fruticosa ; Stress tolerance</subject><ispartof>Plant physiology and biochemistry, 2024-05, Vol.210, p.108569-108569, Article 108569</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier Masson SAS.. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c357t-ef50c275652560241f90ff0776014f1e440e645d24feccc8398bf67cb87ebac23</cites><orcidid>0000-0003-0417-5740 ; 0000-0002-8887-5033 ; 0000-0002-5280-9325 ; 0009-0004-2158-3249 ; 0000-0002-3234-8840</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38552261$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Valle-Romero, Pedro</creatorcontrib><creatorcontrib>Castellanos, Eloy Manuel</creatorcontrib><creatorcontrib>Luque, Carlos J.</creatorcontrib><creatorcontrib>Flores-Duarte, Noris J.</creatorcontrib><creatorcontrib>Romano-Rodríguez, Elena</creatorcontrib><creatorcontrib>Redondo-Gómez, Susana</creatorcontrib><creatorcontrib>Rodríguez-Llorente, Ignacio D.</creatorcontrib><creatorcontrib>Pajuelo, Eloísa</creatorcontrib><creatorcontrib>Mateos-Naranjo, Enrique</creatorcontrib><title>Nitrate modulates the physiological tolerance responses of the halophytic species Sarcocornia fruticosa to copper excess</title><title>Plant physiology and biochemistry</title><addtitle>Plant Physiol Biochem</addtitle><description>Coexistence impact of pollutants of different nature on halophytes tolerance to metal excess has not been thoroughly examined, and plant functional responses described so far do not follow a clear pattern. Using the Cu-tolerant halophyte Sarcocornia fruticosa as a model species, we conducted a greenhouse experiment to evaluate the impact of two concentration of copper (0 and 12 mM CuSO4) in combination with three nitrate levels (2, 14 and 50 mM KNO3) on plant growth, photosynthetic apparatus performance and ROS-scavenging enzymes system. The results revealed that S. fruticosa was able to grow adequately even when exposed to high concentrations of copper and nitrate. This response was linked to the plant capacity to uptake and retain a large amount of copper in its roots (up to 1500 mg kg−1 Cu), preventing its transport to aerial parts. This control of translocation was further magnified with nitrate concentration increment. Likewise, although Cu excess impaired S. fruticosa carbon assimilation capacity, the plant was able to downregulate its light-harvesting complexes function, as indicated its lowers ETR values, especially at 12 mM Cu + 50 mM NO3. This downregulation would contribute to avoid excess energy absorption and transformation. In addition, this strategy of avoiding excess energy was accompanied by the upregulation of all ROS-scavenging enzymes, a response that was further enhanced by the increase in nitrate concentration. Therefore, we conclude that the coexistence of nitrate would favor S. fruticosa tolerance to copper excess, and this effect is mediated by the combined activation of several tolerance mechanisms.
•Role of nitrate on the Cu tolerance of the halophytic S. fruticosa remain unknown.•Nitrate reduces Cu excess impact on photosynthetic apparatus yield under Cu stress.•Nitrate had a positive effect on photosystem light harvest energy efficiency.•Nitrate contribute to maintain plant water use efficiency.•Enzyme oxidative machinery was modulated by nitrate presence.</description><subject>Aizoaceae - drug effects</subject><subject>Aizoaceae - metabolism</subject><subject>Aizoaceae - physiology</subject><subject>Antioxidant activity</subject><subject>Copper</subject><subject>Copper - metabolism</subject><subject>Copper - toxicity</subject><subject>Halophyte</subject><subject>Nitrate</subject><subject>Nitrates - metabolism</subject><subject>Nitrates - pharmacology</subject><subject>Photosynthesis</subject><subject>Photosynthesis - drug effects</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - metabolism</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Salt-Tolerant Plants - drug effects</subject><subject>Salt-Tolerant Plants - metabolism</subject><subject>Sarcocornia fruticosa</subject><subject>Stress tolerance</subject><issn>0981-9428</issn><issn>1873-2690</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kMFO3DAQhq2qqGyBN0CVj71kazuxk1wqVYhSJNQegLPlnYxZr7zr1E4QvH0HQnvsyZbnm3_GH2PnUqylkObLbj1GN26f10qohp46bfp3bCW7tq6U6cV7thJ9J6u-Ud0x-1jKTggi2_oDO647rZUycsWefoYpuwn5Pg1zpEvh0xY55ZaQYnoI4CKfUsTsDoA8YxnToRCV_Cu4dTERPAXgZUQIVLl1GRKkfAiO-zxTKRVHGRzSOGLm-ARYyik78i4WPHs7T9j998u7ix_Vza-r64tvNxXUup0q9FqAarXRShtaX_peeC_a1gjZeIlNI9A0elCNRwDo6r7beNPCpmtx40DVJ-zzkjvm9HvGMtl9KIAxugOmudhaKEomUT2hzYJCTqVk9HbMYe_ys5XCvji3O7s4ty_O7eKc2j69TZg3exz-Nf2VTMDXBUD652PAbAuJIp1DyAiTHVL4_4Q_KXSXeA</recordid><startdate>202405</startdate><enddate>202405</enddate><creator>Valle-Romero, Pedro</creator><creator>Castellanos, Eloy Manuel</creator><creator>Luque, Carlos J.</creator><creator>Flores-Duarte, Noris J.</creator><creator>Romano-Rodríguez, Elena</creator><creator>Redondo-Gómez, Susana</creator><creator>Rodríguez-Llorente, Ignacio D.</creator><creator>Pajuelo, Eloísa</creator><creator>Mateos-Naranjo, Enrique</creator><general>Elsevier Masson SAS</general><scope>6I.</scope><scope>AAFTH</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><orcidid>https://orcid.org/0000-0003-0417-5740</orcidid><orcidid>https://orcid.org/0000-0002-8887-5033</orcidid><orcidid>https://orcid.org/0000-0002-5280-9325</orcidid><orcidid>https://orcid.org/0009-0004-2158-3249</orcidid><orcidid>https://orcid.org/0000-0002-3234-8840</orcidid></search><sort><creationdate>202405</creationdate><title>Nitrate modulates the physiological tolerance responses of the halophytic species Sarcocornia fruticosa to copper excess</title><author>Valle-Romero, Pedro ; Castellanos, Eloy Manuel ; Luque, Carlos J. ; Flores-Duarte, Noris J. ; Romano-Rodríguez, Elena ; Redondo-Gómez, Susana ; Rodríguez-Llorente, Ignacio D. ; Pajuelo, Eloísa ; Mateos-Naranjo, Enrique</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c357t-ef50c275652560241f90ff0776014f1e440e645d24feccc8398bf67cb87ebac23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aizoaceae - drug effects</topic><topic>Aizoaceae - metabolism</topic><topic>Aizoaceae - physiology</topic><topic>Antioxidant activity</topic><topic>Copper</topic><topic>Copper - metabolism</topic><topic>Copper - toxicity</topic><topic>Halophyte</topic><topic>Nitrate</topic><topic>Nitrates - metabolism</topic><topic>Nitrates - pharmacology</topic><topic>Photosynthesis</topic><topic>Photosynthesis - drug effects</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - metabolism</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Salt-Tolerant Plants - drug effects</topic><topic>Salt-Tolerant Plants - metabolism</topic><topic>Sarcocornia fruticosa</topic><topic>Stress tolerance</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Valle-Romero, Pedro</creatorcontrib><creatorcontrib>Castellanos, Eloy Manuel</creatorcontrib><creatorcontrib>Luque, Carlos J.</creatorcontrib><creatorcontrib>Flores-Duarte, Noris J.</creatorcontrib><creatorcontrib>Romano-Rodríguez, Elena</creatorcontrib><creatorcontrib>Redondo-Gómez, Susana</creatorcontrib><creatorcontrib>Rodríguez-Llorente, Ignacio D.</creatorcontrib><creatorcontrib>Pajuelo, Eloísa</creatorcontrib><creatorcontrib>Mateos-Naranjo, Enrique</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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><jtitle>Plant physiology and biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Valle-Romero, Pedro</au><au>Castellanos, Eloy Manuel</au><au>Luque, Carlos J.</au><au>Flores-Duarte, Noris J.</au><au>Romano-Rodríguez, Elena</au><au>Redondo-Gómez, Susana</au><au>Rodríguez-Llorente, Ignacio D.</au><au>Pajuelo, Eloísa</au><au>Mateos-Naranjo, Enrique</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nitrate modulates the physiological tolerance responses of the halophytic species Sarcocornia fruticosa to copper excess</atitle><jtitle>Plant physiology and biochemistry</jtitle><addtitle>Plant Physiol Biochem</addtitle><date>2024-05</date><risdate>2024</risdate><volume>210</volume><spage>108569</spage><epage>108569</epage><pages>108569-108569</pages><artnum>108569</artnum><issn>0981-9428</issn><eissn>1873-2690</eissn><abstract>Coexistence impact of pollutants of different nature on halophytes tolerance to metal excess has not been thoroughly examined, and plant functional responses described so far do not follow a clear pattern. Using the Cu-tolerant halophyte Sarcocornia fruticosa as a model species, we conducted a greenhouse experiment to evaluate the impact of two concentration of copper (0 and 12 mM CuSO4) in combination with three nitrate levels (2, 14 and 50 mM KNO3) on plant growth, photosynthetic apparatus performance and ROS-scavenging enzymes system. The results revealed that S. fruticosa was able to grow adequately even when exposed to high concentrations of copper and nitrate. This response was linked to the plant capacity to uptake and retain a large amount of copper in its roots (up to 1500 mg kg−1 Cu), preventing its transport to aerial parts. This control of translocation was further magnified with nitrate concentration increment. Likewise, although Cu excess impaired S. fruticosa carbon assimilation capacity, the plant was able to downregulate its light-harvesting complexes function, as indicated its lowers ETR values, especially at 12 mM Cu + 50 mM NO3. This downregulation would contribute to avoid excess energy absorption and transformation. In addition, this strategy of avoiding excess energy was accompanied by the upregulation of all ROS-scavenging enzymes, a response that was further enhanced by the increase in nitrate concentration. Therefore, we conclude that the coexistence of nitrate would favor S. fruticosa tolerance to copper excess, and this effect is mediated by the combined activation of several tolerance mechanisms.
•Role of nitrate on the Cu tolerance of the halophytic S. fruticosa remain unknown.•Nitrate reduces Cu excess impact on photosynthetic apparatus yield under Cu stress.•Nitrate had a positive effect on photosystem light harvest energy efficiency.•Nitrate contribute to maintain plant water use efficiency.•Enzyme oxidative machinery was modulated by nitrate presence.</abstract><cop>France</cop><pub>Elsevier Masson SAS</pub><pmid>38552261</pmid><doi>10.1016/j.plaphy.2024.108569</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-0417-5740</orcidid><orcidid>https://orcid.org/0000-0002-8887-5033</orcidid><orcidid>https://orcid.org/0000-0002-5280-9325</orcidid><orcidid>https://orcid.org/0009-0004-2158-3249</orcidid><orcidid>https://orcid.org/0000-0002-3234-8840</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aizoaceae - drug effects Aizoaceae - metabolism Aizoaceae - physiology Antioxidant activity Copper Copper - metabolism Copper - toxicity Halophyte Nitrate Nitrates - metabolism Nitrates - pharmacology Photosynthesis Photosynthesis - drug effects Plant Roots - drug effects Plant Roots - metabolism Reactive Oxygen Species - metabolism Salt-Tolerant Plants - drug effects Salt-Tolerant Plants - metabolism Sarcocornia fruticosa Stress tolerance |
title | Nitrate modulates the physiological tolerance responses of the halophytic species Sarcocornia fruticosa to copper excess |
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