New insights into molecular targets of salt tolerance in sorghum leaves elicited by ammonium nutrition
This study investigated the proteome modulation and physiological responses of Sorghum bicolor plants grown in nutrient solutions containing nitrate (NO3−) or ammonium (NH4+) at 5.0 mM, and subjected to salinity with 75 mM NaCl for ten days. Salinity promoted significant reductions in leaf area, roo...
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Veröffentlicht in: | Plant physiology and biochemistry 2020-09, Vol.154, p.723-734 |
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creator | Oliveira, Francisco Dalton Barreto de Miranda, Rafael de Souza Araújo, Gyedre dos Santos Coelho, Daniel Gomes Lobo, Marina Duarte Pinto Paula-Marinho, Stelamaris de Oliveira Lopes, Lineker de Sousa Monteiro-Moreira, Ana Cristina Oliveira Carvalho, Humberto Henrique de Gomes-Filho, Enéas |
description | This study investigated the proteome modulation and physiological responses of Sorghum bicolor plants grown in nutrient solutions containing nitrate (NO3−) or ammonium (NH4+) at 5.0 mM, and subjected to salinity with 75 mM NaCl for ten days. Salinity promoted significant reductions in leaf area, root and shoot dry mass of sorghum plants, regardless of nitrogen source; however, higher growth was observed in ammonium-grown plants. The better performance of ammonium-fed stressed plants was associated with low hydrogen peroxide accumulation, and improved CO2 assimilation and K+/Na+ homeostasis under salinity. Proteomic study revealed a nitrogen source-induced differential modulation in proteins related to photosynthesis/carbon metabolism, energy metabolism, response to stress and other cellular processes. Nitrate-fed plants induced thylakoidal electron transport chain proteins and structural and carbon assimilation enzymes, but these mechanisms seemed to be insufficient to mitigate salt damage in photosynthetic performance. In contrast, the greater tolerance to salinity of ammonium-grown plants may have arisen from: i.) de novo synthesis or upregulation of enzymes from photosynthetic/carbon metabolism, which resulted in better CO2 assimilation rates under NaCl-stress; ii.) activation of proteins involved in energy metabolism which made available energy for salt responses, most likely by proton pumps and Na+/H+ antiporters; and iii.) reprogramming of proteins involved in response to stress and other metabolic processes, constituting intricate pathways of salt responses. Overall, our findings not only provide new insights of molecular basis of salt tolerance in sorghum plants induced by ammonium nutrition, but also give new perspectives to develop biotechnological strategies to generate more salt-tolerant crops.
•Forage sorghum plants display contrasting responses against salinity under different nitrogen sources.•Ammonium nutrition mitigates salt damage in photosynthetic machinery of sorghum plants by modulating structural and carbon assimilation pathways.•Nitrate-fed sorghum plants failed to activate the intricate defense mechanisms and display elevated sensibility to salt stress. |
doi_str_mv | 10.1016/j.plaphy.2020.06.051 |
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•Forage sorghum plants display contrasting responses against salinity under different nitrogen sources.•Ammonium nutrition mitigates salt damage in photosynthetic machinery of sorghum plants by modulating structural and carbon assimilation pathways.•Nitrate-fed sorghum plants failed to activate the intricate defense mechanisms and display elevated sensibility to salt stress.</description><identifier>ISSN: 0981-9428</identifier><identifier>EISSN: 1873-2690</identifier><identifier>DOI: 10.1016/j.plaphy.2020.06.051</identifier><identifier>PMID: 32763797</identifier><language>eng</language><publisher>France: Elsevier Masson SAS</publisher><subject>Ammonium Compounds ; Nitrogen sources ; Plant Leaves ; Proteomics ; Salinity ; Salt stress ; Salt Tolerance ; Sorghum - physiology ; Sorghum bicolor</subject><ispartof>Plant physiology and biochemistry, 2020-09, Vol.154, p.723-734</ispartof><rights>2020</rights><rights>Copyright © 2020. Published by Elsevier Masson SAS.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c362t-a9c175875403a678272c81b299749c7f6911ec76a1eae11830a9332502e4cdb93</citedby><cites>FETCH-LOGICAL-c362t-a9c175875403a678272c81b299749c7f6911ec76a1eae11830a9332502e4cdb93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.plaphy.2020.06.051$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32763797$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Oliveira, Francisco Dalton Barreto de</creatorcontrib><creatorcontrib>Miranda, Rafael de Souza</creatorcontrib><creatorcontrib>Araújo, Gyedre dos Santos</creatorcontrib><creatorcontrib>Coelho, Daniel Gomes</creatorcontrib><creatorcontrib>Lobo, Marina Duarte Pinto</creatorcontrib><creatorcontrib>Paula-Marinho, Stelamaris de Oliveira</creatorcontrib><creatorcontrib>Lopes, Lineker de Sousa</creatorcontrib><creatorcontrib>Monteiro-Moreira, Ana Cristina Oliveira</creatorcontrib><creatorcontrib>Carvalho, Humberto Henrique de</creatorcontrib><creatorcontrib>Gomes-Filho, Enéas</creatorcontrib><title>New insights into molecular targets of salt tolerance in sorghum leaves elicited by ammonium nutrition</title><title>Plant physiology and biochemistry</title><addtitle>Plant Physiol Biochem</addtitle><description>This study investigated the proteome modulation and physiological responses of Sorghum bicolor plants grown in nutrient solutions containing nitrate (NO3−) or ammonium (NH4+) at 5.0 mM, and subjected to salinity with 75 mM NaCl for ten days. Salinity promoted significant reductions in leaf area, root and shoot dry mass of sorghum plants, regardless of nitrogen source; however, higher growth was observed in ammonium-grown plants. The better performance of ammonium-fed stressed plants was associated with low hydrogen peroxide accumulation, and improved CO2 assimilation and K+/Na+ homeostasis under salinity. Proteomic study revealed a nitrogen source-induced differential modulation in proteins related to photosynthesis/carbon metabolism, energy metabolism, response to stress and other cellular processes. Nitrate-fed plants induced thylakoidal electron transport chain proteins and structural and carbon assimilation enzymes, but these mechanisms seemed to be insufficient to mitigate salt damage in photosynthetic performance. In contrast, the greater tolerance to salinity of ammonium-grown plants may have arisen from: i.) de novo synthesis or upregulation of enzymes from photosynthetic/carbon metabolism, which resulted in better CO2 assimilation rates under NaCl-stress; ii.) activation of proteins involved in energy metabolism which made available energy for salt responses, most likely by proton pumps and Na+/H+ antiporters; and iii.) reprogramming of proteins involved in response to stress and other metabolic processes, constituting intricate pathways of salt responses. Overall, our findings not only provide new insights of molecular basis of salt tolerance in sorghum plants induced by ammonium nutrition, but also give new perspectives to develop biotechnological strategies to generate more salt-tolerant crops.
•Forage sorghum plants display contrasting responses against salinity under different nitrogen sources.•Ammonium nutrition mitigates salt damage in photosynthetic machinery of sorghum plants by modulating structural and carbon assimilation pathways.•Nitrate-fed sorghum plants failed to activate the intricate defense mechanisms and display elevated sensibility to salt stress.</description><subject>Ammonium Compounds</subject><subject>Nitrogen sources</subject><subject>Plant Leaves</subject><subject>Proteomics</subject><subject>Salinity</subject><subject>Salt stress</subject><subject>Salt Tolerance</subject><subject>Sorghum - physiology</subject><subject>Sorghum bicolor</subject><issn>0981-9428</issn><issn>1873-2690</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kEtrGzEQgEVpqJ2k_6AUHXvZrR5rPS6FEpI0YJJLchaydtaW0a5cSZvifx8Fuz32NMPMNzPMh9AXSlpKqPi-bw_BHnbHlhFGWiJasqIf0JIqyRsmNPmIlkQr2uiOqQW6zHlPCGGd5J_QgjMpuNRyiYZH-IP9lP12V3JNSsRjDODmYBMuNm2hluOAsw0Fl9pJdnJQQZxj2u7mEQewr5AxBO98gR5vjtiOY5x87U1zSb74OF2ji8GGDJ_P8Qq93N0-3_xq1k_3Dzc_143jgpXGakflSslVR7gVUjHJnKIbprXstJOD0JSCk8JSsECp4sRqztmKMOhcv9H8Cn077T2k-HuGXMzos4MQ7ARxzoZ1nCqqqpKKdifUpZhzgsEckh9tOhpKzLthszcnw-bdsCHCVMN17Ov5wrwZof839FdpBX6cAKh_vnpIJjsPVVrvE7hi-uj_f-ENVnWPUw</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Oliveira, Francisco Dalton Barreto de</creator><creator>Miranda, Rafael de Souza</creator><creator>Araújo, Gyedre dos Santos</creator><creator>Coelho, Daniel Gomes</creator><creator>Lobo, Marina Duarte Pinto</creator><creator>Paula-Marinho, Stelamaris de Oliveira</creator><creator>Lopes, Lineker de Sousa</creator><creator>Monteiro-Moreira, Ana Cristina Oliveira</creator><creator>Carvalho, Humberto Henrique de</creator><creator>Gomes-Filho, Enéas</creator><general>Elsevier Masson SAS</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>7X8</scope></search><sort><creationdate>202009</creationdate><title>New insights into molecular targets of salt tolerance in sorghum leaves elicited by ammonium nutrition</title><author>Oliveira, Francisco Dalton Barreto de ; Miranda, Rafael de Souza ; Araújo, Gyedre dos Santos ; Coelho, Daniel Gomes ; Lobo, Marina Duarte Pinto ; Paula-Marinho, Stelamaris de Oliveira ; Lopes, Lineker de Sousa ; Monteiro-Moreira, Ana Cristina Oliveira ; Carvalho, Humberto Henrique de ; Gomes-Filho, Enéas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c362t-a9c175875403a678272c81b299749c7f6911ec76a1eae11830a9332502e4cdb93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Ammonium Compounds</topic><topic>Nitrogen sources</topic><topic>Plant Leaves</topic><topic>Proteomics</topic><topic>Salinity</topic><topic>Salt stress</topic><topic>Salt Tolerance</topic><topic>Sorghum - physiology</topic><topic>Sorghum bicolor</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oliveira, Francisco Dalton Barreto de</creatorcontrib><creatorcontrib>Miranda, Rafael de Souza</creatorcontrib><creatorcontrib>Araújo, Gyedre dos Santos</creatorcontrib><creatorcontrib>Coelho, Daniel Gomes</creatorcontrib><creatorcontrib>Lobo, Marina Duarte Pinto</creatorcontrib><creatorcontrib>Paula-Marinho, Stelamaris de Oliveira</creatorcontrib><creatorcontrib>Lopes, Lineker de Sousa</creatorcontrib><creatorcontrib>Monteiro-Moreira, Ana Cristina Oliveira</creatorcontrib><creatorcontrib>Carvalho, Humberto Henrique de</creatorcontrib><creatorcontrib>Gomes-Filho, Enéas</creatorcontrib><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>Oliveira, Francisco Dalton Barreto de</au><au>Miranda, Rafael de Souza</au><au>Araújo, Gyedre dos Santos</au><au>Coelho, Daniel Gomes</au><au>Lobo, Marina Duarte Pinto</au><au>Paula-Marinho, Stelamaris de Oliveira</au><au>Lopes, Lineker de Sousa</au><au>Monteiro-Moreira, Ana Cristina Oliveira</au><au>Carvalho, Humberto Henrique de</au><au>Gomes-Filho, Enéas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>New insights into molecular targets of salt tolerance in sorghum leaves elicited by ammonium nutrition</atitle><jtitle>Plant physiology and biochemistry</jtitle><addtitle>Plant Physiol Biochem</addtitle><date>2020-09</date><risdate>2020</risdate><volume>154</volume><spage>723</spage><epage>734</epage><pages>723-734</pages><issn>0981-9428</issn><eissn>1873-2690</eissn><abstract>This study investigated the proteome modulation and physiological responses of Sorghum bicolor plants grown in nutrient solutions containing nitrate (NO3−) or ammonium (NH4+) at 5.0 mM, and subjected to salinity with 75 mM NaCl for ten days. Salinity promoted significant reductions in leaf area, root and shoot dry mass of sorghum plants, regardless of nitrogen source; however, higher growth was observed in ammonium-grown plants. The better performance of ammonium-fed stressed plants was associated with low hydrogen peroxide accumulation, and improved CO2 assimilation and K+/Na+ homeostasis under salinity. Proteomic study revealed a nitrogen source-induced differential modulation in proteins related to photosynthesis/carbon metabolism, energy metabolism, response to stress and other cellular processes. Nitrate-fed plants induced thylakoidal electron transport chain proteins and structural and carbon assimilation enzymes, but these mechanisms seemed to be insufficient to mitigate salt damage in photosynthetic performance. In contrast, the greater tolerance to salinity of ammonium-grown plants may have arisen from: i.) de novo synthesis or upregulation of enzymes from photosynthetic/carbon metabolism, which resulted in better CO2 assimilation rates under NaCl-stress; ii.) activation of proteins involved in energy metabolism which made available energy for salt responses, most likely by proton pumps and Na+/H+ antiporters; and iii.) reprogramming of proteins involved in response to stress and other metabolic processes, constituting intricate pathways of salt responses. Overall, our findings not only provide new insights of molecular basis of salt tolerance in sorghum plants induced by ammonium nutrition, but also give new perspectives to develop biotechnological strategies to generate more salt-tolerant crops.
•Forage sorghum plants display contrasting responses against salinity under different nitrogen sources.•Ammonium nutrition mitigates salt damage in photosynthetic machinery of sorghum plants by modulating structural and carbon assimilation pathways.•Nitrate-fed sorghum plants failed to activate the intricate defense mechanisms and display elevated sensibility to salt stress.</abstract><cop>France</cop><pub>Elsevier Masson SAS</pub><pmid>32763797</pmid><doi>10.1016/j.plaphy.2020.06.051</doi><tpages>12</tpages></addata></record> |
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subjects | Ammonium Compounds Nitrogen sources Plant Leaves Proteomics Salinity Salt stress Salt Tolerance Sorghum - physiology Sorghum bicolor |
title | New insights into molecular targets of salt tolerance in sorghum leaves elicited by ammonium nutrition |
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