Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings
Despite numerous reports on the role of nitric oxide (NO) in regulating plants growth and mitigating different environmental stresses, its participation in sulfur (S) -metabolism remains largely unknown. Therefore, we studied the role of NO in S acquisition and S-assimilation in tomato seedlings und...
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description | Despite numerous reports on the role of nitric oxide (NO) in regulating plants growth and mitigating different environmental stresses, its participation in sulfur (S) -metabolism remains largely unknown. Therefore, we studied the role of NO in S acquisition and S-assimilation in tomato seedlings under low S-stress conditions by supplying NO to the leaves of S-sufficient and S-deficient seedlings. S-starved plants exhibited a substantial decreased in plant growth attributes, photosynthetic pigment chlorophyll (Chl) and other photosynthetic parameters, and activity of enzymes involved in Chl biosynthesis (δ-aminolevulinic acid dehydratase), and photosynthetic processes (carbonic anhydrase and RuBisco). Also, S-deficiency enhanced reactive oxygen species (ROS) (superoxide and hydrogen peroxide) and lipid peroxidation (malondialdehyde) levels in tomato seedlings. Contrarily, foliar supplementation of NO to S-deficient seedlings resulted in considerably reduced ROS formation in leaves and roots, which alleviated low S-stress-induced lipid peroxidation. However, exogenous NO enhanced proline accumulation by increasing proline metabolizing enzyme (Δ1-pyrroline-5-carboxylate synthetase) activity and also increased NO, hydrogen sulfide (a gasotransmitter small signaling molecule) and S uptake, and content of S-containing compounds (cysteine and reduced glutathione). Under S-limited conditions, NO improved S utilization efficiency of plants by upregulating the activity of S-assimilating enzymes (ATP sulfurylase, adenosine 5-phosphosulfate reductase, sulfide reductase and O-acetylserine (thiol) lyase). Under S-deprived conditions, improved S-assimilation of seedlings receiving NO resulted in improved redox homeostasis and ascorbate content through increased NO and S uptake. Application of 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy l-3-oxide (an NO scavenger) invalidated the effect of NO and again caused low S-stress-induced oxidative damage, confirming the beneficial role of NO in seedlings under S-deprived conditions. Thus, exogenous NO enhanced the tolerance of tomato seedlings to limit S-triggered oxidative stress and improved photosynthetic performance and S assimilation.
•Nitric oxide, a signaling molecule, alleviated oxidative damage induced by low-sulfur stress.•Nitric oxide and hydrogen sulfide enhanced growth and photosynthetic attributes of sulfur deficient-tomato seedlings.•Nitric oxide efficiently improved S utilization efficiency by upregul |
doi_str_mv | 10.1016/j.niox.2019.11.002 |
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•Nitric oxide, a signaling molecule, alleviated oxidative damage induced by low-sulfur stress.•Nitric oxide and hydrogen sulfide enhanced growth and photosynthetic attributes of sulfur deficient-tomato seedlings.•Nitric oxide efficiently improved S utilization efficiency by upregulating the activity of S-assimilating enzymes.•Nitric oxide and hydrogen sulfide coordinated each other and maintained redox state and ASC—GSH cycle.•NO functions as an upstream signaling biomolecule with another gaseous transmitter signaling molecule, hydrogen sulfide.</description><identifier>ISSN: 1089-8603</identifier><identifier>EISSN: 1089-8611</identifier><identifier>DOI: 10.1016/j.niox.2019.11.002</identifier><identifier>PMID: 31707015</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Hydrogen sulfide ; Lycopersicon esculentum - drug effects ; Lycopersicon esculentum - growth & development ; Lycopersicon esculentum - metabolism ; Nitric oxide ; Nitric Oxide - pharmacology ; Oxidative Stress - drug effects ; Photosynthesis ; Proline metabolism ; S-deficiency ; Seedlings - drug effects ; Seedlings - growth & development ; Seedlings - metabolism ; Sulfur - deficiency ; Sulfur - metabolism ; Sulfur assimilation</subject><ispartof>Nitric oxide, 2020-01, Vol.94, p.95-107</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c356t-bc74f4736d2c0144662e8e2dc7c37c107ab9ddb48ce63092c4d733a4adc7273b3</citedby><cites>FETCH-LOGICAL-c356t-bc74f4736d2c0144662e8e2dc7c37c107ab9ddb48ce63092c4d733a4adc7273b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1089860319302101$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31707015$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Siddiqui, Manzer H.</creatorcontrib><creatorcontrib>Alamri, Saud</creatorcontrib><creatorcontrib>Alsubaie, Qasi D.</creatorcontrib><creatorcontrib>Ali, Hayssam M.</creatorcontrib><creatorcontrib>Khan, M. Nasir</creatorcontrib><creatorcontrib>Al-Ghamdi, Abdullah</creatorcontrib><creatorcontrib>Ibrahim, Abdullah A.</creatorcontrib><creatorcontrib>Alsadon, Abdullah</creatorcontrib><title>Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings</title><title>Nitric oxide</title><addtitle>Nitric Oxide</addtitle><description>Despite numerous reports on the role of nitric oxide (NO) in regulating plants growth and mitigating different environmental stresses, its participation in sulfur (S) -metabolism remains largely unknown. Therefore, we studied the role of NO in S acquisition and S-assimilation in tomato seedlings under low S-stress conditions by supplying NO to the leaves of S-sufficient and S-deficient seedlings. S-starved plants exhibited a substantial decreased in plant growth attributes, photosynthetic pigment chlorophyll (Chl) and other photosynthetic parameters, and activity of enzymes involved in Chl biosynthesis (δ-aminolevulinic acid dehydratase), and photosynthetic processes (carbonic anhydrase and RuBisco). Also, S-deficiency enhanced reactive oxygen species (ROS) (superoxide and hydrogen peroxide) and lipid peroxidation (malondialdehyde) levels in tomato seedlings. Contrarily, foliar supplementation of NO to S-deficient seedlings resulted in considerably reduced ROS formation in leaves and roots, which alleviated low S-stress-induced lipid peroxidation. However, exogenous NO enhanced proline accumulation by increasing proline metabolizing enzyme (Δ1-pyrroline-5-carboxylate synthetase) activity and also increased NO, hydrogen sulfide (a gasotransmitter small signaling molecule) and S uptake, and content of S-containing compounds (cysteine and reduced glutathione). Under S-limited conditions, NO improved S utilization efficiency of plants by upregulating the activity of S-assimilating enzymes (ATP sulfurylase, adenosine 5-phosphosulfate reductase, sulfide reductase and O-acetylserine (thiol) lyase). Under S-deprived conditions, improved S-assimilation of seedlings receiving NO resulted in improved redox homeostasis and ascorbate content through increased NO and S uptake. Application of 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy l-3-oxide (an NO scavenger) invalidated the effect of NO and again caused low S-stress-induced oxidative damage, confirming the beneficial role of NO in seedlings under S-deprived conditions. Thus, exogenous NO enhanced the tolerance of tomato seedlings to limit S-triggered oxidative stress and improved photosynthetic performance and S assimilation.
•Nitric oxide, a signaling molecule, alleviated oxidative damage induced by low-sulfur stress.•Nitric oxide and hydrogen sulfide enhanced growth and photosynthetic attributes of sulfur deficient-tomato seedlings.•Nitric oxide efficiently improved S utilization efficiency by upregulating the activity of S-assimilating enzymes.•Nitric oxide and hydrogen sulfide coordinated each other and maintained redox state and ASC—GSH cycle.•NO functions as an upstream signaling biomolecule with another gaseous transmitter signaling molecule, hydrogen sulfide.</description><subject>Hydrogen sulfide</subject><subject>Lycopersicon esculentum - drug effects</subject><subject>Lycopersicon esculentum - growth & development</subject><subject>Lycopersicon esculentum - metabolism</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - pharmacology</subject><subject>Oxidative Stress - drug effects</subject><subject>Photosynthesis</subject><subject>Proline metabolism</subject><subject>S-deficiency</subject><subject>Seedlings - drug effects</subject><subject>Seedlings - growth & development</subject><subject>Seedlings - metabolism</subject><subject>Sulfur - deficiency</subject><subject>Sulfur - metabolism</subject><subject>Sulfur assimilation</subject><issn>1089-8603</issn><issn>1089-8611</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kD1PwzAURS0EolD4AwzII0uCn53aqcSCUPmQkFhgNo79UrlKYrCTqvx70hYYmd4bzr3SPYRcAMuBgbxe5Z0Pm5wzmOcAOWP8gJwAK-dZKQEO_34mJuQ0pRVjrBClPCYTAYopBrMT8r7YhCV2YUi08330loaNd0hN0-Damx4TTUNTD5E6rL312NmvzHdusOh2qOn9GqkzrVki9R3tQ2v6QBOia3y3TGfkqDZNwvOfOyVv94vXu8fs-eXh6e72ObNiJvussqqoCyWk45ZBUUjJsUTurLJCWWDKVHPnqqK0KAWbc1s4JYQpzEhwJSoxJVf73o8YPgdMvW59stg0psNxneYChJxxGG1MCd-jNoaUItb6I_rWxC8NTG_N6pXemtVbsxpAj2bH0OVP_1C16P4ivypH4GYP4Lhy7THqtNOFzke0vXbB_9f_Df4Xi-A</recordid><startdate>20200101</startdate><enddate>20200101</enddate><creator>Siddiqui, Manzer H.</creator><creator>Alamri, Saud</creator><creator>Alsubaie, Qasi D.</creator><creator>Ali, Hayssam M.</creator><creator>Khan, M. Nasir</creator><creator>Al-Ghamdi, Abdullah</creator><creator>Ibrahim, Abdullah A.</creator><creator>Alsadon, Abdullah</creator><general>Elsevier Inc</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>20200101</creationdate><title>Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings</title><author>Siddiqui, Manzer H. ; Alamri, Saud ; Alsubaie, Qasi D. ; Ali, Hayssam M. ; Khan, M. Nasir ; Al-Ghamdi, Abdullah ; Ibrahim, Abdullah A. ; Alsadon, Abdullah</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c356t-bc74f4736d2c0144662e8e2dc7c37c107ab9ddb48ce63092c4d733a4adc7273b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Hydrogen sulfide</topic><topic>Lycopersicon esculentum - drug effects</topic><topic>Lycopersicon esculentum - growth & development</topic><topic>Lycopersicon esculentum - metabolism</topic><topic>Nitric oxide</topic><topic>Nitric Oxide - pharmacology</topic><topic>Oxidative Stress - drug effects</topic><topic>Photosynthesis</topic><topic>Proline metabolism</topic><topic>S-deficiency</topic><topic>Seedlings - drug effects</topic><topic>Seedlings - growth & development</topic><topic>Seedlings - metabolism</topic><topic>Sulfur - deficiency</topic><topic>Sulfur - metabolism</topic><topic>Sulfur assimilation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Siddiqui, Manzer H.</creatorcontrib><creatorcontrib>Alamri, Saud</creatorcontrib><creatorcontrib>Alsubaie, Qasi D.</creatorcontrib><creatorcontrib>Ali, Hayssam M.</creatorcontrib><creatorcontrib>Khan, M. Nasir</creatorcontrib><creatorcontrib>Al-Ghamdi, Abdullah</creatorcontrib><creatorcontrib>Ibrahim, Abdullah A.</creatorcontrib><creatorcontrib>Alsadon, Abdullah</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>Nitric oxide</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Siddiqui, Manzer H.</au><au>Alamri, Saud</au><au>Alsubaie, Qasi D.</au><au>Ali, Hayssam M.</au><au>Khan, M. Nasir</au><au>Al-Ghamdi, Abdullah</au><au>Ibrahim, Abdullah A.</au><au>Alsadon, Abdullah</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings</atitle><jtitle>Nitric oxide</jtitle><addtitle>Nitric Oxide</addtitle><date>2020-01-01</date><risdate>2020</risdate><volume>94</volume><spage>95</spage><epage>107</epage><pages>95-107</pages><issn>1089-8603</issn><eissn>1089-8611</eissn><abstract>Despite numerous reports on the role of nitric oxide (NO) in regulating plants growth and mitigating different environmental stresses, its participation in sulfur (S) -metabolism remains largely unknown. Therefore, we studied the role of NO in S acquisition and S-assimilation in tomato seedlings under low S-stress conditions by supplying NO to the leaves of S-sufficient and S-deficient seedlings. S-starved plants exhibited a substantial decreased in plant growth attributes, photosynthetic pigment chlorophyll (Chl) and other photosynthetic parameters, and activity of enzymes involved in Chl biosynthesis (δ-aminolevulinic acid dehydratase), and photosynthetic processes (carbonic anhydrase and RuBisco). Also, S-deficiency enhanced reactive oxygen species (ROS) (superoxide and hydrogen peroxide) and lipid peroxidation (malondialdehyde) levels in tomato seedlings. Contrarily, foliar supplementation of NO to S-deficient seedlings resulted in considerably reduced ROS formation in leaves and roots, which alleviated low S-stress-induced lipid peroxidation. However, exogenous NO enhanced proline accumulation by increasing proline metabolizing enzyme (Δ1-pyrroline-5-carboxylate synthetase) activity and also increased NO, hydrogen sulfide (a gasotransmitter small signaling molecule) and S uptake, and content of S-containing compounds (cysteine and reduced glutathione). Under S-limited conditions, NO improved S utilization efficiency of plants by upregulating the activity of S-assimilating enzymes (ATP sulfurylase, adenosine 5-phosphosulfate reductase, sulfide reductase and O-acetylserine (thiol) lyase). Under S-deprived conditions, improved S-assimilation of seedlings receiving NO resulted in improved redox homeostasis and ascorbate content through increased NO and S uptake. Application of 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy l-3-oxide (an NO scavenger) invalidated the effect of NO and again caused low S-stress-induced oxidative damage, confirming the beneficial role of NO in seedlings under S-deprived conditions. Thus, exogenous NO enhanced the tolerance of tomato seedlings to limit S-triggered oxidative stress and improved photosynthetic performance and S assimilation.
•Nitric oxide, a signaling molecule, alleviated oxidative damage induced by low-sulfur stress.•Nitric oxide and hydrogen sulfide enhanced growth and photosynthetic attributes of sulfur deficient-tomato seedlings.•Nitric oxide efficiently improved S utilization efficiency by upregulating the activity of S-assimilating enzymes.•Nitric oxide and hydrogen sulfide coordinated each other and maintained redox state and ASC—GSH cycle.•NO functions as an upstream signaling biomolecule with another gaseous transmitter signaling molecule, hydrogen sulfide.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31707015</pmid><doi>10.1016/j.niox.2019.11.002</doi><tpages>13</tpages></addata></record> |
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subjects | Hydrogen sulfide Lycopersicon esculentum - drug effects Lycopersicon esculentum - growth & development Lycopersicon esculentum - metabolism Nitric oxide Nitric Oxide - pharmacology Oxidative Stress - drug effects Photosynthesis Proline metabolism S-deficiency Seedlings - drug effects Seedlings - growth & development Seedlings - metabolism Sulfur - deficiency Sulfur - metabolism Sulfur assimilation |
title | Exogenous nitric oxide alleviates sulfur deficiency-induced oxidative damage in tomato seedlings |
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