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Nitric oxide alleviates programmed cell death induced by cadmium in Solanum lycopersicum seedlings through protein S-nitrosylation

Cadmium (Cd), as a non-essential and toxic heavy metal in plants, has deleterious effects on plant physiological and biochemical processes. Nitric oxide (NO) is one of the most important signaling molecules for plants to response diverse stresses. Here, we found that Cd-induced programmed cell death...

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Published in:The Science of the total environment 2024-06, Vol.931, p.172812-172812, Article 172812
Main Authors: Huang, Dengjing, Chen, Xinfang, Yun, Fahong, Fang, Hua, Wang, Chunlei, Liao, Weibiao
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Chen, Xinfang
Yun, Fahong
Fang, Hua
Wang, Chunlei
Liao, Weibiao
description Cadmium (Cd), as a non-essential and toxic heavy metal in plants, has deleterious effects on plant physiological and biochemical processes. Nitric oxide (NO) is one of the most important signaling molecules for plants to response diverse stresses. Here, we found that Cd-induced programmed cell death (PCD) was accompanied by NO bursts, which exacerbated cell death when NO was removed and vice versa. Proteomic analysis of S-nitrosylated proteins showed that the differential proteins in Cd-induced PCD and in NO-alleviated PCD mainly exist together in carbohydrate metabolism and amino acid metabolism, while some of the differential proteins exist alone in metabolism of cofactors and vitamins and lipid metabolism. Meanwhile, S-nitrosylation of proteins in porphyrin and chlorophyll metabolism and starch and sucrose metabolism could explain the leaf chlorosis induced by PCD. Moreover, protein transport protein SEC23, ubiquitinyl hydrolase 1 and pathogenesis-related protein 1 were identified to be S-nitrosylated in vivo, and their expressions were increased in Cd-induced PCD while decreased in NO treatment. Similar results were obtained in tomato seedlings with higher S-nitrosylation. Taken together, our results indicate that NO might be involved in the regulation of Cd-induced PCD through protein S-nitrosylation, especially proteins involved in PCD response. [Display omitted] •High concentrations of Cd induced PCD, while NO pretreatment mitigated this process.•NO alleviates Cd-induced PCD through protein S-nitrosylation (SNO).•Proteins in porphyrin and chlorophyll metabolism were SNOed and down-regulated.•Key proteins in starch and sucrose metabolism were SNOed and up-regulated in PCD.•The SNO of SEC23, ATXN3, and PR1 resulted in higher PCD response.
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Nitric oxide (NO) is one of the most important signaling molecules for plants to response diverse stresses. Here, we found that Cd-induced programmed cell death (PCD) was accompanied by NO bursts, which exacerbated cell death when NO was removed and vice versa. Proteomic analysis of S-nitrosylated proteins showed that the differential proteins in Cd-induced PCD and in NO-alleviated PCD mainly exist together in carbohydrate metabolism and amino acid metabolism, while some of the differential proteins exist alone in metabolism of cofactors and vitamins and lipid metabolism. Meanwhile, S-nitrosylation of proteins in porphyrin and chlorophyll metabolism and starch and sucrose metabolism could explain the leaf chlorosis induced by PCD. Moreover, protein transport protein SEC23, ubiquitinyl hydrolase 1 and pathogenesis-related protein 1 were identified to be S-nitrosylated in vivo, and their expressions were increased in Cd-induced PCD while decreased in NO treatment. Similar results were obtained in tomato seedlings with higher S-nitrosylation. Taken together, our results indicate that NO might be involved in the regulation of Cd-induced PCD through protein S-nitrosylation, especially proteins involved in PCD response. [Display omitted] •High concentrations of Cd induced PCD, while NO pretreatment mitigated this process.•NO alleviates Cd-induced PCD through protein S-nitrosylation (SNO).•Proteins in porphyrin and chlorophyll metabolism were SNOed and down-regulated.•Key proteins in starch and sucrose metabolism were SNOed and up-regulated in PCD.•The SNO of SEC23, ATXN3, and PR1 resulted in higher PCD response.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2024.172812</identifier><identifier>PMID: 38703854</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Apoptosis - drug effects ; Cadmium - toxicity ; Caspase-like 3/9 ; Mitogen-activated protein kinase ; Nitric Oxide - metabolism ; Pathogenesis-related protein 1 ; Photosynthesis ; Plant Proteins - metabolism ; S-nitrosoglutathione reductase ; Seedlings - drug effects ; Seedlings - metabolism ; Soil Pollutants - metabolism ; Soil Pollutants - toxicity ; Solanum lycopersicum - metabolism ; Ubiquitination cascade</subject><ispartof>The Science of the total environment, 2024-06, Vol.931, p.172812-172812, Article 172812</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. 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Nitric oxide (NO) is one of the most important signaling molecules for plants to response diverse stresses. Here, we found that Cd-induced programmed cell death (PCD) was accompanied by NO bursts, which exacerbated cell death when NO was removed and vice versa. Proteomic analysis of S-nitrosylated proteins showed that the differential proteins in Cd-induced PCD and in NO-alleviated PCD mainly exist together in carbohydrate metabolism and amino acid metabolism, while some of the differential proteins exist alone in metabolism of cofactors and vitamins and lipid metabolism. Meanwhile, S-nitrosylation of proteins in porphyrin and chlorophyll metabolism and starch and sucrose metabolism could explain the leaf chlorosis induced by PCD. Moreover, protein transport protein SEC23, ubiquitinyl hydrolase 1 and pathogenesis-related protein 1 were identified to be S-nitrosylated in vivo, and their expressions were increased in Cd-induced PCD while decreased in NO treatment. 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subjects Apoptosis - drug effects
Cadmium - toxicity
Caspase-like 3/9
Mitogen-activated protein kinase
Nitric Oxide - metabolism
Pathogenesis-related protein 1
Photosynthesis
Plant Proteins - metabolism
S-nitrosoglutathione reductase
Seedlings - drug effects
Seedlings - metabolism
Soil Pollutants - metabolism
Soil Pollutants - toxicity
Solanum lycopersicum - metabolism
Ubiquitination cascade
title Nitric oxide alleviates programmed cell death induced by cadmium in Solanum lycopersicum seedlings through protein S-nitrosylation
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