Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato
Tomato is the vegetable with the largest greenhouse area in China, and low temperature is one of the main factors affecting tomato growth, yield, and quality. Hydrogen sulfide (H<sub>2</sub>S) plays an important role in regulating plant chilling tolerance, but its downstream cascade reac...
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MDPI AG
2024-03-01
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| Series: | Antioxidants |
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| author | Guoxiu Wu Xuxu Niu Jiahui Chen Changjiang Wu Yang Li Yanman Li Dandan Cui Xueying He Fan Wang Shengli Li |
| author_facet | Guoxiu Wu Xuxu Niu Jiahui Chen Changjiang Wu Yang Li Yanman Li Dandan Cui Xueying He Fan Wang Shengli Li |
| author_sort | Guoxiu Wu |
| collection | DOAJ |
| description | Tomato is the vegetable with the largest greenhouse area in China, and low temperature is one of the main factors affecting tomato growth, yield, and quality. Hydrogen sulfide (H<sub>2</sub>S) plays an important role in regulating plant chilling tolerance, but its downstream cascade reaction and mechanism remain unclear. Mitogen-activated protein kinases (MAPK/MPKs) are closely related to a variety of signaling substances in stress signal transmission. However, whether H<sub>2</sub>S is related to the MPK cascade pathway in response to low-temperature stress is rarely reported. In this study, NaHS treatment significantly decreased the electrolyte leakage (EL), superoxide anion (O<sub>2</sub><sup>−</sup>) production rate, and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) content of seedlings at low temperatures. In addition, the activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were obviously increased; and the photochemical efficiency of PSII (Fv/Fm) was enhanced with treatment with NaHS, indicating that NaHS improved the seedlings’ cold tolerance by alleviating the degree of membrane lipid peroxidation and oxidative damage. However, H<sub>2</sub>S scavenger hypotaurine (HT) treatment showed the opposite effect. We found that H<sub>2</sub>S content, L-cysteine desulfhydrase (LCD) activity, and mRNA expression were increased by chilling stress but reduced by MPK inhibitor PD98059; PD98059 reversed the alleviating effect of H<sub>2</sub>S via increasing the EL and H<sub>2</sub>O<sub>2</sub> contents. The expression levels of <i>MPK1</i>–<i>MPK7</i> at low temperatures showed that <i>SlMPK4</i> was significantly induced by exogenous NaHS and showed a trend of first increasing and then decreasing, while the expression level of <i>SlMPK4</i> in HT-treated seedlings was lower than that of the control. After <i>SlMPK4</i> was silenced by virus-induced gene silencing, the H<sub>2</sub>S-induced upregulation of C-repeat-Binding Factor (CBF1), inducer of CBF expression 1 (ICE1), respiratory burst oxidase homologs (RBOH1, RBOH2) at low temperatures disappeared, and tomato cold tolerance decreased. In conclusion, H<sub>2</sub>S improves the cold tolerance of tomato plants by increasing the activity of antioxidant enzymes and reducing reactive oxygen species (ROS) accumulation and membrane lipid peroxidation. MPK4 may act as a downstream signaling molecule in this process. |
| first_indexed | 2024-04-24T18:37:14Z |
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| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-04-24T18:37:14Z |
| publishDate | 2024-03-01 |
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| series | Antioxidants |
| spelling | doaj.art-e54ddb7fd23643d9b3eb4083f1d113962024-03-27T13:18:34ZengMDPI AGAntioxidants2076-39212024-03-0113332310.3390/antiox13030323Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in TomatoGuoxiu Wu0Xuxu Niu1Jiahui Chen2Changjiang Wu3Yang Li4Yanman Li5Dandan Cui6Xueying He7Fan Wang8Shengli Li9College of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou 450046, ChinaTomato is the vegetable with the largest greenhouse area in China, and low temperature is one of the main factors affecting tomato growth, yield, and quality. Hydrogen sulfide (H<sub>2</sub>S) plays an important role in regulating plant chilling tolerance, but its downstream cascade reaction and mechanism remain unclear. Mitogen-activated protein kinases (MAPK/MPKs) are closely related to a variety of signaling substances in stress signal transmission. However, whether H<sub>2</sub>S is related to the MPK cascade pathway in response to low-temperature stress is rarely reported. In this study, NaHS treatment significantly decreased the electrolyte leakage (EL), superoxide anion (O<sub>2</sub><sup>−</sup>) production rate, and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) content of seedlings at low temperatures. In addition, the activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were obviously increased; and the photochemical efficiency of PSII (Fv/Fm) was enhanced with treatment with NaHS, indicating that NaHS improved the seedlings’ cold tolerance by alleviating the degree of membrane lipid peroxidation and oxidative damage. However, H<sub>2</sub>S scavenger hypotaurine (HT) treatment showed the opposite effect. We found that H<sub>2</sub>S content, L-cysteine desulfhydrase (LCD) activity, and mRNA expression were increased by chilling stress but reduced by MPK inhibitor PD98059; PD98059 reversed the alleviating effect of H<sub>2</sub>S via increasing the EL and H<sub>2</sub>O<sub>2</sub> contents. The expression levels of <i>MPK1</i>–<i>MPK7</i> at low temperatures showed that <i>SlMPK4</i> was significantly induced by exogenous NaHS and showed a trend of first increasing and then decreasing, while the expression level of <i>SlMPK4</i> in HT-treated seedlings was lower than that of the control. After <i>SlMPK4</i> was silenced by virus-induced gene silencing, the H<sub>2</sub>S-induced upregulation of C-repeat-Binding Factor (CBF1), inducer of CBF expression 1 (ICE1), respiratory burst oxidase homologs (RBOH1, RBOH2) at low temperatures disappeared, and tomato cold tolerance decreased. In conclusion, H<sub>2</sub>S improves the cold tolerance of tomato plants by increasing the activity of antioxidant enzymes and reducing reactive oxygen species (ROS) accumulation and membrane lipid peroxidation. MPK4 may act as a downstream signaling molecule in this process.https://www.mdpi.com/2076-3921/13/3/323tomatomitogen-activated protein kinaseschilling stressoxidative damage |
| spellingShingle | Guoxiu Wu Xuxu Niu Jiahui Chen Changjiang Wu Yang Li Yanman Li Dandan Cui Xueying He Fan Wang Shengli Li Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato Antioxidants tomato mitogen-activated protein kinases chilling stress oxidative damage |
| title | Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato |
| title_full | Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato |
| title_fullStr | Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato |
| title_full_unstemmed | Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato |
| title_short | Hydrogen Sulfide Alleviates Oxidative Damage under Chilling Stress through Mitogen-Activated Protein Kinase in Tomato |
| title_sort | hydrogen sulfide alleviates oxidative damage under chilling stress through mitogen activated protein kinase in tomato |
| topic | tomato mitogen-activated protein kinases chilling stress oxidative damage |
| url | https://www.mdpi.com/2076-3921/13/3/323 |
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