Abiotic stress-triggered oxidative challenges: Where does H2S act?
doi: 10.1016/j.jgg.2022.02.019
Abiotic stress-triggered oxidative challenges: Where does H2S act?
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摘要: Hydrogen sulfide (H2S) was once principally considered the perpetrator of plant growth cessation and cell death. However, this has become an antiquated view, with cumulative evidence showing that the H2S serves as a biological signaling molecule notably involved in abiotic stress response and adaptation, such as defense by phytohormone activation, stomatal movement, gene reprogramming, and plant growth modulation. Reactive oxygen species (ROS)-dependent oxidative stress is involved in these responses. Remarkably, an ever-growing body of evidence indicates that H2S can directly interact with ROS processing systems in a redox-dependent manner, while it has been gradually recognized that H2S-based posttranslational modifications of key protein cysteine residues determine stress responses. Furthermore, the reciprocal interplay between H2S and nitric oxide (NO) in regulating oxidative stress has significant importance. The interaction of H2S with NO and ROS during acclimation to abiotic stress may vary from synergism to antagonism. However, the molecular pathways and factors involved remain to be identified. This review not only aims to provide updated information on H2S action in regulating ROS-dependent redox homeostasis and signaling, but also discusses the mechanisms of H2S-dependent regulation in the context of oxidative stress elicited by environmental cues.
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关键词:
- Hydrogen sulfide /
- Oxidative stress /
- ROS /
- Nitric oxide /
- Redox signaling
Abstract: Hydrogen sulfide (H2S) was once principally considered the perpetrator of plant growth cessation and cell death. However, this has become an antiquated view, with cumulative evidence showing that the H2S serves as a biological signaling molecule notably involved in abiotic stress response and adaptation, such as defense by phytohormone activation, stomatal movement, gene reprogramming, and plant growth modulation. Reactive oxygen species (ROS)-dependent oxidative stress is involved in these responses. Remarkably, an ever-growing body of evidence indicates that H2S can directly interact with ROS processing systems in a redox-dependent manner, while it has been gradually recognized that H2S-based posttranslational modifications of key protein cysteine residues determine stress responses. Furthermore, the reciprocal interplay between H2S and nitric oxide (NO) in regulating oxidative stress has significant importance. The interaction of H2S with NO and ROS during acclimation to abiotic stress may vary from synergism to antagonism. However, the molecular pathways and factors involved remain to be identified. This review not only aims to provide updated information on H2S action in regulating ROS-dependent redox homeostasis and signaling, but also discusses the mechanisms of H2S-dependent regulation in the context of oxidative stress elicited by environmental cues.-
Key words:
- Hydrogen sulfide /
- Oxidative stress /
- ROS /
- Nitric oxide /
- Redox signaling
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Alvarez, C., Calo, L., Romero, L. C., Garcia, I., Gotor, C., 2010. An O-acetylserine(thiol)lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol. 152(2), 656-669 Aroca, A., Benito, J. M., Gotor, C., Romero, L. C., 2017. Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis. J. Exp. Bot. 68, 4915-4927 Aroca, A., Serna, A., Gotor, C., Romero, L. C., 2015. S-sulfhydration:a cysteine posttranslational modification in plant systems. Plant Physiol. 168, 334-342 Aroca, A., Zhang, J., Xie, Y., Romero, L. C., Gotor, C., 2021. Hydrogen sulfide signaling in plant adaptations to adverse conditions:molecular mechanisms. J. Exp. Bot. 72, 5893-5904 Baudouin, E., Poilevey, A., Hewage, N. I., Cochet, F., Puyaubert, J., Bailly, C.; 2016. The significance of hydrogen sulfide for Arabidopsis seed germination. Front. Plant Sci. 7, 930 Bauer, M., Dietrich, C., Nowak, K., Sierralta, W. D., Papenbrock, J., 2004. Intracellular localization of Arabidopsis sulfurtransferases. Plant Physiol. 135(2), 916-926 Begara-Morales, J. C., Chaki, M., Sanchez-Calvo, B., Mata-Perez, C., Leterrier, M., Palma, J. M., Barroso, J. B., Corpas, F. J., 2013. Protein tyrosine nitration in pea roots during development and senescence. J. Exp. Bot. 64, 1121-1134 Carballal, S., Trujillo, M., Cuevasanta, E., Bartesaghi, S., Moller, M. N., Folkes, L. K., Garcia-Bereguiain, M. A., Gutierrez-Merino, C., Wardman, P., Denicola, A., et al., 2011. Reactivity of hydrogen sulfide with peroxynitrite and other oxidants of biological interest. Free Radic. Biol. Med. 50(1), 196-205 Chaki, M., Valderrama, R., Fernandez-Ocana, A. M., Carreras, A., Gomez-Rodriguez, M. V., Lopez-Jaramillo, J., Begara-Morales, J. C., Sanchez-Calvo, B., Luque, F., Leterrier, M., et al., 2011. High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ. 34, 1803-1818 Chen, J., Wang, W., Wu, F., He, E., Liu, X., Shangguan, Z., Zheng, H., 2015. Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci. Rep. 5, 12516 Chen, J., Wu, F., Wang, W., Zheng, C., Lin, G., Dong, X., He, J., Pei, Z., Zheng, H., 2011. Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J. Exp. Bot. 62(13), 4481-4493 Chen, P., Yang, W., Wen, M., Jin, S., Liu, Y., 2021. Hydrogen sulfide alleviates salinity stress in Cyclocarya paliurus by maintaining chlorophyll fluorescence and regulating nitric oxide level and antioxidant capacity. Plant Physiol. Biochem. 167, 738-747 Chen, S., Jia, H., Wang, X., Shi, C., Wang, X., Ma, P., Wang, J., Ren, M., Li, J., 2020a. Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol. Plant 13, 732-744 Chen, T., Tian, M., Han, Y., 2020b. Hydrogen sulfide:a multi-tasking signal molecule in the regulation of oxidative stress responses. J. Exp. Bot. 71,2862-2869 Cheng, W., Zhang, L., Jiao, C., Su, M., Yang, T., Zhou, L., Peng, R., Wang, R., Wang, C., 2013. Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol. Biochem. 70, 278-286 Christou, A., Manganaris, G. A., Papadopoulos, I., Fotopoulos, V., 2013. Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J. Exp. Bot. 64, 1953-1966 Corpas F. J., 2019. Hydrogen sulfide:a new warrior against abiotic stress. Trends Plant Sci. 24(11), 983-988 Corpas, F. J., Barroso, J. B., 2013. Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol. 199, 633-635 Corpas, F. J., Barroso, J. B., Gonzalez-Gordo, S., Munoz-Vargas, M. A., Palma, J. M., 2019. Hydrogen sulfide:a novel component in Arabidopsis peroxisomes which triggers catalase inhibition. J. Integr. Plant Biol. 61, 871-883 Cui, W., Chen, H., Zhu, K., Jin, Q., Xie, Y., Cui, J., Xia, Y., Zhang, J., Shen, W., 2014. Cadmium-induced hydrogen sulfide synthesis is involved in cadmium tolerance in Medicago sativa by reestablishment of reduced (homo)glutathione and reactive oxygen species homeostasis. PLoS One 9, e109669 da-Silva, C. J., Mollica, D., Vicente, M. H., Peres, L., Modolo, L. V., 2018. NO, hydrogen sulfide does not come first during tomato response to high salinity. Nitric Oxide 76, 164-173 Deng, G., Zhou, L., Wang, Y., Zhang, G., Chen, X., 2020. Hydrogen sulfide acts downstream of jasmonic acid to inhibit stomatal development in Arabidopsis. Planta 251(2), 42 Duan, X., Xu, S., Xie, Y., Li, L., Qi, W., Parizot, B., Zhang, Y., Chen, T., Han, Y., Van Breusegem, F., et al., 2021. Periodic root branching is influenced by light through an HY1-HY5-auxin pathway. Curr. Biol. 31(17), 3834-3847.e5 Fang, H., Liu, Z., Long, Y., Liang, Y., Jin, Z., Zhang, L., Liu, D., Li, H., Zhai, J., Pei, Y., 2017. The Ca2+/calmodulin2-binding transcription factor TGA3 elevates LCD expression and H2S production to bolster Cr6+ tolerance in Arabidopsis. Plant J. 91(6), 1038-1050 Foyer, C.H., Noctor G., 2020. Redox homeostasis and signaling in a higher-CO2 world. Annu. Rev. Plant Biol. 71, 157-182 Fu, L., Liu, K., He, J., Tian, C., Yu, X., Yang, J., 2020. Direct proteomic mapping of cysteine persulfidation. antioxid redox signal. 33(15), 1061-1076 Gonzalez-Gordo, S., Palma, J. M., Corpas, F. J., 2020. Appraisal of H2S metabolism in Arabidopsis thaliana:in silico analysis at the subcellular level. Plant Physiol. Biochem. 155, 579-588 Han, Y., Zhang, J., Chen, X., Gao, Z., Xuan, W., Xu, S., Ding, X., Shen, W., 2008. Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol. 177(1),155-166 Hatzfeld, Y., Maruyama, A., Schmidt, A., Noji, M., Ishizawa, K., Saito, K., 2000. beta-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol. 123(3), 1163-1171 Hou, Z., Wang, L., Liu, J., Hou, L., Liu, X., 2013. Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J. Integr. Plant Biol. 55(3), 277-289 Hu, K., Zhang, X., Yao, G., Rong, Y., Ding, C., Tang, J., Yang, F., Huang, Z., Xu, Z., Chen, X., et al., 2020. A nuclear-localized cysteine desulfhydrase plays a role in fruit ripening in tomato. Hortic. Res. 7(1),211 Huang, J., Willems, P., Wei, B., Tian, C., Ferreira, R. B., Bodra, N., Martinez Gache, S. A., Wahni, K., Liu, K., Vertommen, D., et al., 2019. Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites. Proc. Natl. Acad. Sci. U.S.A. 116(42), 21256-21261 Iqbal, N., Umar, S., Khan, N. A., Corpas, F. J., 2021. Nitric oxide and hydrogen sulfide coordinately reduce glucose sensitivity and decrease oxidative stress via ascorbate-glutathione cycle in heat-stressed wheat (Triticum aestivum L.) Plants. Antioxidants (Basel). 10, 108 Jin, Z., Shen, J., Qiao, Z., Yang, G., Wang, R., Pei, Y., 2011. Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 414(3), 481-486 Jurado-Flores, A., Romero, L. C., Gotor, C., 2021. Label-free quantitative proteomic analysis of nitrogen starvation in Arabidopsis root reveals new aspects of H2S signaling by protein persulfidation. Antioxidants (Basel). 10, 508 Kaya, C., Higgs, D., Ashraf, M., Alyemeni, M. N., Ahmad, P., 2020. Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol. Plantarum 168 Kharbech, O., Ben Massoud, M., Sakouhi, L., Djebali, W., Jose Mur, L. A., Chaoui, A., 2020. Exogenous application of hydrogen sulfide reduces chromium toxicity in maize seedlings by suppressing NADPH oxidase activities and methylglyoxal accumulation. Plant Physiol. Biochem. 154, 646-656 Kovacs, I., Holzmeister, C., Wirtz, M., Geerlof, A., Frohlich, T., Romling, G., Kuruthukulangarakoola, G. T., Linster, E., Hell, R., Arnold, G. J., et al., 2016. ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of anti-oxidative mechanisms. Front. Plant Sci. 7, 1669 Laureano-Marin, A. M., Garcia, I., Romero, L. C., Gotor, C., 2014. Assessing the transcriptional regulation of L-cysteine desulfhydrase 1 in Arabidopsis thaliana. Front. Plant Sci. 5, 683 Laureano-Marin, A. M., Moreno, I., Romero, L. C., Gotor, C., 2016. Negative regulation of autophagy by sulfide is independent of reactive oxygen species. Plant Physiol. 171(2), 1378-1391 Li, J., Shi, C., Wang, X., Liu, C., Ding, X., Ma, P., Wang, X., Jia, H., 2020. Hydrogen sulfide regulates the activity of antioxidant enzymes through persulfidation and improves the resistance of tomato seedling to Copper Oxide nanoparticles (CuO NPs)-induced oxidative stress. Plant Physiol. Biochem. 156, 257-266 Li, Z., Xie, L., Li, X., 2015. Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J. Plant Physiol. 177, 121-127 Li, Z., Yang, S., Long, W., Yang, G., Shen, Z., 2013. Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ. 36, 1564-1572 Li, Z., Zhu, Y., He, X., Yong, B., Peng, Y., Zhang, X., Ma, X., Yan, Y., Huang, L., Nie, G., 2019. The hydrogen sulfide, a downstream signaling molecule of hydrogen peroxide and nitric oxide, involves spermidine-regulated transcription factors and antioxidant defense in white clover in response to de-hydration. Environ. Exp. Bot. 161, 255-264 Lin, Y., Zhang, W., Qi, F., Cui, W., Xie, Y., Shen, W., 2014. Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner. J. Plant Physiol. 171(2), 1-8 Liu, Y., Shen, Z., Simon, M., Li, H., Ma, D., Zhu, X., Zheng, H., 2019. Comparative proteomic analysis reveals the regulatory effects of H2S on salt tolerance of mangrove plant Kandelia obovata. Int. J. Mol. Sci. 21, 118 Ma, L., Yang, L., Zhao, J., Wei, J., Kong, X., Wang, C., Zhang, X., Yang, Y., Hu, X., 2015. Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotata to altitude gradient in the Northern Tibetan Plateau. Planta 241, 887-906 Ma, X., Zhang, L., Pei, Z., Zhang, L., Liu, Z., Liu, D., Hao, X., Jin, Z., Pei, Y., 2021a. Hydrogen sulfide promotes flowering in heading Chinese cabbage by S-sulfhydration of BraFLCs. Hortic. Res. 8(1), 19 Ma, Y., Shao, L., Zhang, W., Zheng, F., 2021b. Hydrogen sulfide induced by hydrogen peroxide mediates brassinosteroid-induced stomatal closure of Arabidopsis thaliana. Funct. Plant Biol. 48, 195-205 Mei, Y., Chen, H., Shen, W., Shen, W., Huang, L., 2017. Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol. 17(1), 162 Mills, G.; Schmidt, K. H.; Matheson, M. S.; Meisel, D., 1987. Thermal and photochemical reactions of sulfhydryl radicals. Implications for colloid photocorrosion. Phys. Chem. 91, 1590-1596 Moseler, A., Dhalleine, T., Rouhier, N., Couturier, J., 2021. Arabidopsis thaliana 3-mercaptopyruvate sulfurtransferases interact with and are protected by reducing systems. J. Boil. Chem. 296, 100429 Muñoz-Vargas, M. A., González-Gordo, S., Cañas, A., Lopez-Jaramillo, J., Palma, J. M., Corpas, F. J., 2018. Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and NO. Nitric Oxide 81, 36-45 Ni, X., Li, X., Shen, T., Qian, W., Xian, M., 2021. A sweet H2S/H2O2 dual release system and specific protein S-persulfidation mediated by thioglucose/glucose oxidase. J. Am. Chem. Soc. 143(33), 13325-13332 Nishizawa, A., Yabuta, Y., Shigeoka, S., 2008. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147(3), 1251-1263 Noctor, G., Reichheld, J. P., Foyer, C. H., 2018. ROS-related redox regulation and signaling in plants. Semin. Cell Dev. Biol. 80, 3-12 Polle A., 2001. Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol. 126(1), 445-462 Riemenschneider, A., Wegele, R., Schmidt, A., Papenbrock, J., 2005. Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J. 272(5), 1291-1304 Scuffi, D., Alvarez, C., Laspina, N., Gotor, C., Lamattina, L., Garcia-Mata, C., 2014. Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol. 166, 2065-2076 Scuffi, D., Nietzel, T., Di Fino, L. M., Meyer, A. J., Lamattina, L., Schwarzlander, M., Laxalt, A. M., Garcia-Mata, C., 2018. Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling. Plant Physiol. 176, 2532-2542 Shan, C., Dai, H., Sun Y., 2012. Hydrogen sulfide protects wheat seedlings against copper stress by regulating the ascorbate and glutathione metabolism in leaves. Aust. J. Crop. Sci. 6, 248-254 Shan, C., Zhang, S., Li, D., Zhao, Y., Tian, X., Zhao, X., Wu, Y., Wei, X., Liu, R., 2011. Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol. Plant. 33, 2533-2540 Shen, J., Xing, T., Yuan, H., Liu, Z., Jin, Z., Zhang, L., Pei, Y., 2013. Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS One. 8, e77047 Shen, J., Zhang, J., Zhou, M., Zhou, H., Cui, B., Gotor, C., Romero, L. C., Fu, L., Yang, J., Foyer, C. H.,et al., 2020. Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling. Plant Cell 32, 1000-1017 Shi, H., Ye, T., Han, N., Bian, H., Liu, X., Chan, Z., 2015. Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J. Integr. Plant Biol. 57(7), 628-640 Shimizu, T., Hayashi, Y., Arai, M., McGlynn, S. E., Masuda, T., Masuda, S., 2021. Repressor activity of SqrR, a master regulator of persulfide-responsive genes, is regulated by heme coordination. Plant Cell Physiol. 62(1), 100-110 Sirichandra, C., Gu, D., Hu, H. C., Davanture, M., Lee, S., Djaoui, M., Valot, B., Zivy, M., Leung, J., Merlot, S., et al., 2009. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 583(18), 2982-2986 Takahashi, H., Kopriva, S., Giordano, M., Saito, K., Hell, R., 2011. Sulfur assimilation in photosynthetic organisms:molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62, 157-184 Tang, X., An, B., Cao, D., Xu, R., Wang, S., Zhang, Z., Liu, X., Sun, X., 2020. Improving photosynthetic capacity, alleviating photosynthetic inhibition and oxidative stress under low temperature stress with exogenous hydrogen sulfide in blueberry seedlings. Front. Plant Sci. 11, 108 Wang, P., Du, Y., Hou, Y., Zhao, Y., Hsu, C., Yuan, F., Zhu, X., Tao, W., Song, C., Zhu, J., 2015. Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc. NatI. Acad. Sci. U. S. A. 112, 613-618 Wedmann, R., Bertlein, S., Macinkovic, I., Boltz, S., Miljkovic, J., Munoz, L. E., Herrmann, M., Filipovic, M. R., 2014. Working with "H2S":facts and apparent artifacts. Nitric Oxide. 41, 85-96 Wei, B., Zhang, W., Chao, J., Zhang, T., Zhao, T., Noctor, G., Liu, Y., Han, Y., 2017. Functional analysis of the role of hydrogen sulfide in the regulation of dark-induced leaf senescence in Arabidopsis. Sci. Rep. 7, 2615 Wei, M., Liu, J., Li, H., Hu, W., Shen, Z., Qiao, F., Zhu, C., Chen, J., Liu, X., Zheng, H., 2021. Proteomic analysis reveals the protective role of exogenous hydrogen sulfide against salt stress in rice seedlings. Nitric Oxide. 111-112, 14-30 Winterbourn C. C., 2013. The biological chemistry of hydrogen peroxide. Methods Enzymol. 528:3-25 Winterbourn, C. C., Metodiewa, D., 1994. The reaction of superoxide with reduced glutathione. Arch. Biochem. Biophys. 314(2), 284-290 Yang, H., Mu, J., Chen, L., Feng, J., Hu, J., Li, L., Zhou, J., Zuo, J., 2015. S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol. 167, 1604-1615 Yun, B., Feechan, A., Yin, M., Saidi, N. B., Le Bihan, T., Yu, M., Moore, J. W., Kang, J., Kwon, E., Spoel, S. H., et al., 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478(7368), 264-268 Zhan, N., Wang, C., Chen, L., Yang, H., Feng, J., Gong, X., Ren, B., Wu, R., Mu, J., Li, Y., et al., 2018. S-Nitrosylation targets GSNO reductase for selective autophagy during hypoxia responses in plants. Mol. Cell. 71(1), 142-154 Zhang, D., Macinkovic, I., Devarie-Baez, N. O., Pan, J., Park, C. M., Carroll, K. S., Filipovic, M. R., Xian, M., 2014. Detection of protein S-sulfhydration by a tag-switch technique. Angew Chem. Int. Ed. Engl. 53(2), 575-581 Zhang, H., Tang, J., Liu, X., Wang, Y., Yu, W., Peng, W., Fang, F., Ma, D., Wei, Z., Hu, L., 2009. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J. Integr. Plant Biol. 51(12), 1086-1094 Zhang, J., Zhou, M., Ge, Z., Shen, J., Zhou, C., Gotor, C., Romero, L. C., Duan, X., Liu, X., Wu, D., et al., 2020a. Abscisic acid-triggered guard cell L-cysteine desulfhydrase function and in situ hydrogen sulfide production contributes to heme oxygenase-modulated stomatal closure. Plant Cell Environ. 43(3), 624-636 Zhang, J., Zhou, M., Zhou, H., Zhao, D., Gotor, C., Romero, L. C., Shen, J., Ge, Z., Zhang, Z., Shen, W., et al., 2021. Hydrogen sulfide, a signaling molecule in plant stress responses. J. Integr. Plant Biol. 63(1), 146-160 Zhang, N., Zou, H., Lin, X., Pan, Q., Zhang, W., Zhang, J., Wei, G., Shangguan, Z., Chen, J., 2020b. Hydrogen sulfide and rhizobia synergistically regulate nitrogen (N) assimilation and remobilization during N deficiency-induced senescence in soybean. Plant Cell Environ. 43(5), 1130-1147 Zhang, Q., Cai, W., Ji, T., Ye, L., Lu, Y., Yuan, T., 2020c. WRKY13 enhances cadmium tolerance by promoting D-CYSTEINE DESULFHYDRASE and hydrogen sulfide production. Plant Physiol. 183(1), 345-357 Zhang, T., Ma, M., Chen, T., Zhang, L., Fan, L., Zhang, W., Wei, B., Li, S., Xuan, W., Noctor, G., et al., 2020d. Glutathione-dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H2O2. Plant Cell Environ. 43, 1175-1191 Zhang, X., Liu, F., Zhai, J., Li, F., Bi, H., Ai, X., 2020e. Auxin acts as a downstream signaling molecule involved in hydrogen sulfide-induced chilling tolerance in cucumber. Planta 251, 69 Zhao, D., Zhang, J., Zhou, M., Zhou, H., Gotor, C., Romero, L. C., Shen, J., Yuan, X., Xie, Y., 2020a. Current approaches for detection of hydrogen sulfide and persulfidation in biological systems. Plant Physiol. Biochem. 155, 367-373 Zhao, M., Liu, Q., Zhang, Y., Yang, N., Wu, G., Li, Q., Wang, W., 2020b. Alleviation of osmotic stress by H2S is related to regulated PLDα1 and suppressed ROS in Arabidopsis thaliana. J. Plant Res. 133(3), 393-407
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