Exogenous hydrogen sulfide alleviates salt stress by improving antioxidant defenses and the salt overly sensitive pathway in wheat seedlings

• Autorzy: Ding H. , Ma D. , Huang X. , Hou J. , Wang C. , Xie Y. , Wang Y. , Qin H. , Guo T.
• Języki publikacji: EN

Abstrakty

EN

Hydrogen sulfide (H₂S) has the ability to strengthen plant stress tolerance; however, the effects of H₂S on wheat seedlings under salt stress and the underlying molecular mechanism are still unclear. This study examined the effects of exogenous NaHS as H₂S donor on photosynthesis, antioxidant system, and the expression profile of genes related to antioxidant defense responses, the salt overly sensitive (SOS) and mitogen-activated protein kinase (MAPK) pathways in wheat seedlings treated with NaCl stress. H₂S application improved photosynthesis, and decreased H₂O₂ and malondialdehyde (MDA) contents in wheat seedling leaves under NaCl stress. In addition, antioxidant enzyme activity and the content of ascorbic acid and reduced glutathione increased with H₂S application. Moreover, H₂S pretreatment up-regulated expression levels of genes related to antioxidant system, SOS pathway and MAPK pathway as well as the transcription factor dehydration-responsive element binding gene. Overall, these findings suggest that H₂S alleviates salt stress in wheat seedlings not only by strengthening antioxidant defense systems, but by coordinating signal transduction pathways related to the stress response at a transcriptional level.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 07
• Opis fizyczny: Article 123 [11p.], fig.,ref.

Twórcy

autor

Ding H.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China

autor

Ma D.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China
• National Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou 450002, China

autor

Huang X.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China

autor

Hou J.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China

autor

Wang C.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China
• National Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou 450002, China

autor

Xie Y.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China
• Collaborative Innovation Center of Henan Food Crops, Henan Agricultural University, Zhengzhou 45002, China

autor

Wang Y.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China
• Collaborative Innovation Center of Henan Food Crops, Henan Agricultural University, Zhengzhou 45002, China

autor

Qin H.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China

autor

Guo T.

• Agronomy College, National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou 450002, China
• Collaborative Innovation Center of Henan Food Crops, Henan Agricultural University, Zhengzhou 45002, China

Bibliografia

• Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plant. Plant Cell Rep 25:1263–1274
• Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1334–1337
• Ali B, Song WJ, Hu WZ, Luo XN, Gill RA, Wang J, Zhou WJ (2014) Hydrogen sulfide alleviates lead-induced photosynthetic and ultrastructural changes in oilseed rape. Ecotox Environ Safe 102:25–33
• Beauchamp C, Fridovich I (1971) Superoxide dismutase improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
• Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257
• Buwalda F, Kok LJD, Srulen I, Kuiper PJC (1988) Cysteine, γ-glutamyl-cysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. Physiol Plantarum 74:663–668
• Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530
• Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493
• Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318
• Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulfide enhance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516
• Christou A, Manganaris G, 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
• Christou A, Filippou P, Manganaris G, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14:42
• Deng YQ, Bao J, Yuan F, Liang X, Feng ZT, Wang BS (2016) Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na⁺ content. Plant Growth Regul 79:391–399
• Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
• Ding HN, Han QX, Ma DY, Hou JF, Huang X, Wang CY, Xie YX, Kang GZ, Guo TC (2018) Characterizing physiological and proteomic analysis of the action of H2S to mitigate drought stress in young seedling of wheat. Plant Mol Biol Rep 36:45–57
• Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8(4):e62048
• Du X, Jin Z, Liu D, Yang G, Pei Y (2017) Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana. Plant Physiol Bioch 120:112–119
• Duan BB, Ma YH, Jiang MR, Yang F, Ni L, Lu W (2015) Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul 75:33–34
• Foyer C, Rowell J, Walker D (1983) Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239–244
• Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212
• Hancock JT (2017) Harnessing evolutionary toxins for signaling: reactive oxygen species, nitric oxide and hydrogen sulfide in plant cell regulation. Front Plant Sci 8:189
• Hao L, Wen YL, Zhao YY, Lu WJ, Xiao K (2015) Wheat mitogen-activated protein kinase gene TaMPK4 improves plant tolerance to multiple stresses through modifying root growth, ROS metabolism, and nutrient acquisition. Plant Cell Rep 34:2081–2097
• Jin ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Bioph Res Co 414:481–486
• Li ZG, Gong M, Liu P (2012) Hydrogen sulfide is a mediator in H₂O₂-induced seed germination in Jatropha Curcas. Acta Physiol Plant 34:2207–2213
• Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc T 11:591–592
• Ma DY, Sun DX, Wang CY, Qin HX, Ding HN, Li YG, Guo TC (2015) Silicon application alleviates drought stress in wheat through transcriptional regulation of multiple antioxidant defense pathways. J Plant Growth Regul 35:1–10
• Ma DY, Ding HN, Wang CY, Qin HX, Han QX, Hou JF, Lu HF, Xie YX, Guo TC (2016) Alleviation of drought stress by hydrogen sulfide is partially related to the abscisic acid signaling pathway in wheat. PLoS One 11(9):e0163082
• Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Archi Biochem Biophys 444:139–158
• Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467
• Mostofal MG, Saegusa D, Fujita M, Tran LS (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na⁺/K⁺balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:662–676
• Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
• Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
• Qiu SH, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1 a plasma membrane Na⁺/H⁺exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441
• Qiu SH, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu JK (2004) Regulation of vacuolar Na⁺/H⁺ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279:207–215
• Robinson MJ, Cobb MH (1997) Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 9:180–186
• Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649
• Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345:1253–1264
• Sathee L, Sairam RK, Chinnusamy V, Jha SK (2015) Differential transcript abundance of salt overly sensitive (sos) pathway genes is a determinant of salinity stress tolerance of wheat. Acta Physiol Plant 37:1–10
• Shan C, Zhang S, Ou X (2018) The roles of H₂S and H₂O₂ in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. Protoplasma 21:1–6
• Smirnoff N (2006) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58
• Wen YL, Li XJ, Guo CJ, Ma CY, Duan WW, Lu WJ, Xiao K (2015) Characterization and expression analysis of mitogen-activated protein kinase cascade genes in wheat subjected to phosphorus and nitrogen deprivation, high salinity, and drought. J Plant Biochem Biot 24:184–196
• Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid inducible mitogen-activated protein kinase. Plant Cell 15:745–759
• Zhang J, Kirkham MB (1994) Drought stress induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791
• Zhang H, Wang MJ, Hu LY, Wang SH, Hu KD, Bao LJ, Luo JP (2010) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physl 57:532–539
• Zheng YH, Jia AJ, Ning TY, Xu JL, Li ZJ, Jiang GM (2008) Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance. J Plant Physiol 165:1455–1465
• Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948
• Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

Identyfikatory

DOI

10.1007/s11738-019-2918-6