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Journal of Integrative Agriculture  2016, Vol. 15 Issue (12): 2745-2758    DOI: 10.1016/S2095-3119(16)61358-8
Physiology·Biochemistry·Cultivation·Tillage Advanced Online Publication | Current Issue | Archive | Adv Search |
Foliar application of sodium hydrosulfide (NaHS), a hydrogen sulfide (H2S) donor, can protect seedlings against heat stress in wheat (Triticum aestivum L.)
YANG Min1*, QIN Bao-ping1*, MA Xue-li1, WANG Ping2, LI Mei-ling1, CHEN Lu-lu1, CHEN Lei-tai1, SUN Ai-qing1, WANG Zhen-lin1, YIN Yan-ping1
1 State Key Laboratory of Crop Biology/Agronomy College, Shandong Agricultural University, Tai’an 271018, P.R.China
2 Tai’an Academy of Agricultural Sciences, Tai’an 271018, P.R.China
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Abstract      Temperature extremes represent an important limiting factor to plant growth and productivity. Low concentration of hydrogen sulfide (H2S) has been proven to function in physiological responses to various stresses. The present study evaluated the effect of foliar application of wheat seedlings with a H2S donor, sodium hydrosulfide (NaHS), on the response to acute heat stress. The results showed that pretreatment with NaHS could promote heat tolerance of wheat seedlings in a dose-dependent manner. Again, it was verified that H2S, rather than other sulfur-containing components or sodion derived from NaHS solution, should contribute to the positive role in promoting wheat seedlings against heat stress. To further study antioxidant mechanisms of NaHS-induced heat tolerance, superoxide dismutase (SOD, EC, catalase (CAT, EC and ascorbate peroxidase (APX, EC activities, and H2S, hydrogen peroxide (H2O2), malonaldehyde (MDA), and soluble sugar contents in wheat seedlings were determined. The results showed that, under heat stress, the activities of SOD, CAT, and APX, H2S, H2O2, MDA, and soluble sugar contents in NaHS-pretreated seedlings and its control all increased. Meanwhile, NaHS-pretreated seedlings showed higher antioxidant enzymes activities and gene expression levels as well as the H2S and soluble sugar levels, and lower H2O2, MDA contents induced by heat stress. While little effect was detected in antioxidant enzymes activities and soluble substances contents in pretreated wheat seedlings compared with its control under normal culture conditions (data not shown). All of our results suggested that exogenous NaHS could alleviate oxidative damage and improve heat tolerance by regulating the antioxidant system in wheat seedlings under heat stress.
Keywords:  wheat seedlings        sodium hydrosulfide        heat stress        antioxidant system        mitigative effect  
Received: 17 December 2015   Accepted:

This study was supported by the Special Fund for Agro-scientific Research in the Public Interest of China (201203029).

Corresponding Authors:  YIN Yan-ping, E-mail:    
About author:  YANG Min, E-mail:; QIN Bao-ping, E-mail:;

Cite this article: 

YANG Min, QIN Bao-ping, MA Xue-li, WANG Ping, LI Mei-ling, CHEN Lu-lu, CHEN Lei-tai, SUN Aiqing, WANG Zhen-lin, YIN Yan-ping. 2016. Foliar application of sodium hydrosulfide (NaHS), a hydrogen sulfide (H2S) donor, can protect seedlings against heat stress in wheat (Triticum aestivum L.). Journal of Integrative Agriculture, 15(12): 2745-2758.

Altenbach S. 2012. New insights into the effects of high temperature, drought and post-anthesis fertilizer on wheat grain development. Journal of Cereal Science, 56, 39–50.

Aroca Á, Serna A, Gotor C, Romero L. 2015. S-sulfhydration: A cysteine posttranslational modification in plant systems. Plant Physiology, 168, 334–342.

Barnabás B, Jäger K, Fehér A. 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell and Environment, 31, 11–38.

Bohnert H, Gong Q, Li P, Ma S. 2006. Unraveling abiotic stress tolerance mechanisms - getting genomics going. Current Opinion in Plant Biology, 9, 180–188.

Bolouri-Moghaddam M, Roy K, Li X, Rolland F, Ende W. 2010. Sugar signalling and antioxidant network connections in plant cells. The FEBS Journal, 277, 2022–2037.

Brunel-Muguet S, D’hooghe P, Bataille M, Larré C, Kim T, Trouverie J, Avice J, Etienne P, Durr C. 2015. Heat stress during seed filling interferes with sulfur restriction on grain composition and seed germination in oilseed rape (Brassica napus L.). Frontiers in Plant Science, 6, 213.

Caverzan A, Passaia G, Rosa S, Ribeiro C, Lazzarotto F, Margis-Pinheiro M. 2012. Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genetics and Molecular Biology, 35, 1011–1019.

Chen J, Wang W, Wu F, You C, Liu T, Dong X, He J, Zheng H. 2013. Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant and Soil, 362, 301–318.

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. Journal of Experimental Botany, 62, 4481–4493.

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. Journal of Experimental Botany, 64, 1953–1966.

Cooper C, Brown G. 2008. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: Chemical mechanism and physiological significance. Journal of Bioenergetics and Biomembranes, 40, 533–539.

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 homeostases. PLOS ONE, 9, e109669.

Dawood M, Cao F, Jahangir M, Zhang G, Wu F. 2012. Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. Journal of Hazardous Materials, 209–210, 121–128.

Fu P, Wang W, Hou L, Liu X. 2013. Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Societatis Botanicorum Poloniae, 82, 295–302.

García-Mata C, Lamattina L. 2010. Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytologist, 188, 977–984.

Gomathi R, Shiyamala S, Vasantha S, Johnson D, Janani P. 2013. Kinetics of metabolism in sugarcane (Saccharum officinarum L.) under heat stress. Indian Journal of Plant Physiology, 18, 41–47.

Hancock J, Whiteman M. 2014. Hydrogen sulfide and cell signaling: Team player or referee? Plant Physiology and Biochemistry, 78, 37–42.

Hasanuzzaman M, Nahar K, Alam M, Roychowdhury R, Fujita M. 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. International Journal of Molecular Sciences, 14, 9643–9684.

Hodges D, DeLong J, Forney C, Prange R. 1999. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta, 207, 604–611.

Hu K, Wang Q, Hu L, Gao S, Wu J, Li Y, Zheng J, Han Y, Liu Y, Zhang H. 2014. Hydrogen sulfide prolongs postharvest storage of fresh-cut pears (Pyrus pyrifolia) by alleviation of oxidative damage and inhibition of fungal growth. PLOS ONE, 9, e85524.

Hu L, Hu S, Wu J, Li Y, Zheng J, Wei Z, Liu J, Wang H, Liu Y, Zhang H. 2012. Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. Journal of Agricultural and Food Chemistry, 60, 8684–8693.

Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y. 2011. Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochemical and Biophysical Research Communications, 414, 481–486.

Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y. 2013. Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiology and Biochemistry, 62, 41–46.

Li L, Wang Y, Shen W. 2012. Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. BioMetals, 25, 617–631.

Li Z. 2013. Hydrogen sulfide: A multifunctional gaseous molecule in plants. Russian Journal of Plant Physiology, 60, 733–740.

Li Z, Ding X, Du P. 2013a. Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. Journal of Plant Physiology, 170, 741–747.

Li Z, Gong M, Liu P. 2012a. Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas. Acta Physiologiae Plantarum, 34, 2207–2213.

Li Z, Gong M, Xie H, Yang L, Li J. 2012b. Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Science, 185–186, 185–189.

Li Z, Long W, Yang S, Wang Y, Tang J, Chen T. 2015a. Involvement of sulfhydryl compounds and antioxidant enzymes in H2S-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension-cultured cells. In Vitro Cellular and Developmental Biology (Plant), 51, 428–437.

Li Z, Luo L, Sun Y. 2015b. Signal crosstalk between nitric oxide and hydrogen sulfide may be involved in hydrogen peroxide-induced thermotolerance in maize seedlings. Russian Journal of Plant Physiology, 62, 507–514.

Li Z, Luo L, Zhu L. 2014a. Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings. Botanical Studies, 55, 1–9.

Li Z, Yang S, Long W, Yang G, Shen Z. 2013b. Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant, Cell and Environment, 36, 1564–1572.

Li Z, Yi X, Li Y. 2014b. Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia, 69, 1001–1009.

Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood M, Whiteman M, Hancock J. 2010. A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiology and Biochemistry, 48, 931–935.

Lisjak M, Tekli? T, Wilson I, Wood M, Whiteman M, Hancock J. 2011. Hydrogen sulfide effects on stomatal apertures. Plant Signaling and Behavior, 6, 1444–1446.

Liu J, Hou L, Liu G, Liu X, Wang X. 2011. Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chinese Science Bulletin, 56, 3547–3553.

Liu J, Hou Z, Liu G, Hou L, Liu X. 2012. Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L. Journal of Integrative Agriculture, 11, 1644–1653.

Liu R, Lal R. 2015. Effects of low-level aqueous hydrogen sulfide and other sulfur species on Lettuce (Lactuca sativa) seed germination. Communications in Soil Science and Plant Analysis, 46, 576–587.

Miller G, Tognetti V, Vandepoele K, Breusegem F, Mittler R, Vanderauwera S, Suzuki N, Gollery M, Shulaev V. 2011. ROS signaling: The new wave? Trends in Plant Science, 16, 300–309.

Mittler R, Finka A, Goloubinoff P. 2012. How do plants feel the heat? Trends in Biochemical Sciences, 37, 118–125.

Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in Spinach chloroplasts. Plant and Cell Physiology, 22, 867–880.

Papanatsiou M, Scuffi D, Blatt M, García-Mata C. 2015. Hydrogen sulfide regulates inward-rectifying K+ channels in conjunction with stomatal closure. Plant Physiology, 168, 29–35.

Qiao Z, Jing T, Liu Z, Zhang L, Jin Z, Liu D, Pei Y. 2015. H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant and Soil, 393, 137–146.

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 Physiologiae Plantarum, 33, 2533–2540.

Shen J, Qiao Z, Xing T, Zhang L, Liang Y, Jin Z, Yang G, Wang R, Pei Y. 2012. Cadmium toxicity is alleviated by AtLCD and AtDCD in Escherichia coli. Journal of Applied Microbiology, 113, 1130–1138.

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.

Shi H, Ye T, Chan Z. 2013. Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiology and Biochemistry, 71, 226–234.

Shi H, Ye T, Chan Z. 2014. Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiology and Biochemistry, 74, 99–107.

Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S. 2013. Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiology and Biochemistry, 65, 67–74.

Sung D, Kaplan F, Lee K, Guy C. 2003. Acquired tolerance to temperature extremes. Trends in Plant Science, 8, 179–187.

Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D. 2008. Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica, 46, 21–27.

Wang B, Shi L, Li Y, Zhang W. 2010. Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta, 231, 1301–1309.

Wang R. 2002. Two’s company, three’s a crowd: Can H2S be the third endogenous gaseous transmitter? The FASEB Journal, 16, 1792–1798.

Wang R. 2012. Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiological Reviews, 92, 791–896.

Wang Y, Li L, Cui W, Xu S, Shen W, Wang R. 2012. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant and Soil, 351, 107–119.

Xie Y, Zhang C, Lai D, Sun Y, Samma M, Zhang J, Shen W. 2014. Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. Journal of Plant Physiology, 171, 53–62.

Yu B, Zhao C, Li J, Li J, Peng G. 2015. Morphological, physiological, and biochemical responses of Populus euphratica to soil flooding. Photosynthetica, 53, 110–117.

Zhang H, Dou W, Jiang C, Wei Z, Liu J, Jones R. 2010a. Hydrogen sulfide stimulates β-amylase activity during early stages of wheat grain germination. Plant Signaling and Behavior, 5, 1031–1033.

Zhang H, Hu L, Hu K, He Y, Wang S, Luo J. 2008. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. Journal of Integrative Plant Biology, 50, 1518–1529.

Zhang H, Hu L, Li P, Hu K, Jiang C, Luo J. 2010b. Hydrogen sulfide alleviated chromium toxicity in wheat. Biologia Plantarum, 54, 743–747.

Zhang H, Hu S, Zhang Z, Hu L, Jiang C, Wei Z, Liu J, Wang H, Jiang S. 2011. Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biology and Technology, 60, 251–257.

Zhang H, Jiao H, Jiang C, Wang S, Wei Z, Luo J, Jones R. 2010c. Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiologiae Plantarum, 32, 849–857.

Zhang H, Tan Z, Hu L, Wang S, Luo J, Jones R. 2010d. Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. Journal of Integrative Plant Biology, 52, 556–567.

Zhang H, Tang J, Liu X, Wang Y, Yu W, Peng W, Fang F, Ma D, Wei Z, Hu L. 2009a. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. Journal of Integrative Plant Biology, 51, 1086–1094.

Zhang H, Wang M, Hua L, Wang S, Hua K, Bao L, Luo J. 2010e. Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russian Journal of Plant Physiology, 57, 532–539.

Zhang H, Ye Y, Wang S, Luo J, Tang J, Ma D. 2009b. Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regulation, 58, 243–250.
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