Document Type : Research paper
Authors
1 Biology Department, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran
2 Department of Biology, Shahid Bahonar University of Kerman, Kerman, Iran
Abstract
One of the major abiotic stresses limiting the productivity and the geographical distribution of many important crops is low temperature. Hydrogen sulfide (H2S) is an important signaling molecule involved in several stress-resistance processes such as drought, salinity and heavy metal stresses in plants. The aim of this study was to investigate the effects of exogenous H2S on improving chilling tolerance of cucumber seedlings. The results indicated that seedlings exposed to chilling stress (4 ºC) increased the level of electrolyte leakage, lipid peroxidation, hydrogen peroxide, proline content and guaiacol peroxidase (GPX) activity; while sugar soluble content decreased. Pretreatment with sodium hydrosulfide (NaHS), a hydrogen sulfide donor, slightly reduced the malondialdehyde content, hydrogen peroxide content and electrolyte leakage, which were induced by chilling stress and also elevated the activity of antioxidant enzymes, soluble sugar and proline levels, and reduced glutathione content in plants under chilling stress condition. Pre-treatment with other Na+ and sulfur-containing components including Na2S, Na2SO4, Na2SO3 showed no significant effect on lipid peroxidation and hydrogen peroxide content under chilling stress. It can be concluded that the effect of NaHS pretreatment on alleviation of cold stress damages is probably related to its ability to release H2S because Na+- or sulfur-containing compounds (except NaHS) had no similar effects on alleviation of chilling damages.
Keywords
- Ai L, Li ZH, Xie ZX, Tian XL, Eneji AE, Duan LS. 2008. Coronatine alleviates polyethylene glycol-induced water stress in two rice (Oryza sativa L.) cultivars. Journal of Agronomy and Crop Science 194, 360-368.
- 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 and Environment 24, 1337-1344.
- Ali B, Theodore M, Rafaqat A, Yang C, Ali SH, Muhammad K, Wu Y, Zhou W. 2014. Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regulation 74, 261-273.
- Bates L, Waldern R, Tare I. 1973. Rapid determination of free proline for water stress studies. Plant Soil 29, 205-207.
- Ben Hamed K, Castagna A, Salem E, Ranieri A, Abdelly C. 2007. Sea fennel (Crithmum maritimum L.) under salinity conditions: a comparison of leaf and root antioxidant responses. Plant Growth Regulation 53, 185-194.
- Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MS. 2014. Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environment Science Pollution Research 21, 717-731.
- Bohnert HJ, Sheveleva E. 1998. Plant stress adaptations making metabolism move. Current Opinion on Plant Biology 1, 267-274.
- Bradford, MM. 1976. Arapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochemistry 72, 248-254.
- Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL. 2011. Hydrogen sulfide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. Journal of Experimental Botany 62, 4481-4493.
10. Christou A, Manganaris GA, 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 defense pathways, Journal of Experimental Botany 64, 1953-1966.
11. Dhindsa RS, Dhindsa P, Thorpe AT. 1981. Leaf senescence correlated with increased level of membrane permeability and lipid peroxidation and decrease levels of superoxide dismutase and catalase. Journal of Experimental Botany 32, 93-101.
12. Ellman Gl. 1959. Tissue sulfydryl groups. Archive of Biochemistry and Biophysics 82, 70-77.
13. Farooq M, Basra S, Wahid A, Rehman H. 2009. Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). Journal of Agronomy and Crop Science 195, 254-261.
14. Fu P, Wang W, Hou L, Liu X. 2013. Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Society of Botanical of Poland 82, 295-302.
15. Garbero M, Pedranzani H, Zirulnik F, Molina A, Pérez-Chaca MV, Vigliocco A, Abdala G. 2011. Short-term cold stress in two cultivars of Digitaria eriantha: effects on stress-related hormones and antioxidant defense system. Acta Physiologia Plantarum 33, 497-507.
16. Hana B, Bischofa JC. 2004. Direct cell injury associated with eutectic crystallization during freezing. Cryobiology 48, 8-21.
17. Hancock J, Whiteman M. 2014. Hydrogen sulfide and cell signaling: Team player or referee? Plant Physiology and Biochemistry. 78, 37-42.
18. Heath RL, Packer L. 1968. Photoperoxidation in isolated chloroplast, kinetics and satoichiometry of fatty acid peroxidation. Archive of Biochemistry and Biophysics 125, 189-198.
19. Hosoki R, Matsuki N, Kimura H. 1997. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochemistry and Biophysics Research Communications 237, 527-531.
20. Hu X, Wang W, Li C, Zhang J, Lin F, Zhang A, Jiang M. 2008. Cross-talks between Ca2+CaM and H2O2 in abscisic acid induced antioxidant defense in leaves of maize plants exposed to water stress. Plant Growth Regulation 55, 183-198.
21. Janicka M, Reda M, Czyżewska K, Kabała K. 2017. Involvement of signaling molecules NO, H2O2 and H2S in modification of plasma membrane proton pump in cucumber roots subjected to salt or low temperature stress. Functional Plant Biology 45, 428-439.
22. 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.
23. Kuk I, Sin J, Burgos N, Hwang T, Han O, Cho B, Jung S, Guh J. 2003. Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sciences, 43, 2109-2117.
24. Lefer DJ. 2007. A new gaseous signaling molecule emerges: cardioprotective role of hydrogen sulfide. Proceeding National Academic Sciences U. S. A 104, 17907-17908.
25. Lei Y, Li C. 2007. Adaptive responses of Populus przewalskii to drought stress and SNP application. Acta Physiologia Plantarum 29, 519-526.
26. Li L, Wang Y, Shen W. 2012a. Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25, 617-631.
27. Li ZG, Ding XJ, Du PF. 2013. Hydrogen sulfide donor sodium hydrosulfide improved heat tolerance in maize and involvement of proline. Journal of Plant Physiology 170, 741-747.
28. Li ZG, 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 Sciences 185-189.
29. Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ. 2013b. Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance on maize (Zea mays L.) seedlings. Plant Cell Environment 36, 1564-1572.
30. Liu Y, Jiang H, Zhao Z, An L. 2010. Nitric oxide synthase like activity dependent nitric oxide production protects against chilling induced oxidative damage in Chorispora bungeana suspension cultured cells. Plant Physiology and Biochemistry 48, 936-944.
31. Lopez-carrion A, Castellano R, Rosales M, Ruiz J, Romero L. 2008. Role of nitric oxide under saline stress: implications on proline metabolism. Biololgia Plantarum 52, 587-591.
32. Maller P, Mckay K. Jenks B. 2002. Growing chickpea in the northern Great Plains. Montana State University press. 134-137.
33. Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach choloroplast. Plant Cell Physiology 22, 867-880.
34. Plewa M, Smith S, Wanger E. 1991. Diethyl dithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutation Research 247, 57-64.
35. Rausch T, Wachter A. 2005. Sulfur metabolism a versatile platform for launching defense operations. Trends in Plant Science 10, 503-509.
36. Roe JH. 1955. The determination of sugar in blood and spinal fluid with anthrone reagent. Journal of Chemical Biology 212, 335-343.
37. Ruelland E, Vaultier MN, Zachowski A, Hurry V, Kader JC, Delseny M. 2009.Cold signalling and cold acclimation in plants. Adverse Botanical Research 49, 35-150.
38. Shan C, Zhang SH, 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 leave under water stress. Acta Physiologia Plantarum 33, 2533-2540.
39. Shi H, Ye T, Chan Z. 2013. Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in Bermuda grass (Cynodond actylon (L). Pers.). Plant Physiology and Biochemistry 71, 226-234.
40. Shi H, Ye T, Chan Z. 2014. Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in Bermuda grass (Cynodond actylon (L). Pers.). Plant Physiology Biochemistry 74, 99-107.
41. Souri MK, Sooraki FY. 2019. Benefits of organic fertilizers spray on growth quality of chili pepper seedlings under cool temperature. Journal of plant nutrition, 42(6), 650-656.
42. 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.
43. Tambussi E, Bartoli G, Guiamet J, Beltrano J,
Araus J. 2004. Oxidative stress and photo damage at low temperatures in soybean (Glycine max L. Merr.) leaves. Plant Science 167, 19-26.
44. Uemura M, Warren G, Steponkus PL. 2003. Freezing sensitivity in the sfr4 mutant of Arabidopsis is due to low sugar content and is manifested by loss of osmotic responsiveness. Plant Physiology 131, 1800-1807.
45. Wang R. 2002. Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB 16, 1792-1798.
46. Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R. 2012. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351, 107-119.
47. Zeng Y, Yu J, Cang J, Liu L, Mu Y, Wang J, Zhang D. 2011. Detection of sugar accumulation and expression levels of correlative key enzymes in winter wheat (Triticum aestivum) at low temperatures. Bioscience, Biotechnology and Biochemistry 75, 681-687.
48. Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP. 2010a. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress, Journal of Integrative Plant Biology 50, 1518-1529.
49. Zhang S, Jiang H, Peng S, Korpelainen H, Li C. 2011. Sex-related differences in morphological, physiological, and ultra-structural responses of Populus cathayana to chilling. Journal of Experimental Botany 62, 675- 686.
50. Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY. 2009. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. Journal of Integrative Plant Biology 51, 1086-1094.
51. Zhu JH, Dong CH, Zhu JK. 2007. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Current Opinion in Plant Biology 10, 290-295.
)