硫化氢在植物中的生理功能及作用机制

doi:10.11983/CBB17099

摘要/Abstract

摘要： 硫化氢(H₂S)是继一氧化氮(NO)和一氧化碳(CO)之后第3个气体信号分子, 在植物体内参与许多重要的生理活动, 能够促进植物光合作用和有机物的积累, 缓解各种生物和非生物胁迫并促进植物生长发育。该文综述了植物体内H₂S的物理化学性质、产生机制、主要生理功能和作用机制以及与其它信号分子的互作关系, 并展望了H₂S信号分子的研究前景。

关键词: 硫化氢(H₂S), 信号分子, 生理功能, 作用机制

Abstract: Hydrogen sulfide (H₂S) is the third gas signaling molecule after nitric oxide (NO) and carbon monoxide (CO) and is of great importance in many physiological activities in plants. H₂S can promote plant photosynthesis, alleviate various stresses and promote plant growth and development. However, functional research of H₂S in plants is relatively scarce. This article summarizes the latest research of the physicochemical properties, main physiological functions and mechanism of H₂S and the interaction with other signaling molecules. Future prospects of H₂S signaling are discussed.

Key words: hydrogen sulfide (H₂S), signal molecule, physiological function, mechanism

尚玉婷, 张妮娜, 上官周平, 陈娟. 硫化氢在植物中的生理功能及作用机制. 植物学报, 2018, 53(4): 565-574.

Shang Yuting, Zhang Nina, Shangguan Zhouping, Chen Juan. Physiological Function and Mechanism of Hydrogen Sulfide in Plants. Chinese Bulletin of Botany, 2018, 53(4): 565-574.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB17099

https://www.chinbullbotany.com/CN/Y2018/V53/I4/565

图/表 2

参考文献 68

1	崔为体, 沈文飚 (2012). 植物中硫化氢的生理功能及其分子机理. 生命的化学 32, 385-389.
2	侯智慧, 刘菁, 侯丽霞, 李希东, 刘新 (2011). H2S可能作为H2O2的下游信号介导茉莉酸诱导的蚕豆气孔关闭. 植物学报 46, 396-406.
3	李东波, 肖朝霞, 刘灵霞, 王金成, 宋国力, 毕玉蓉 (2010). 外源硫化氢对豌豆根尖及其边缘细胞的影响. 植物学报 45, 354-362.
4	李顺, 景举伟, 严金平, 陈宣钦, 徐慧妮 (2015). 气体信号分子H2S在植物中的研究进展. 植物生理学报 51, 579-585.
5	刘志强, 裴雁曦, 方慧慧, 田保华 (2015). H2S巯基化修饰蛋白质调节谷子响应逆境胁迫. 中国生物化学与分子生物学报 31, 1085-1091.
6	裴雁曦 (2016). 植物中的气体信号分子硫化氢: 无香而立, 其臭如兰. 中国生物化学与分子生物学报 32, 721-733.
7	单长卷, 赵元增 (2015). 外源硫化氢对干旱胁迫下玉米幼苗水分生理特性的影响. 干旱地区农业研究 33, 81-84, 231.
8	孙晓莉, 姜倩倩, 田寿乐, 许林, 沈广宁 (2016). 新型气体信号分子H2S在植物中的研究进展. 山东农业科学 48(9), 151-156, 161.
9	王鸿蕉, 张丽萍, 刘志强, 刘旦梅, 金竹萍, 裴雁曦 (2015). 外源硫化氢对冷胁迫下白菜幼苗生长和光合作用的影响. 西北植物学报 35, 780-786.
10	于立旭, 尚宏芹, 张存家, 王秀峰, 魏珉, 杨凤娟, 史庆华 (2011). 外源硫化氢对镉胁迫下黄瓜胚轴和胚根生理生化特性的影响. 园艺学报 38, 2131-2139.
11	朱会朋, 孙健, 赵楠, 马旭君, 张玉红, 沈昕, 陈少良 (2013). 盐胁迫下硫化氢调控杨树根系的离子流. 植物生理学报 49, 561-567.
12	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.Eco- tox Environ Safe 102, 25-33.
13	Aroca Á, Serna A, Gotor C, Romero LC (2015). S-sulfhy- dration: a cysteine posttranslational modification in plant systems.Plant Physiol 168, 334-342.
14	Baudouin E, Poilevey A, Hewage NI, Cochet F, Puyaubert J, Bailly C (2016). The significance of hydrogen sulfide for Arabidopsis seed germination.Front Plant Sci 7, 930.
15	Chen J, Shang YT, Wang WH, Chen XY, He EM, Zheng HL, Shangguan ZP (2016a). Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seed- lings. Front Plant Sci 7, 1173.
16	Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015a). Hydrogen sulfide enhances salt tole- rance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots.Sci Rep 5, 12516.
17	Chen J, Wu FH, Shang YT, Wang WH, Hu WJ, Simon M, Liu X, Shangguan ZP, Zheng HL (2015b). Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency. J Exp Bot 66, 6605-6622.
18	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.
19	Chen XD, Chen Q, Zhang XM, Li RJ, Jia YJ, Ef AA, Jia AQ, Hu XW (2016b). Hydrogen sulfide mediates nicotine biosynthesis in tobacco (Nicotiana tabacum) under high temperature conditions. Plant Physiol Biochem 104, 174-179.
20	Chen Z, Chen MS, Jiang M (2017). Hydrogen sulfide alleviates mercury toxicity by sequestering it in roots or regulating reactive oxygen species productions in rice seedlings.Plant Physiol Biochem 111, 179-192.
21	Cui WT, Chen HP, Zhu KK, Jin QJ, Xie YJ, Cui J, Xia Y, Zhang J, Shen WB (2014). Cadmium-induced hydrogen sulfide synthesis is involved in cadmium tolerance in Me- dicago sativa by reestablishment of reduced (Homo) glutathione and reactive oxygen species homeostases. PLoS One 9, e109669.
22	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 Grow- th Regul 79, 391-399.
23	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 Re- gul 75, 33-44.
24	Fang T, Cao ZY, Li JL, Shen WB, Huang LQ (2014). Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato.Plant Physiol Biochem 76, 44-51.
25	García-Mata C, Lamattina L (2010). Hydrogen sulphide, a novel gasotransmitter involved in guard cell signaling.New Phytol 188, 977-984.
26	Hu HL, Liu D, Li PX, Shen WB (2015). Hydrogen sulfide delays leaf yellowing of stored water spinach (Ipomoea aquatica) during dark-induced senescence by delaying chlorophyll breakdown, maintaining energy status and increasing antioxidative capacity. Postharv Biol Technol 108, 8-20.
27	Jin ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011). Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414, 481-486.
28	Jin ZP, Wang ZQ, Ma QX, Sun LM, Zhang LP, Liu ZQ, Liu DM, Hao XF, Pei YX (2017). Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana. Plant Soil 419, 141-152.
29	Jin ZP, Xue SW, Luo YA, Tian BH, Fang HH, Li H, Pei YX (2013). Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis.Plant Physiol Biochem 62, 41-46.
30	Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hänsch R, Mendel RR, Meyer AJ, Wirtz M, Hell R (2010). Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Ara- bidopsis thaliana. Plant Cell 22, 1216-1231.
31	Kimura H (2002). Hydrogen sulfide as a neuromodulator.Mol Neurobiol 26, 13-19.
32	Lai DW, Mao Y, Zhou H, Li F, Wu MZ, Zhang J, He ZY, Cui WT, Xie YJ (2014). Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa. Plant Sci 225, 117-129.
33	Li JS, Jia HL, Wang J, Cao QH, Wen ZC (2014). Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251, 899-912.
34	Li ZG, Ding XJ, Du PF (2013a). Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline.J Plant Physiol 170, 741-747.
35	Li ZG, Gong M, Liu P (2012a). Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas. Acta Physiol Plant 34, 2207-2213.
36	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 Sci 185-186, 185-189.
37	Li ZG, Xie LR, Li XJ (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.
38	Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b). 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.
39	Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012). Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation.J Plant Growth Regul 31, 519-528.
40	Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010). A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation.Plant Phy- siol Biochem 48, 931-935.
41	Liu J, Hou LX, Liu GH, Liu X, Wang XC (2011). Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull 56, 3547-3553.
42	Liu J, Hou ZH, Liu GH, Hou LX, Liu X (2012). Hydrogen sulfide may function downstream of nitric oxide in ethy- lene-induced stomatal closure in Vicia faba L. J Integr Agric 11, 1644-1653.
43	Liu X, Chen J, Wang GH, Wang WH, Shen ZJ, Luo MR, Gao GF, Simon M, Ghoto K, Zheng HL (2016). Hydrogen sulfide alleviates zinc toxicity by reducing zinc uptake and regulating genes expression of antioxidative enzymes and metallothioneins in roots of the cadmium/zinc hyperaccumulator Solanum nigrum L. Plant Soil 400, 177-192.
44	Müller M, De Kok LJ, Weidner W, Tausz M (2002). Differential effects of H2S on cytoplasmic and nuclear thiol concentrations in different tissues of Brassica roots. Plant Phy- siol Biochem 40, 585-589.
45	Papanatsiou M, Scuffi D, Blatt MR, García-Mata C (2015). Hydrogen sulfide regulates inward-rectifying K+ channels in conjunction with stomatal closure.Plant Physiol 168, 29-35.
46	Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007). Characterization of cysteinede- grading and H2S-releasing enzymes of higher plants from the field to the test tube and back.Plant Biol 9, 582-588.
47	Peng RY, Bian ZY, Zhou LN, Cheng W, Hai N, Yang CQ, Yang T, Wang XY, Wang CY (2016). Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.). Plant Cell Rep 35, 2325-2340.
48	Qiao ZJ, Jing T, Liu ZQ, Zhang LP, Jin ZP, Liu DM, Pei YX (2015). H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis.Plant Soil 393, 137-146.
49	Scuffi D, Álvarez C, Laspina N, Gotor C, Lamattina L, García-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.
50	Shan C, Liu H, Zhao L, Wang X (2014). Effects of exogenous hydrogen sulfide on the redox states of ascorbate and glutathione in maize leaves under salt stress.Biol Plant 58, 169-173.
51	Shen JJ, Xing TJ, Yuan HH, Liu ZQ, Jin ZP, Zhang LP, Pei YX (2013). Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS One 8, e77047.
52	Shi HT, Ye TT, Chan ZL (2014). Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon(L). Pers.). Plant Phy- siol Biochem 74, 99-107.
53	Shi HT, Ye TT, Han N, Bian HW, Liu XD, Chan ZL (2015). Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis.J Integr Plant Biol 57, 628-640.
54	Singh VP, Singh S, Kumar J, Prasad SM (2015). Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: possible involvement of nitric oxide.J Plant Physiol 181, 20-29.
55	Wang BL, Shi L, Li YX, Zhang WH (2010). Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231, 1301-1309.
56	Wang R (2012). Physiological implications of hydrogen sulfide: a whiff exploration that blossomed.Physiol Rev 92, 791-896.
57	Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012). Hydrogen sulfide enhances alfalfa (Medicago sativa) tole- rance against salinity during seed germination by nitric oxide pathway. Plant Soil 351, 107-119.
58	Wilson LG, Bressan RA, Filner P (1978). Light-dependent emission of hydrogen sulfide from plants.Plant Physiol 61, 184-189.
59	Xie YJ, Zhang C, Lai DW, Sun Y, Samma MK, Zhang J, Shen WB (2014). Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression.J Plant Physiol 171, 53-62.
60	Yang GD, Wu LY, Jiang B, Yang W, Qi JS, Cao K, Meng QH, Mustafa AK, Mu WT, Zhang SM, Snyder SH, Wang R (2008). H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase.Science 322, 587-590.
61	Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008). Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress.J Integr Plant Biol 50, 1518-1529.
62	Zhang H, Hu LY, Li P, Hu KD, Jiang CX, Luo JP (2010a). Hydrogen sulfide alleviated chromium toxicity in wheat.Biol Plant 54, 743-747.
63	Zhang H, Hu SL, Zhang ZJ, Hu LY, Jiang CX, Wei ZJ, Liu J, Wang HL, Jiang ST (2011). Hydrogen sulfide acts as a regulator of flower senescence in plants.Postharvest Biol Technol 60, 251-257.
64	Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010b). Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress.Acta Physiol Plant 32, 849-857.
65	Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010c). Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings.J Integr Plant Biol 52, 556-567.
66	Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a). Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51, 1086-1094.
67	Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b). Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative da- mage against osmotic stress.Plant Growth Regul 58, 243-250.
68	Zhao JQ, Li S, Jiang TF, Liu Z, Zhang WW, Jian GL, Qi FJ (2012). Chilling stress—the key predisposing factor for causing Alternaria alternata infection and leading to cotton(Gossypium hirsutum L.) leaf senescence. PLoS One 7, e36126.

参与过程	生理功能	植物	参考文献
促进形态建成	种子萌发	小麦、麻风树和黄瓜	Zhang et al., 2008; 于立旭等, 2011; Li et al., 2012a
促进形态建成	根的形成	豌豆、番薯和番茄	Zhang et al., 2009a; 李东波等, 2010; Fang et al., 2014
调节生理生化过程	气孔调节	蚕豆、凤仙和拟南芥	García-Mata and Lamattina, 2010; Lisjak et al., 2010; Liu et al., 2012; Jin et al., 2017
	光合作用	甘薯、菠菜、水稻和玉米	Zhang et al., 2009b; Chen et al., 2011, 2015b; Duan et al., 2015
	物质代谢	拟南芥和豌豆	Müller et al., 2002; 李东波等, 2010; Shi et al., 2015
	延缓衰老	水蕹菜	Hu et al., 2015
缓解非生物胁迫	干旱胁迫	番薯、大豆、拟南芥、蚕豆、苏丹凤仙花、玉米和菠菜	Zhang et al., 2009b, 2010b; García-Mata and Lamattina, 2010; Jin et al., 2011; 单长卷和赵元增, 2015; Chen et al., 2016a
	盐胁迫	拟南芥、玉米、紫花苜蓿、杨树、小麦和大麦	Wang et al., 2012; 朱会朋等, 2013; Li et al., 2014; Shan et al., 2014; Lai et al., 2014; Chen et al., 2015a; Deng et al., 2016
	高、低温胁迫	玉米、烟草和白菜	Li et al., 2012b, 2013a, 2013b; 王鸿蕉等, 2015; Chen et al., 2016b
	重金属胁迫	黄瓜、小麦、苜蓿、豌豆、龙葵、油菜和水稻	Zhang et al., 2008, 2010a, 2010c; Wang et al., 2010; Ali et al., 2014; Shi et al., 2014; Cui et al., 2014; Singh et al., 2015; Liu et al., 2016; Chen et al., 2017

参与过程	生理功能	植物	参考文献
促进形态建成	种子萌发	小麦、麻风树和黄瓜	Zhang et al., 2008; 于立旭等, 2011; Li et al., 2012a
促进形态建成	根的形成	豌豆、番薯和番茄	Zhang et al., 2009a; 李东波等, 2010; Fang et al., 2014
调节生理生化过程	气孔调节	蚕豆、凤仙和拟南芥	García-Mata and Lamattina, 2010; Lisjak et al., 2010; Liu et al., 2012; Jin et al., 2017
	光合作用	甘薯、菠菜、水稻和玉米	Zhang et al., 2009b; Chen et al., 2011, 2015b; Duan et al., 2015
	物质代谢	拟南芥和豌豆	Müller et al., 2002; 李东波等, 2010; Shi et al., 2015
	延缓衰老	水蕹菜	Hu et al., 2015
缓解非生物胁迫	干旱胁迫	番薯、大豆、拟南芥、蚕豆、苏丹凤仙花、玉米和菠菜	Zhang et al., 2009b, 2010b; García-Mata and Lamattina, 2010; Jin et al., 2011; 单长卷和赵元增, 2015; Chen et al., 2016a
	盐胁迫	拟南芥、玉米、紫花苜蓿、杨树、小麦和大麦	Wang et al., 2012; 朱会朋等, 2013; Li et al., 2014; Shan et al., 2014; Lai et al., 2014; Chen et al., 2015a; Deng et al., 2016
	高、低温胁迫	玉米、烟草和白菜	Li et al., 2012b, 2013a, 2013b; 王鸿蕉等, 2015; Chen et al., 2016b
	重金属胁迫	黄瓜、小麦、苜蓿、豌豆、龙葵、油菜和水稻	Zhang et al., 2008, 2010a, 2010c; Wang et al., 2010; Ali et al., 2014; Shi et al., 2014; Cui et al., 2014; Singh et al., 2015; Liu et al., 2016; Chen et al., 2017

[1]	杜志烨, 李明玉, 陈稷, 黄进. 植物胁迫相关蛋白功能研究进展[J]. 植物学报, 2024, 59(1): 110-121.
[2]	张标, 吴健, 张杨, 董小卫, 韩硕, 高昕, 杜从伍, 李慧英, 种学法, 朱莹莹, 刘海伟. 木栓层在水和溶质运输中的生理功能研究进展[J]. 植物学报, 2023, 58(6): 1008-1018.
[3]	龚容, 高琼. 叶片结构的水力学特性对植物生理功能影响的研究进展[J]. 植物生态学报, 2015, 39(3): 300-308.
[4]	吴林坤, 林向民, 林文雄. 根系分泌物介导下植物-土壤-微生物互作关系研究进展与展望[J]. 植物生态学报, 2014, 38(3): 298-310.
[5]	田世平. 果实成熟和衰老的分子调控机制[J]. 植物学报, 2013, 48(5): 481-488.
[6]	董秀梅, 晁青, 王柏臣. 植物磷酸烯醇式丙酮酸羧激酶(PEPCK)研究进展[J]. 植物学报, 2013, 48(3): 320-328.
[7]	顿新鹏　陈正望. 碱性7S 球蛋白和豆类胰岛素研究进展[J]. 植物学报, 2005, 22(增刊): 68-74.
[8]	王忠华;贾育林;夏英武. 植物抗病分子机制研究进展[J]. 植物学报, 2004, 21(05): 521-530.
[9]	安华明陈力耕樊卫国胡西琴. 高等植物中维生素C 的功能、合成及代谢研究进展[J]. 植物学报, 2004, 21(05): 608-617.
[10]	童建松阳振乐李良璧匡廷云. 光合膜膜脂双半乳糖二酰基甘油的研究进展[J]. 植物学报, 2003, 20(05): 531-538.
[11]	孙清鹏王小菁. 植物伤反应中的茉莉酸类信号[J]. 植物学报, 2003, 20(04): 481-488.
[12]	何龙飞刘友良沈振国王爱勤. 植物离子通道特征、功能、调节与分子生物学[J]. 植物学报, 1999, 16(05): 517-525.