Chinese Bulletin of Botany ›› 2012, Vol. 47 ›› Issue (3): 217-225.doi: 10.3724/SP.J.1259.2012.00217

Previous Articles     Next Articles

H2S Induced by H2O2 Mediates Drought-induced Stomatal Closure in Arabidopsis thaliana

Lanxiang Wang, Zhihui Hou, Lixia Hou, Fanggui Zhao, Xin Liu*   

  1. Key Laboratory of Plant Biotechnology in Universities of Shandong, College of Life Science, Qingdao Agricultural University, Qingdao 266109, China
  • Received:2011-09-01 Revised:2011-12-20 Online:2012-07-06 Published:2012-05-01
  • Contact: Xin Liu
  • Supported by:

    the National Science Foundation

Abstract: Using the Arabidopsis thaliana wild-type; mutants atrbohD, atrbohF, atrbohD/F, atl-cdes, and atd-cdes; and D-/L-cysteine desulfhydrase overexpression plants, we investigated the roles of hydrogen sulfide (H2S) in drought-induced stomatal closure in A. thaliana. We used a pharmacological experiment combined with laser scanning confocal microscopy and spectrophotography. The H2S scavenger hypotaurine and H2S synthesis inhibitors aminooxy acetic acid, hydroxylamine, potasium pyruvate and ammonia all inhibited drought-induced stomatal closure. Drought-induced stomatal closure was greater in overexpression than wild-type plants, with the effect not obvious in atl-cdes and atd-cdes. Moreover, drought stress enhanced the level of hydrogen peroxide (H2O2) in guard cells and increased the content of H2S and the activity and expression of D-/L-cysteine desulfhydrase in leaves but had no significant effect in atrbohD, atrbohF, and atrbohD/F. The H2O2 scavenger decreased drought-induced H2S production and the activity of D-/L-cysteine desulfhydrase in leaves. H2S may function downstream of H2O2 in the signal transduction pathway of drought-induced stomatal closure in A. thaliana.

CLC Number: 

  • Q945

刘新, 张蜀秋, 娄成后(2003). Ca2+参与NO对蚕豆气孔运动的调控. 植物生理与分子生物学学报 29, 342-346.
安国勇, 宋纯鹏, 张骁, 荆艳彩, 阳冬梅, 黄美娟, 周培爱, 吴才宏 (2000). 过氧化氢对蚕豆气孔运动和质膜K+通道的影响. 植物生理学报 26, 458-464.
高巍, 尚忠林(2010). 细胞内离子在气孔运动中的作用. 植物学报45, 632-639.
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
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.
刘国华, 刘菁, 侯丽霞, 唐静, 刘新(2009). NO可能作为Ca2+的下游信号介导乙烯诱导的蚕豆气孔关闭. 分子细胞生物学报42, 145-155.
刘菁, 侯智慧, 赵方贵, 刘新(2011). H2S参与ABA诱导的蚕豆气孔关闭. 西北植物学报, 31, 298-304
张岁歧, 李金虎, 山仑(2001). 干旱下植物气孔运动的调控. 西北植物学报21, 1263-1270.
Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ(2006). Ethylene-induced stomatal closure in Arabidopsis occurs via atrbohF-mediated hydrogen peroxide synthesis. Plant J 6, 907-916.
Frandsen G, Müller-Uri F, Nielsen M, Mundy J, Skriver K(1996). Novel plant Ca2+-binding protein expressed in response to abscisic acid and osmotic stress. J Biol Chem 271, 343-348.
García-Mata C, Lamattina L(2010). Hydrogen sulphide, a novel gasotransmitter involved in guard cell signaling. New Phytolohist 188, 977-984.
Kajimura M, Fukuda R, Bateman RM, Yamamoto T, Suematsu M(2010).Interactions of multiple gas-transducing systems: hallmarks and uncertainties of CO, NO, and H2S gas biology. Antioxid Redox Signal 13, 157-192.
Kolla VA, Vavasseur A, Raghavendra AS (2007). Hydrogen peroxide production is an early event during bicarbonate induced stomatal closure in abaxial epidermis of Arabidopsis. Planta 225, 1421-1429.
Lowicka E, Betowski J(2007). Hydrogen sulfide (H2S)-the third gas of interest for pharmacologists. Pharmacol Rep 59, 14-24.
Mata G C, Lamattina L(2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126, 1196-1204.
McAinsh MR, Clayton H, Mansfield TA, Hetherington AM(1996). Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111, 1031-1042.
Munemasa S, Oda K, Watanabe-Sugimoto M, NakamuraY, Shimoishi Y, Murata Y (2007). The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Speci?c impairment of ion channel activation and second messenger production. Plant physiol 143, 1398-1407.
Mustilli A C, Merlot S, Vavasseur A, Fenzi F, Giraudat J(2002). Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14, 3089-3099.
Pei Z M, Murata Y, Benning G, Thomine S, Klmiener B, Allen G J, Grill E, Schroeder J L(2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406, 731-734.
Riemenschneider A, Nikiforova V, Hoefgen R, Luit J, Kok D, Papenbrock J (2005). Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43, 473-483.
Seemann JR, Critehley C(1985). Effect of salt Stress on the growth,ion content,stomatal behavior and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164, 151-162. Sekiya J, Schmidt A, Wilson LG, Filner P (1982). Emission of hydrogen sulfide by leaf tissue in response to L-Cysteine. Plant Physiol 70, 430-436.
Stuiver CEE, De Kok LJ, Kuiper PJC(1992). Freezing tolerance and biochemical changes in wheat shoots as affected by H2S fumigation. Plant Physiol Biochem 30, 47-55.
Tan BH, Wong PT, Bian JS(2010).Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56, 3-10.
Yong QC, Choo CH, Tan BH, Low CM, Bian JS (2010).Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells. Neurochem Int 56, 508-515.
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.
Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009). Hydrogen sul?de counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58, 243-250.
Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010). Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings.J Integr Plant Biol 52, 556-567.
Zhang X, Dong FC, Gao JF, Song CP (2001). Hydrogen peroxide-induced changes in intracellular pH of guard cells precede stomatal closure. Cell Res 11, 37-43.
Zhao Z, Chen G, Zhang C(2001). Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Aust J plant Physiol 28, 1055-1061.
[1] Baozhu Li, Xiaoliang Zhao, Lei Peng. Research Advances in the Development and Regulation of Plant Chloroplasts [J]. Chinese Bulletin of Botany, 2014, 49(3): 337-345.
[2] Xueqin Wei, Changfeng Zhang, Jie Pang, Dandan Kou, Run Lan. Research Progress in the Chemistry and Structure of Plant Cuticles Related to Water Permeability [J]. Chinese Bulletin of Botany, 2013, 48(5): 573-587.
[3] Longying Wen, Tuo Chen. Changes of Pigments in Sabina przewalskii and Picea crassifolia Needles Along with Different Altitudes [J]. Chinese Bulletin of Botany, 2012, 47(4): 405-412.
[4] Chenghou Wu, Dongmei Li, Huiqiao Tian. Isolation of Zygotes and Proembryos in Doritis pulcherrima [J]. Chinese Bulletin of Botany, 2012, 47(3): 286-291.
[5] Yanming Miao, Jinzhi Lü, Runcheng Bi, Guiqin Yan. Dynamic Changes of Traits of Leaves from Elaeagnus mollis [J]. Chinese Bulletin of Botany, 2012, 47(3): 257-263.
[6] Zhihui Hou, Jing Liu, Lixia Hou, Xidong Li, Xin Liu. H2S May Function Downstream of H2O2 in Jasmonic Acid-induced Stomatal Closure in Vicia faba [J]. Chinese Bulletin of Botany, 2011, 46(4): 396-406.
Full text



[1] Yu Feng-lan;Wang Jing-ping;Li Jing-min and Shan Xue-qin. The Isolation and Identification of Sterols and Other Constituents from Seed Fat of Sapium sebiferum[J]. Chinese Bulletin of Botany, 1989, 6(02): 121 -123 .
[2] LI Al-Fen;CHEN Min amd ZHOU Bai-Cheng. Advances and Problems in Studies of Photosynthetic Pigment-Protein Complexes of Brown Algae[J]. Chinese Bulletin of Botany, 1999, 16(04): 365 -371 .
[3] CHEN Xiao-Mei and GUO Shun-Xing. Research Advances in Plant Disease Resistive Material[J]. Chinese Bulletin of Botany, 1999, 16(06): 658 -664 .
[4] LI Ji-Quan JIN You-Ju SHEN Ying-Bai HONG Rong. The Effect of Environmental Factors on Emission of Volatile Organic Compounds from Plants[J]. Chinese Bulletin of Botany, 2001, 18(06): 649 -656 .
[5] . [J]. Chinese Bulletin of Botany, 2005, 22(增刊): 157 .
[6] Jianxia Li, Chulan Zhang, Xiaofei Xia, Liangcheng Zhao. Cryo-sectioning Conditions and Histochemistry Comparison with Paraffin Sectioning[J]. Chinese Bulletin of Botany, 2013, 48(6): 643 -650 .
[7] JIANG Yang-Ming, CUI Wei-Hong, and DONG Qian-Lin. Comprehensive evaluation and analysis of tobacco planting environment based on space technology[J]. Chin J Plan Ecolo, 2012, 36(1): 47 -54 .
[8] Hu Cheng-biao, Zhu Hong-guang, Wei Yuan-lian. A Study on Microorganism and Biochemical Activity of Chinese-fir Plantation on Different Ecological Area in Guangxi[J]. Chin J Plan Ecolo, 1991, 15(4): 303 -311 .
[9] Hong-Xin SU Fan BAI Guang-Qi LI. Seasonal dynamics in leaf area index in three typical temperate montane forests of China: a comparison of multi-observation methods[J]. Chin J Plan Ecolo, 2012, 36(3): 231 -242 .
[10] AN Ran, GONG Ji-Rui, YOU Xin, GE Zhi-Wei, DUAN Qing-Wei, YAN Xin. Seasonal dynamics of soil microorganisms and soil nutrients in fast-growing Populus plantation forests of different ages in Yili, Xinjiang, China[J]. Chin J Plan Ecolo, 2011, 35(4): 389 -401 .