Welcome to Acta Agronomica Sinica,

Acta Agron Sin ›› 2010, Vol. 36 ›› Issue (3): 533-538.doi: 10.3724/SP.J.1006.2010.00533

• RESEARCH ACTIVITIES • Previous Articles    

Cytoplasmic Alkalization Mediates Exogenous Nitric Oxide-Induced Stomatal Closure in Vicia faba

ZHAO Shi-Ling,SUN Li-Rong,ZHANG Huan,MA Li-Ya,LU Bao-Shi,HAO Fu-Shun*   

  1. Henan Key Laboratory of Plant Stress Biology, College of Life Sciences, Henan University, Kaifeng 475004, China
  • Received:2009-07-17 Revised:2009-12-08 Online:2010-03-12 Published:2010-01-22
  • Contact: HAO Fu-Shun, E-mail: haofsh@henu.edu.cn

Abstract:

The effects of exogenous NO on changes in cytosolic pH of guard cells from epidermal fragments and of the pH on NO-induced stomatal closure in Vicia faba were investigated by using a pH specific fluorescence probe SNARF-1-AM and a confocal laser scanning microscopy. The results showed that treatments with 100 μmol L–1 sodium nitroprusside (SNP), a widely used NO donor, led to a significant increase in cytosolic pH (from 6.91 to 7.19, i.e. 0.28 pH unit) and stomatal closure in comparison with the control. Furthermore, SNP-induced cytosolic alkalization and stomatal closure were significantly inhibited by NO scavenger c-PTIO or weak acid butyrate, and promoted by the weak base benzylamine. Whereas two structural analogs of SNP such as Fe(II)CN and Fe(III)CN, which can not release NO, failed to induce guard cell cytoplasmic alkalization and stomatal closure. These findings suggest that cytoplasmic alkalization of guard cells mediates NO-induced stomatal closure. In addition, pH in guard cell vacuoles and cell walls was measured during the cytosolic alkalization. However, no significant changes of pH in the two regions were found, implying that the cytoplasmic protons of guard cells may not go into vacuoles or cell walls during the NO-promoted alkalization in Vicia faba.

Key words: Nitric oxide, pH, Vicia faba, Stomatal closure

[1] Lamattina L, García-Mata C, Graziano M, Pagnussat G. Nitric oxide: The versatility of an extensive signal molecule. Annu Rev Plant Biol, 2003, 54: 109-136

[2] Neill S J, Desikan R, Hancock J T. Nitric oxide signalling in plants. New Phyt, 2003, 159: 11-35

[3] Delledonne M. NO news is good news for plants. Curr Opin Plant Biol, 2005, 8: 390-396

[4] Liu W-Z(刘维仲), Zhang R-J(张润杰), Pei Z-M(裴真明), He Y-Q(何奕昆). Investigation on functions of nitric oxide as a signal molecular in plants: Advance and perspective. Prog Nat Sci (自然科学进展), 2008, 18 (1): 10-24 (in Chinese)

[5] Liu X, Zhang S Q, Lou C H. Involvement of nitric oxide in the signal transduction of salicylic acid regulating stomatal movement. Chin Sci Bull, 2003, 48: 449-452

[6] Liu X, Shi W L, Zhang S Q, Lou C H. Nitric oxide involved in signal transduction of jasmonic acid-induced stomatal closure of Vicia faba L. Chin Sci Bull, 2005, 50: 520-525

[7] Melotto M, Underwood W, Koczan J, Nomura K, He S Y. Plant stomata function in innate immunity against bacterial invasion. 2006, Cell, 126: 969-980

[8] Garcia-Mata C, Lamattina L. Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide, 2007, 17: 143-151

[9] Kolla V A, Raghavendra A S. Nitric oxide as an intermediate in bicarbonate-induced stomatal closure in Pisum sativum. Physiol Plant, 2007, 130: 91-98

[10] Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y. The coronatine-insensitive 1 mutation reveals the hormone signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiol, 2007, 143: 1398-1407

[11] Zhang X, Takemiya A, Kinoshita T, Shimazaki K. Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signaling pathways in Vicia guard cells. Plant Cell Physiol, 2007, 48: 715-723

[12] Song X G, She X P, Zhang B. Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiol Plant, 2008, 132: 514-525

[13] Desikan R, Griffiths R, Hancock J, Neill S. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA,2002, 99: 16314-16318

[14] Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I. Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot, 2008, 59: 165-176

[15] Lü D(吕东), Zhang X(张骁), Jiang J(江静), An G-Y(安国勇), Zhang L-R(张玲瑞), Song C-P(宋纯鹏). NO may function in the downstream of H2O2 in ABA-induced stomatal closure in Vicia faba L. Acta Phytophysiol Sin (植物生理与分子生物学学报), 2005, 31(1): 62–70 (in Chinese with English abstract)

[16] Bright J, Desikan R, Hancock J T, Weir L S, Neill S J. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J, 2006, 45: 113-122

[17] Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt M R. Nitric oxide regulates K+ and Cl– channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA, 2003, 100: 11116-11121

[18] Sokolovski S, Blatt M R. Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol, 2004, 136: 4275-4284

[19] Wilkinson S. pH as a stress signal. Plant Growth Regul, 1999, 29: 87-99

[20] Felle H H. pH: Signal and messenger in plant cells. Plant Biol, 2001, 3: 577-591

[21] Irving H R, Gehring C A, Parish R W. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA, 1992, 89: 1790-1794

[22] Blatt M R, Armstrong F. K+ channels of stomatal guard cells: Abscisic acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta, 1993, 191: 330-341

[23] Gehring C A, Irving H R, McConchie R, Parish R W. Jasmonates induce intracellular alkalization and closure of Paphiopedilum guard cell. Ann Bot, 1997, 80: 485-489

[24] Grabov A, Blatt M R. Parallel control of the inward rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells. Planta, 1997, 201: 84-95

[25] Suhita D, Raghavendra A S, Kwak J M, Vavasseur A. Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol, 2004, 134: 1536-1545

[26] Gonugunta V K, Srivastava N, Puli M R, Raghavendra A S. Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid. Plant Cell Environ, 2008, 31: 1717-1724

[27] Li S, Assmann S M, Albert R. Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol, 2006, 4: 1732-1747

[28] Zhang X, Dong F C, Gao J F, Song C P. Hydrogen peroxide-induced changes in intracellular pH of guard cells precede stomatal closure. Cell Res, 2001, 11: 37-43

[29] Kwak J M, Mori I C, Pei Z M, Leonhardt N, Torres M A, Dangl J L, Bloom R E, Bodde S, Jones J D, Schroeder J I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J, 2003, 22: 2623-2633

[30] Torres M A, Dangl J L. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol, 2005, 8: 397-403

[31] Rober-Kleber N, Albrechtova J T, Fleig S, Fleig S, Huck N, Michalke W, Wagner E, Speth V, Neuhaus G, Fischer-Iglesias C. Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiol, 2003, 131: 1302-1312

[32] Bethke P C, Libourel I G L, Reinöhl V, Jones R L. Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta, 2006, 223: 805-812

[1] Liu En-Bo, Chen Jing, Li Hong-Xing, Yu Ning-Ning, Ren Bai-Zhao, Zhao Bin, Liu Peng, Zhang Ji-Wang. Shading inhibits ear and tassel development of summer maize by altering source-sink balance and regulating carbohydrate metabolism [J]. Acta Agronomica Sinica, 2026, 52(6): 1891-1901.
[2] Ma Xiao-Qian, Qin Na, Dai Shu-Tao, Qin Jia-Fan, Li Xiao-Yan, Wang Shu-Ting, Liu Zhong-Ling, Li Jun-Xia. Phenotypic variation analysis of 175 foxtail millet (Setaria italica) germplasm accessions under two environments [J]. Acta Agronomica Sinica, 2026, 52(6): 1757-1773.
[3] Jin Yu-He, Wang Xue-Fei, Xu Zhang-Yi-Wa, Miao Yi-Ning, Jiang Yun-Jie, Yi Ying, Miao De-Lin, Zhu Jing-Yi, Zhong Yi-Fan, Chen Ming-Heng, Fang Fang, Liu Peng. Effects of exogenous hormones on chlorophyll fluorescence parameters and the antioxidant enzyme system in soybean leaves under low-temperature stress [J]. Acta Agronomica Sinica, 2026, 52(6): 1817-1829.
[4] Hu Zhao, Qian Run, Xie Feng-Pu, Ying Su-Ping. Genome-wide identification and expression analysis of the SPX gene family in rice under phosphorus treatment [J]. Acta Agronomica Sinica, 2026, 52(6): 1902-1912.
[5] Zhang Si-Si, Zhao Xiang-Hui, Zhou Yang, Yao Yun-Feng, Zhu Rong-Yu, Dong Yuan-Jie, Hu Guo-Qing, Xu Tong, Liu Zhao-Xin. Effects of plowing and green manure returning in winter fallow period on soil physicochemical properties and yield in continuously cropped peanut [J]. Acta Agronomica Sinica, 2026, 52(5): 1472-1486.
[6] Ren Yi-Han, Zhao Man-Li, Dai Jing, Li Yin-Shui, Gu Chi-Ming, Yang Lu, Du Xue-Zhu, Hu Wen-Shi, Qin Lu. Effects of dynamic changes in leaf functional nitrogen on photosynthetic rate and photosynthetic nitrogen use efficiency in Brassica napus [J]. Acta Agronomica Sinica, 2026, 52(5): 1459-1471.
[7] Zhao Jia-Xue, Zhou Long-Hao, Guo Qi-Yuan, Shang Lun-Xiao, Wang Han, Liu Zhi-Tao, Chen Xi, Zhang Xiao-Pei, Song Xian-Liang, Ahmedov Miraziz Baltaevich, Mao Li-Li. Long-term stubble return and subsoiling enhance cotton yields in coastal saline-alkali soils by improving soil conditions and photosynthetic characteristics [J]. Acta Agronomica Sinica, 2026, 52(5): 1548-1560.
[8] Yang Yang, Chang Shi-Hui, Tian Hong-Li, Yi Hong-Mei, Wang Lu, Ren Jie, Fan Ya-Ming, Liu Ya-Wei, Wang Feng-Ge, Zhao Jiu-Ran. Genetic diversity analysis of nationally approved maize varieties in different ecological regions [J]. Acta Agronomica Sinica, 2026, 52(5): 1352-1364.
[9] Guo Xing-Yu, Hu Dan, Lin Su-Qi, Wang Meng-Kai, Tan Wen-Feng, Huang Chuan-Qin. Biochar combined with chemical fertilizer increases maize yield and soil ecosystem multifunctionality in an intercropped maize-soybean [J]. Acta Agronomica Sinica, 2026, 52(5): 1536-1547.
[10] Zhang Hong-Rong, Wang Fei-Er, Li Pan, Qiu Hai-Long, Zhu Jing, Zhao Lian-Hao, Nan Yun-You, He Wei, Fan Zhi-Long, Hu Fa-Long, Chai Qiang, Yin Wen. Photosynthetic characteristics of 20% reduced irrigation combined with 25% organic substitution for chemical fertilizer in increasing silage maize yield [J]. Acta Agronomica Sinica, 2026, 52(5): 1487-1500.
[11] Zhang Zhen, Feng Lian-Jie, Shi Yu, Yu Zhen-Wen, Zhang Yong-Li. Yield formation of wheat with different ear types under water-saving supplementary irrigation conditions [J]. Acta Agronomica Sinica, 2026, 52(5): 1522-1535.
[12] Cai Hong-Wei, Yu Ai-Zhong, Jiang Ke-Qiang, Wang Peng-Fei, Wang Yu-Long, Huo Jian-Zhe, Pang Xiao-Neng, Yin Bo, Shang Yong-Pan. Key mechanisms underlying the enhancement of sweet maize yield through partial substitution of chemical fertilizers with organic manure in arid irrigation districts [J]. Acta Agronomica Sinica, 2026, 52(4): 1166-1180.
[13] Cui Xue-Mei, Liu Yan-Di, Liu Jing-Hui, Mi Jun-Zhen, Wu Jun-Ying, Zhao Bao-Ping. Study on the relationship between physiological characteristics of superior and inferior grains with yield in different oat genotypes [J]. Acta Agronomica Sinica, 2026, 52(4): 1220-1235.
[14] Xu Jian-Xia, Ding Yan-Qing, Cao Ning, Cheng Bin, Gao Xu, Li Wen-Zhen, Wang Ruo-Ruo, Wang Lei, Zhang Li-Yi. Phenotypic diversity analysis and comprehensive evaluation of 397 sorghum germplasm resources in Guizhou, China [J]. Acta Agronomica Sinica, 2026, 52(4): 1073-1087.
[15] Zhang Quan-Jun, Wu Dong-Li, Liu Cong, Zhu Yong-Chao, Yang Da-Sheng, Kong Xiang-Sheng. Spatiotemporal evolution of rapeseed phenological periods in the Middle and Lower Reaches of the Yangtze River from 1981 to 2024 [J]. Acta Agronomica Sinica, 2026, 52(4): 1140-1152.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!