A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and Hydrogen Peroxide Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

被引:76
作者
Li, Jian-Hua [1 ]
Liu, Yin-Qian [1 ]
Lue, Pin [2 ]
Lin, Hai-Fei [1 ]
Bai, Yang [1 ]
Wang, Xue-Chen [3 ]
Chen, Yu-Ling [1 ]
机构
[1] Hebei Normal Univ, Coll Life Sci, Hebei Key Lab Mol & Cellular Biol, Shijiazhuang 050016, Peoples R China
[2] Hebei Med Univ, Sch Basic Med Sci, Shijiazhuang 050017, Peoples R China
[3] China Agr Univ, Coll Biol Sci, Natl Lab Plant Physiol & Biochem, Beijing 100094, Peoples R China
基金
美国国家科学基金会;
关键词
SUSPENSION-CULTURED CELLS; ABSCISIC-ACID; ALPHA-SUBUNIT; HYPOCOTYL ELONGATION; POLLEN GERMINATION; CA2+; SYNTHASE; CALCIUM; ABA; CHANNELS;
D O I
10.1104/pp.109.137067
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Extracellular calmodulin (ExtCaM) regulates stomatal movement by eliciting a cascade of intracellular signaling events including heterotrimeric G protein, hydrogen peroxide (H2O2), and Ca2+. However, the ExtCaM-mediated guard cell signaling pathway remains poorly understood. In this report, we show that Arabidopsis (Arabidopsis thaliana) NITRIC OXIDE ASSOCIATED1 (AtNOA1)-dependent nitric oxide (NO) accumulation plays a crucial role in ExtCaM-induced stomatal closure. ExtCaM triggered a significant increase in NO levels associated with stomatal closure in the wild type, but both effects were abolished in the Atnoa1 mutant. Furthermore, we found that ExtCaM-mediated NO generation is regulated by GPA1, the G alpha-subunit of heterotrimeric G protein. The ExtCaM-dependent NO accumulation was nullified in gpa1 knockout mutants but enhanced by overexpression of a constitutively active form of GPA1 (cG alpha). In addition, cG alpha Atnoa1 and gpa1-2 Atnoa1 double mutants exhibited a similar response as did Atnoa1. The defect in gpa1 was rescued by overexpression of AtNOA1. Finally, we demonstrated that G protein activation of NO production depends on H2O2. Reduced H2O2 levels in guard cells blocked the stomatal response of cG alpha lines, whereas exogenously applied H2O2 rescued the defect in ExtCaM-mediated stomatal closure in gpa1 mutants. Moreover, the atrbohD/F mutant, which lacks the NADPH oxidase activity in guard cells, had impaired NO generation in response to ExtCaM, and H2O2-induced stomatal closure and NO accumulation were greatly impaired in Atnoa1. These findings have established a signaling pathway leading to ExtCaM-induced stomatal closure, which involves GPA1-dependent activation of H2O2 production and subsequent AtNOA1-dependent NO accumulation.
引用
收藏
页码:114 / 124
页数:11
相关论文
共 61 条
[1]   A defined range of guard cell calcium oscillation parameters encodes stomatal movements [J].
Allen, GJ ;
Chu, SP ;
Harrington, CL ;
Schumacher, K ;
Hoffman, T ;
Tang, YY ;
Grill, E ;
Schroeder, JI .
NATURE, 2001, 411 (6841) :1053-1057
[2]   Novel mechanisms of G protein-dependent regulation of endothelial nitric- oxide synthase [J].
Andreeva, AV ;
Vaiskunaite, R ;
Kutuzov, MA ;
Profirovic, J ;
Skidgel, RA ;
Yasenetskaya, TV .
MOLECULAR PHARMACOLOGY, 2006, 69 (03) :975-982
[3]   Localization of nitric-oxide synthase in plant peroxisomes [J].
Barroso, JB ;
Corpas, FJ ;
Carreras, A ;
Sandalio, LM ;
Valderrama, R ;
Palma, JM ;
Lupiáñez, JA ;
del Río, LA .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1999, 274 (51) :36729-36733
[4]   Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants [J].
Beligni, MV ;
Lamattina, L .
PLANTA, 2000, 210 (02) :215-221
[5]   CHARACTERIZATION OF OAT CALMODULIN AND RADIOIMMUNOASSAY OF ITS SUBCELLULAR-DISTRIBUTION [J].
BIRO, RL ;
DAYE, S ;
SERLIN, BS ;
TERRY, ME ;
DATTA, N ;
SOPORY, SK ;
ROUX, SJ .
PLANT PHYSIOLOGY, 1984, 75 (02) :382-386
[6]   ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis [J].
Bright, J ;
Desikan, R ;
Hancock, JT ;
Weir, IS ;
Neill, SJ .
PLANT JOURNAL, 2006, 45 (01) :113-122
[7]   Extracellular calmodulin-induced stomatal closure is mediated by heterotrimeric G protein and H2O2 [J].
Chen, YL ;
Huang, RF ;
Xiao, YM ;
Lü, P ;
Chen, J ;
Wang, XC .
PLANT PHYSIOLOGY, 2004, 136 (04) :4096-4103
[8]  
Chen YL, 2003, ACTA BOT SIN, V45, P40
[9]   The ascorbic acid redox state controls guard cell signaling and stomatal movement [J].
Chen, Z ;
Gallie, DR .
PLANT CELL, 2004, 16 (05) :1143-1162
[10]   Floral dip:: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana [J].
Clough, SJ ;
Bent, AF .
PLANT JOURNAL, 1998, 16 (06) :735-743