全 文 ：植物生理学报 Plant Physiology Journal 2014, 50 (8): 1144~1150　　doi: 10.13592/j.cnki.ppj.2014.00981144
收稿 2014-03-27　　修定 2014-07-22
资助 国家“863”项目(2012AA309)、天津市教委科研计划项目
(20130606和20130620)、天津市科委应用基础与前沿技术
研究计划项目(14JCYBJC30600)。
* 共同第一作者。
** 通讯作者(E-mail: xiex@tjau.edu.cn; Tel: 022-23798697)。
低空气湿度下气孔运动的调控
郭瑶琳1,*, 王俊斌2,*, 丁博1, 李明1, 陈帅君1, 张卫国3, 黄国中1, 谢晓东1,**
1天津农学院农学与资源环境学院, 天津300384; 2天津农学院基础科学学院, 天津300384; 3内蒙古民族大学农学院, 内蒙古
通辽028000
摘要: 植物气孔应答气候环境因子的机制, 一直是植物抗逆生理研究领域的热点课题。空气湿度是主要的气候环境因子之
一, 人们很早就发现降低空气湿度能导致气孔开度变小, 但到目前为止, 对调控这一生物学过程的机制还知之甚少。本文
概述近年来在植物气孔应答低空气湿度信号的运动规律、水被动反馈假说、水主动反馈假说、水力调节与代谢调节的关
系等方面的进展, 并基于进化学的理论, 提出了水力调节和代谢调节的反向消长模式, 以期解释大量物种气孔对低空气湿
度的不同应答反应。
关键词: 气孔运动; 低空气湿度; 调控机制
Regulation of Stomatal Movement under Low Atmospheric Humidity
GUO Yao-Lin1,*, WANG Jun-Bin2,*, DING Bo1, LI Ming1, CHEN Shuai-Jun1, ZHANG Wei-Guo3, HUANG Guo-Zhong1, XIE
Xiao-Dong1,**
1College of Agronomy, Resources and Environmental Sciences, Tianjin Agricultural University, Tianjin 300384, China; 2College
of Basic Sciences, Tianjin Agricultural University, Tianjin 300384, China; 3College of Agriculture, National University of Inner
Mongolia, Tongliao, Inner Mongolia 028000, China
Abstract: Studies on mechanisms underlying the plant stomatal responses to climatic factors have been hot
topics in the field of plant stress physiology. In earlier studies, stomatal closure was observed in response to low
atmospheric humidity, one of key climatic factors, but regulatory mechanisms of this biological process remain
elusive. In this review, we summarize the research advances in stomatal movement patterns, hydro-passive and
hydro-active feedback theories and the interactions between hydraulic and metabolic regulations. Based on evo-
lutionary differences of stomatal responses to low humidity, we propose a reverse trend model of hydraulic and
metabolic regulations to delineate the patterns of stomatal movement for macro-scale species.
Key words: stomatal movement; low atmospheric humidity; regulatory mechanisms
植物气孔是由两个保卫细胞围绕成的孔隙。
环境因子变化时, 植物能通过调整气孔开度, 控制
CO2的摄取和水分的散失(Hetherington 2001), 来调
节植物适应环境的能力。就湿度气候因子而言,
Darwin (1898)在110多年前就发现, 降低空气湿度
会导致气孔的开度变小, 但随后的研究发现, 一些
物种的气孔导度(Gs)和蒸腾速率(E)都降低, 称为前
馈应答(feed forward)反应(Cowan 1977; Farquhar
1978; Maier-Maercker 1983; Xue 2000)。而另一些
物种的蒸腾速率增加, 气孔导度降低, 是一种反馈
应答(feed back)反应(Mott和Parkhurst 1991; Monte-
ith 1995; Streck 2002, 2003)。上述两种应答反应类
型表现不一, 因而低空气湿度条件下的气孔运动
不是简单的水力调节问题, 代谢调节也是非常重
要的调节方式(Zhang等1987; Dodd等1996; Hills等
2012)。当前, 以现有实验数据为基础, 已构建了不
同的数学模型来拟合气孔的运动变化趋势(Lange
等1971; Monteith 1995; Peak和Mott 2011; Hills等
2012), 但由于对气孔应答机制不明, 这些数学模型
具有一定的局限性。本文概述了低空气湿度处理
下气孔运动的规律, 以及气孔应答低空气湿度调
控理论的研究进展, 并从进化学的角度, 对气孔的
调控机制进行了分析。
1 气孔对低空气湿度信号应答的规律
在低空气湿度影响气孔运动的机理研究中,
常采用叶气蒸气压差(vapour pressure deficit, VPD)
郭瑶琳等: 低空气湿度下气孔运动的调控 1145
来衡量空气湿度的胁迫水平。叶气蒸气压差是指
空气中水蒸气与叶片中水蒸气的压力差(Meidner
1987)。对大量植物材料观察后发现, 当空气湿度
降低或叶气蒸气压差增加时, 气孔导度会有短时
的升高(wrong way), 而后降低, 最后达到稳定的低
于起始值的气孔导度(right way) (Sheriff 1979;
Meidner 1986; Grantz 1990; Yong等1997; Buckley
和Mott 2002; Franks和Farquhar 2007) (图1-A)。但
在应答低空气湿度的过程中, 不同物种蒸腾速率
的变化却有所不同, 据此可将气孔应答低空气湿
度的反应概况为3种类型: (1)叶气蒸气压差的值较
低时, 叶片处于高湿度的环境, 气孔导度较高, 此
时蒸腾速率会增加, 而气孔导度降低不明显(类型
3, 反馈应答反应); (2)当叶气蒸气压差在中值区间
时, 蒸腾速率增加, 气孔导度变小(类型1, 反馈应答
反应); (3)在叶气蒸气压差值超过一定阈值后, 蒸
腾速率会下降, 气孔导度变小(类型2, 前馈应答反
应) (图1-B) (Monteith 1995; Eamus和Shanahan
2002)。为了揭示上述气孔应答低空气湿度反应的
机制, 科学家们开展了广泛而深入的研究, 水力调
节和代谢调节在不同应答反应中的作用也得到解
析。
图1 气孔应答低空气湿度的运动规律
Fig.1 Stomatal responses to low atmospheric humidity
A: 气孔导度的动态变化, 箭头表示低空气湿度处理的时间点; B: 气孔导度与蒸腾速率的关系[参照Monteith (1995)文献修改], 1、2、3表
示不同的气孔应答类型; C: 不同进化水平物种的水力调节和代谢调节变化, M为假定的代谢调节效应值, H为假定的水力调节效应值。
2 水力调节
水分可在土壤-植物-大气构成的水力系统中
达到供需平衡, 气孔会对任何改变这一平衡状态
的环境因子进行应答。低空气湿度会改变水力平
衡, 引发蒸腾需求, 气孔降低开度有利于减少水分
散失, 保持水力平衡。但是低空气湿度信号诱导
气孔运动的机制目前还不明了。对大量物种的研
究表明, 随着叶气蒸气压差增加, 蒸腾速率不断升
高 , 叶片水势降低 , 导致气孔导度减小(Mott和
Parkhurst 1991; Monteith 1995; Streck 2003) (图1-B,
类型1和3), 是一种负反馈应答(Cowan 1965; Ra-
schke和Kuhl 1969)。为阐明反馈应答的机制, 提出
了水被动反馈(hydro-passive feedback)和水主动反
馈(hydro-active feedback)两种假说。水被动反馈
假说认为, 在低空气湿度条件下, 蒸腾作用导致保
卫细胞被动失水, 保卫细胞膨压降低, 气孔开度变
小(Nonami等1990; Mott和Parkhurst 1991; Franks等
1997)。但是由于表皮细胞比保卫细胞具有机械优
势(mechanical advantage) (DeMichele和Sharp
1973), 因而在表皮细胞和保卫细胞同时被动失水
时(图2), 表皮细胞失水更多而膨压降低更大, 拉动
保卫细胞, 依据水被动反馈假说, 气孔会维持在开
放的状态。而实际上气孔导度只是发生了短暂的
升高, 然后降低到小于初始值的稳定状态(图1-A)
(Cowan 1977; Grantz等1990; Oren等1999)。而水
主动反馈假说可以更好地解释气孔的运动趋势:
低空气湿度处理后, 气孔的蒸腾作用增加, 保卫细
胞和表皮细胞被动失水(图2), 由于表皮细胞的机
植物生理学报1146
械优势, 会出现短暂的气孔被动张开反应, 随后由
于保卫细胞主动进行代谢调节, 气孔导度又降低
直至达到稳定状态(图1-A) (Meidner 1986; Grantz
1990; Buckley和Mott 2002; Franks和Farquhar
2007)。
但是随之而来的问题是, 水主动反馈假说如
何解释植物的前馈应答反应。前馈应答反应, 即
蒸腾速率降低, 气孔导度减小, 该反应不需要叶片
水分状态发生改变(Cowan 1977; Farquhar 1978)
(图1-B, 类型2)。为了解释这一现象, 有些研究引
用了气孔周围蒸腾(peristomatal transpiration)的概
念, 指出气孔周围的保卫细胞和邻近细胞的角质
层水分散失(而不是气孔蒸腾)影响了气孔的开度
(图2), 也得到一些研究的证实(Lange等1971;
Schulze等1972; Maier-Maercher 1983; Dewar
2002)。但如果气孔周围蒸腾是其产生原因, 由于
表皮细胞的机械优势, 气孔会维持开放的状态, 而
不是关闭。而水主动反馈假说认为, 当蒸腾速率
接近于最大值, 水势值接近植物木质部空洞形成
(cavitation)的临界点时, 低空气湿度处理会导致前
馈应答反应发生, 此时蒸腾速率降低, 而叶片的水
分状态不会有明显的变化(near-homeostas is)
(Buckley等2003), 保卫细胞的主动代谢调节使得
气孔导度降低(Buckley 2005)。
阐明气孔应答低空气湿度的机制, 还需确定
低空气湿度信号感受器(sensor)的位置和信号传递
的方式。气孔蒸腾包括气孔下腔内叶肉细胞、表
皮细胞和保卫细胞的水分蒸发(图2), 其水分蒸发
量显著大于通过气孔外角质层的蒸发量(Boyer等
1997)。因而, 低空气湿度信号的感受器应位于叶
片内部, 而不是叶片气孔外面的角质层。采用电
子显微镜进行形态学观察, 结果表明, 紫鸭跖草
(Tradescant virginiana)表皮角质层覆盖在副卫细
胞、保卫细胞甚至大部分表皮细胞的内表面上,
而这种角质层由外部向气孔腔内部的扩展终止于
表皮细胞和叶肉细胞之间。因而在低空气湿度条
件下, 叶肉细胞的水分散失最多, 水势最低(Nona-
mi等1990)。叶肉细胞可能是低空气湿度信号的感
受位点, 然后通过表皮细胞水势的改变导致气孔
运动。另外, 低空气湿度导致表皮细胞膨压下降
(Frensch和Schulze 1988; Nonami等1990), 引起附近
气孔的应答反应(Mott等1997; Mott和Franks 2001),
图2 气孔应答低空气湿度的调控机制模式
Fig.2 The regulatory mechanism model underlying stomatal responses to low atmospheric humidity
黑色实心箭头表示水分移动的方向; 红色实心箭头表示CO2扩散的方向; 黑色虚线箭头表示代谢物可能的转运方向。
郭瑶琳等: 低空气湿度下气孔运动的调控 1147
但并不会导致叶片水势的明显改变。这表明表皮
细胞也可能是低空气湿度信号的感受器(Buckley
2005)。而且, 阻断某个气孔的蒸腾作用, 不会影响
这一气孔的应答反应, 表明气孔是对其周边诸多
表皮细胞所传递的信号进行应答。此外, 低空气
湿度信号不仅仅通过周边表皮细胞的水势来传递,
其他的信号传递机制也可能参与其中(Kaiser和
Legner 2007)。
3 代谢调节
如上所述, 水主动反馈假说能很好地解释低
空气湿度条件下气孔的应答反应(图1-A和B), 有关
该假说中的主动代谢调节方式的研究, 目前已取
得一些进展。研究发现, 一些参与ABA信号通路
的信号元件也参与气孔对低空气湿度信号的调控
(Xie等2006)。低空气湿度条件下, ABA可能通过
合成、运输或再分配等途径在保卫细胞和其质外
体累积(Trejo等1993; Zhang等2001; Zhang和Out-
law 2001; Wilkinson和Davies 2002; Kang等2010;
Kuromori和Shinozaki 2010)。保卫细胞的ABA受
体PYRABACTIN RESISTANCE1/REGULATORY
COMPONENTS OF ABA RECEPTORS (PYR1/
RCAR)在细胞质结合ABA, 形成ABA-PYR/
RCARs-PP2C (PROTEIN PHOSPHATASE 2C)复合
体(Park等2009; Ma等2009; Merilo等2013), 降低了
PP2C的磷酸酶活性 , 从而解除对OST1 (OPEN
STOMATA 1)蛋白激酶的抑制(Mustilli等2002; Xie
等2006; Yoshida等2006; Vlad等2009; Lee和Luan
2012)。此后, OST1蛋白激酶通过磷酸化作用激活
慢型阴离子通道SLAC1 (SLOW ANION CHAN-
NEL ASSOCIATED 1) (Vahisalu等2008, 2010; Gei-
ger等2009; Lee等2009), 导致氯离子和苹果酸根离
子等阴离子流出保卫细胞(Negi等2008; Vahisalu等
2010), 保卫细胞失水, 气孔开度变小。低空气湿度
条件下, 与ABA合成相关的ABA1、ABA2、ABA3
合成酶的活性提高 , 而与ABA降解相关的CY-
P707a1和CRP707a3酶的活性受到抑制(Xie等2006;
Okamoto等2009; Aliniaeifard和van Meeteren 2013;
Bauer等2013a; Merilo等2013)。通过对ost1和slac1
突变体转录组的分析, 鉴定出了蔗糖合成酶基因
SUS3, 其编码的蛋白参与蔗糖和苹果酸等渗透调
节物质的代谢, 揭示了糖代谢在气孔应答湿度中
的作用(Bauer等2013b)。研究表明, 与生物胁迫应
答相关的基因也参与了植物对湿度信号的应答,
例如, CPR22 (CONSTITUTIVE EXPRESSER OF
PATHOGENESIS-RELATED GENES 22)基因(Mosh-
er等2010)和抗性基因SLH1 (SENSITIVE TO LOW
HUMIDITY 1) (Noutoshi等2005)。此外, 植物体内
除ABA外, 还有许多小分子代谢物参与了气孔应
答逆境胁迫的过程(张岁岐等2001), 例如: 过氧化
氢、细胞分裂素、生长素、乙烯和赤霉素等(安国
勇等2000; 苗雨晨等2000; Tanaka等2006; Zhang等
2001; Bunce 1998; Tardieu和Simonneau 1998; Dodd
等1996; Bano等1993; Zhang等1987; Livne和Vaadia
1965)。这些代谢物及相关的信号元件也可能参与
气孔应答低空气湿度信号的过程。
采用数学模型可对气孔应答湿度的反应进行
解释和预测(Farquhar和Wong 1984; Eamus和Sha-
nahan 2002; West等2005; Peak和Mott 2011; 陈骎和
梁宗锁2013), 但是已有的模型主要是建立在水力
学数据基础上的 , 不能反映细胞中代谢物的变
化。为此, Li等(2006)选取40余个ABA信号通路的
元件, 构建了Boolean数学模型, 能准确预测这些元
件对气孔运动的影响, 但这个模型尚不具备实时
和动态的特征。Gradmann等(1993)使用钾离子和
氯离子离子通道、质子泵和氢离子-氯离子同向运
输通道(symport)的数据模拟了保卫细胞电压的实
时波动。在此基础上, Hills等(2012)增加了更多的
离子通道, 设置了反映离子通道对细胞内钙离子
浓度和pH值敏感度的参数, 建立了OnGuard模型。
该模型能准确预测氯化钾、氯化钙和pH处理后气
孔的开度、保卫细胞体积和膨压、细胞质膜和液
泡膜的电压等。此外, Chen等(2012)使用OnGuard
模型, 成功预测了日变化时保卫细胞中不同离子
的浓度变化。
4 结语
在低空气湿度或高的叶气蒸气压差下, 气孔
导度会短暂升高, 然后下降, 最后达到平稳状态,
且低于起始气孔导度(Grantz 1990; Monteith 1995;
Buckley 2005)。在这一过程中, 不同物种的蒸腾速
率变化不同, 有些会升高(反馈应答), 有些会降低
(前馈应答)。结合木质部阻力和空洞化理论, 水主
动反馈应答假说能够很好地解释不同的气孔应答
植物生理学报1148
反应(Buckley 2005)。但应注意的是, 水主动反馈
假说并非适用所有植物。研究表明, 被子植物的
保卫细胞受周围表皮细胞的机械优势影响, 而真
蕨类植物和石松类植物保卫细胞与其表皮细胞的
互作并不紧密(McAdam和Brodribb 2012; Brodribb
和McAdam 2011), 因而后者并不遵循水主动反馈
假说, 而是符合水被动反馈假说。从进化的角度
上讲, 裸子植物介于被子植物和蕨类植物之间, 其
在中等强度的水分胁迫下, 气孔运动表现为被动
的水力学过程(passive-hydraulic process); 仅在极端
干旱的情况下, 随着水分胁迫的加强, ABA浓度升
高, 并主动促进气孔的关闭(McAdam和Brodribb
2014)。综合这些分析, 可以对气孔应答湿度的机
制从进化的角度进行重新阐述: 气孔应答湿度信
号时存在被动的水力调节和主动的代谢调节, 对
进化水平较低的物种, 水力调节占主导(图1-C中的
H), 而进化水平较高的物种(例如被子植物), 水力
调节作用降低, 代谢调节作用升高(图1-C中的M),
水力调节和代谢调节存在进化上的反向消长关
系。
就目前研究进展来说, 要揭示气孔应答低空
气湿度的机制, 还须开展大量的研究, 包括: (1)确
定木质部空洞化导致的水阻作用及植物水力系统
不同部位的水阻作用; (2)鉴定低空气湿度信号的
原初感受部位, 明确信号传递给保卫细胞的机制;
(3)保卫细胞中除ABA外, 还有受ABA调控的钾离
子、氯离子和钙离子等渗透调节物质, 对这些离
子的作用机制有待解析; (4)按照水力调节和代谢
调节反向消长的假定, 把两种类型的数学模型进
行整合, 以获得针对不同物种的普适模型。
参考文献
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 (5): 458~464
陈骎, 梁宗锁(2013). 气孔导度对空气湿度的反应的数学概括及其
可能的机理. 植物生理学报, 49 (3): 241~246
苗雨晨, 宋纯鹏, 董发才, 王学臣(2000). ABA诱导蚕豆气孔保卫细
胞H2O2的产生. 植物生理学报, 26 (1): 53~58
张岁岐, 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 (6): 1263~1270
Aliniaeifard S, van Meeteren U (2013). Can prolonged exposure to
low VPD disturb the ABA signalling in stomatal guard cells? J
Exp Bot, 64 (12): 3551~3566
Bano A, Dorffling K, Bettin D, Hahn H (1993). Abscisic acid and
cytokinins as possible root-to-shoot signals in xylem sap of rice
plants in drying soil. Aust J Plant Physiol, 20: 109~115
Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid KA,
Sonnewald S, Sonnewald U, Kneitz S, Lachmann N et al (2013a).
The stomatal response to reduced relative humidity requires
guard cell autonomous ABA synthesis. Curr Biol, 23 (1): 53~57
Bauer H, Ache P, Wohlfart F, Al-Rasheid KA, Sonnewald S, Son-
newald U, Kneitz S, Hetherington AM, Hedrich R (2013b). How
do stomata sense reductions in atmospheric relative humidity?
Mol Plant, 6 (5): 1703~1706
Boyer JS, Wong SC, Farquhar GD (1997). CO2 and water vapor ex-
change across leaf cuticle (epidermis) at various water potentials.
Plant Physiol, 114: 185~191
Brodribb TJ, McAdam SA (2011). Passive origins of stomatal control
in vascular plants. Science, 331 (6017): 582~585
Buckley TN (2005). The control of stomata by water balance. New
Phytol, 168: 275~292
Buckley TN, Mott KA (2002). Stomatal water relations and the con-
trol of hydraulic supply and demand. Prog Bot, 63: 309~325
Buckley TN, Mott KA, Farquhar GD (2003). A hydromechanical and
biochemical model of stomatal conductance. Plant Cell Environ,
26: 1767~1785
Bunce JA (1998). Effects of humidity on short-term response of sto-
matal conductance to an increase in carbon dioxide concentra-
tion. Plant Cell Environ, 21: 115~120
Chen ZH, Hills A, Bätz U, Amtmann A, Lew VL, Blatt MR (2012).
Systems dynamic modeling of the stomatal guard cell predicts
emergent behaviors in transport, signaling, and volume control.
Plant Physiol, 159 (3): 1235~1251
Cowan IR (1965). Transport of water in the soil-plant-atmosphere
system. J Appl Ecol, 2 (3): 221~239
Cowan IR (1977). Stomatal behaviour and environment. Adv Bot Res,
4: 117~228
Darwin F (1898). Observations on stomata. Proc R Soc Lond, 63:
413~417
DeMichele DW, Sharpe PJH (1973). An analysis of the mechanics of
guard cell motion. J Theor Biol, 41: 77~96
Dewar RC (2002). The Ball-Berry-Leuning and Tardieu-Davies mod-
els: synthesis and extension at guard cell level. Plant Cell Envi-
ron, 25: 1383~1398
Dodd IC, Stikic R, Davies WJ (1996). Chemical regulation of gas
exchange and growth of plants in drying soil in the field. J Exp
Bot, 47: 1475~1490
Eamus D, Shanahan ST (2002). A rate equation model of stomatal re-
sponses to vapour pressure deficit and drought. BMC Ecol, 2: 8
Farquhar GD (1978). Feedforward responses to stomata to humidity.
Aust J Plant Physiol, 5: 787~800
Farquhar GD, Wong SC (1984). An empirical model of stomatal con-
ductance. Aust J Plant Physiol, 11 (3): 191~210
Franks PJ, Cowan IR, Farquhar GD (1997). The apparent feedforward
response of stomata to air vapour pressure deficit: information
revealed by different experimental procedures with two rainfor-
est trees. Plant Cell Environ, 20: 142~145
郭瑶琳等: 低空气湿度下气孔运动的调控 1149
Franks PJ, Farquhar GD (2007). The mechanical diversity of stomata
and its significance in gas exchange control. Plant Physiol, 143:
78~87
Frensch J, Schulze ED (1988). The effect of humidity and light on
cellular water relations and diffusion conductance of leaves of
Tradescantia virginiana L. Planta, 173 (4): 554~562
Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache
P, Matschi S, Liese A, Al-Rasheid KA et al (2009). Activity of
guard cell anion channel SLAC1 is controlled by drought-stress
signaling kinase-phosphatase pair. Proc Natl Acad Sci USA, 106:
21425~21430
Gradmann D, Blatt MR, Thiel G (1993). Electrocoupling of ion trans-
porters in plants. J Membr Biol, 136: 327~332
Grantz DA (1990). Plant response to atmospheric humidity. Plant Cell
Environ, 13: 667~679
Hetherington AM (2001). Guard cell signaling. Cell, 107: 711~714
Hills A, Chen ZH, Amtmann A, Blatt MR, Lew VL (2012). OnGuard,
a computational platform for quantitative kinetic modeling of
guard cell physiology. Plant Physiol, 159 (3): 1026~1042
Kaiser H, Legner N (2007). Localization of mechanisms involved in
hydropassive and hydroactive stomatal responses of Sambucus
nigra to dry air. Plant Physiol, 143 (2): 1068~1077
Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee
Y (2010). PDR-type ABC transporter mediates cellular uptake of
the phytohormone abscisic acid. Proc Natl Acad Sci USA, 107:
2355~2360
Kuromori T, Shinozaki K (2010). ABA transport factors found in Ara-
bidopsis ABC transporters. Plant Signal Behav, 5: 1124~1126
Lange OL, Lösch R, Schulze ED, Kappen L (1971). Responses of sto-
mata to changes in humidity. Planta, 100: 76~86
Lee SC, Lan W, Buchanan BB, Luan S (2009). A protein kinase-phos-
phatase pair interacts with an ion channel to regulate ABA
signaling in plant guard cells. Proc Natl Acad Sci USA, 106:
21419~21424
Lee SC, Luan S (2012). ABA signal transduction at the crossroad of
biotic and abiotic stress responses. Plant Cell Environ, 35: 53~60
Li S, Assmann SM, Albert R (2006). Predicting essential components
of signal transduction networks: a dynamic model of guard cell
abscisic acid signaling. PLoS Biol, 4 (10): e312
Livne A, Vaadia Y (1965). Stimulation of transpiration rate in bar-
ley leaves by kinetin and gibberellic acid. Physiol Plant, 18:
658~664
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill
E (2009). Regulators of PP2C phosphatase activity function as
abscisic acid sensors. Science, 324: 1064~1068
Maier-Maercker U (1983). The role of peristomatal transpiration in
the mechanism of stomatal movement. Plant Cell Environ, 6:
369~380
McAdam SA, Brodribb TJ (2012). Fern and lycophyte guard cells
do not respond to endogenous abscisic acid. Plant Cell, 24 (4):
1510~1521
McAdam SA, Brodribb TJ (2014). Separating active and passive in-
fluences on stomatal control of transpiration. Plant Physiol, 164:
1578~1586
Meidner H (1986). Cuticular conductance and the humidity response
of stomata. J Exp Bot, 37: 517~525
Meidner H (1987). Three hundred years of research into stomata. In:
Zeiger E, Farquhar GD, Cowan IR (eds). Stomatal Function.
Stanford: Stanford University Press, 7~27
Merilo E, Laanemets K, Hu H, Xue S, Jakobson L, Tulva I, Gonza-
lez-Guzman M, Rodriguez PL, Schroeder JI, Broschè M et al
(2013). PYR/RCAR receptors contribute to ozone-, reduced
air humidity-, darkness-, and CO2-induced stomatal regulation.
Plant Physiol, 162 (3): 1652~1668
Monteith JL (1995). A reinterpretation of stomatal responses to hu-
midity. Plant Cell Environ, 18: 357~364
Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH, Urquhart
W, Klessig DF, Kim SK, Nambara E, Yoshioka K (2010). The
lesion-mimic mutant cpr22 shows alterations in abscisic acid
signaling and abscisic acid insensitivity in a salicylic acid-depen-
dent manner. Plant Physiol, 152: 1901~1913
Mott KA, Denne F, Powell J (1997). Interactions among stomata in
response to perturbations in humidity. Plant Cell Environ, 20:
1098~1107
Mott KA, Franks PJ (2001). The role of epidermal turgor in stomatal
interactions following a perturbation in humidity. Plant Cell En-
viron, 24 (6): 657~662
Mott KA, Parkhurst DF (1991). Stomatal responses to humidity in air
and helox. Plant Cell Environ, 14: 509~515
Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002). Ara-
bidopsis OST1 protein kinase mediates the regulation of stomatal
aperture by abscisic acid and acts upstream of reactive oxygen
species production. Plant Cell, 14 (12): 3089~3099
Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada
M, Uchimiya H, Hashimoto M, Iba K (2008). CO2 regulator
SLAC1 and its homologues are essential for anion homeostasis
in plant cells. Nature, 452: 483~486
Nonami H, Schulze ED, Ziegler H (1990). Mechanisms of stomatal
movement in response to air humidity, irradiance and xylem wa-
ter potential. Planta, 183: 57~64
Noutoshi Y, Ito T, Seki M, Nakashita H, Yoshida S, Marco Y, Shira-
su K, Shinozaki K (2005). A single amino acid insertion in the
WRKY domain of the Arabidopsis TIR–NBS–LRR–WRKY-
type disease resistance protein SLH1 (sensitive to low humidity
1) causes activation of defense responses and hypersensitive cell
death. Plant J, 43: 873~888
Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E
(2009). High humidity induces abscisic acid 8′-hydroxylase in
stomata and vasculature to regulate local and systemic abscisic
acid responses in Arabidopsis. Plant Physiol, 149: 825~834
Oren R, Philips N, Ewers BE, Pataki DE, Megonigal JP (1999). Sap-
flux-scaled transpiration responses to light, vapor pressure
deficit, and leaf area reduction in a flooded Taxodium distichum
forest. Tree Physiol, 19 (6): 337~347
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba
S, Santiago J, Rodrigues A, Chow TF et al (2009). Abscisic acid
inhibits type 2C protein phosphatases via the PYR/PYL family
of START proteins. Science, 324: 1068~1071
植物生理学报1150
Peak D, Mott KA (2011). A new vapour-phase mechanism for stoma-
tal responses to humidity and temperature. Plant Cell Environ,
34: 162~178
Raschke K, Kuhl U (1969). Stomatal responses to changes in atmo-
spheric humidity and water supply: experiments with leaf sec-
tions of Zea mays in CO2-free air. Planta, 87: 36~48
Schulze ED, Lange OL, Buschbom U, Kappen L, Evenari M (1972).
Stomatal responses to changes in humidity in plants growing in
the desert. Planta, 108: 259~270
Sheriff DW (1979). Stomatal aperture and the sensing of the environ-
ment by guard cells. Plant Cell Environ, 2: 15~22
Streck NA (2002). Developmental and physiological responses of
winter wheat (Triticum aestivum L.) to selected environmental
factors [PhD thesis]. Nebraska, US: University of Nebraska-Lin-
coln
Streck NA (2003). Stomatal response to water vapor pressure deficit:
an unsolved issue. Rev Bras Agroc, 9: 317~322
Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S
(2006). Cytokinin and auxin inhibit abscisic acid-induced stoma-
tal closure by enhancing ethylene production in Arabidopsis. J
Exp Bot, 57: 2259~2266
Tardieu F, Simonneau T (1998). Variability among species of stoma-
tal control under fluctuating soil water status and evaporative
demand: modelling isohydric and anisohydric behaviours. J Exp
Bot, 49: 419~432
Trejo CL, Davies WJ, Ruiz L (1993). Sensitivity of stomata to abscis-
ic acid (an effect of the mesophyll). Plant Physiol, 102: 497~502
Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G,
Lamminmäki A, Brosché M, Moldau H, Desikan R et al (2008).
SLAC1 is required for plant guard cell S-type anion channel
function in stomatal signalling. Nature, 452 (7186): 487~491
Vahisalu T, Puzorjova I, Brosche M, Valk E, Lepiku M, Moldau
H, Pechter P, Wang YS, Lindgren O, Salojärvi J et al (2010).
Ozone-triggered rapid stomatal response involves the production
of reactive oxygen species, and is controlled by SLAC1 and
OST1. Plant J, 62: 442~453
Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N,
Leung J, Rodriguez PL, Laurière C, Merlot S (2009). Protein
phosphatases 2C regulate the activation of the Snf1-related
kinase OST1 by abscisic acid in Arabidopsis. Plant Cell, 21:
3170~3184
West JD, Peak D, Peterson JQ, Mott KA (2005). Dynamics of stoma-
tal patches for a single surface of Xanthium strumarium L. leaves
observed with fluorescence and thermal images. Plant Cell Envi-
ron, 28: 633~641
Wilkinson S, Davies WH (2002). ABA-based chemical signalling: the
co-ordination of responses to stress in plants. Plant Cell Environ,
25: 195~210
Xie X, Wang Y, Williamson L, Holroyd GH, Tagliavia C, Murchie E,
Theobald J, Knight MR, Davies WJ, Leyser HM et al (2006).
The identification of genes involved in the stomatal response to
reduced atmospheric relative humidity. Curr Biol, 16: 882~887
Xue Q (2000). Phenology and gas exchange in winter wheat (Triticum
aestivum L.) [PhD thesis]. Nebraska, US: University of Nebras-
ka-Lincoln
Yong JWH, Wong SC, Farquhar GD (1997). Stomatal responses to
changes in vapour pressure difference between leaf and air. Plant
Cell Environ, 20: 1213~1216
Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F,
Shinozaki K (2006). The regulatory domain of SRK2E/OST1/
SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA)
and osmotic stress signals controlling stomatal closure in Arabi-
dopsis. J Biol Chem, 281: 5310~5318
Zhang J, Schurr U, Davies WJ (1987). Control of stomatal behaviour
by abscisic acid which apparently orginates in the roots. J Exp
Bot, 38 (7): 1174~1181
Zhang SQ, Outlaw WH Jr (2001). Abscisic acid introduced into the
transpiration stream accumulates in the guard cell apoplast and
causes stomatal closure. Plant Cell Environ, 24: 1045~1054
Zhang SQ, Outlaw WH Jr, Aghoram K (2001). Relationship be-
tween changes in the guard cell abscisic-acid content and other
stress-related physiological parameters in intact plants. J Exp
Bot, 52: 301~308
Zhang X, Zhang L, Dong F, Gao J, Song CP (2001). Hydrogen perox-
ide involves abscisic acid-induced stomatal movement in Vicia
faba L. Plant Physiol, 126: 1438~1448