Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 312 (5771): 264-266

Copyright © 2006 by the American Association for the Advancement of Science

A Bifurcating Pathway Directs Abscisic Acid Effects on Stomatal Closure and Opening in Arabidopsis

Girish Mishra,* Wenhua Zhang,* Fan Deng, Jian Zhao, Xuemin Wang{dagger}

Abstract: Terrestrial plants lose water primarily through stomata, pores on the leaves. The hormone abscisic acid (ABA) decreases water loss by regulating opening and closing of stomata. Here, we show that phospholipase D{alpha}1 (PLD{alpha}1) mediates the ABA effects on stomata through interaction with a protein phosphatase 2C (PP2C) and a heterotrimeric GTP-binding protein (G protein) in Arabidopsis. PLD{alpha}1-produced phosphatidic acid (PA) binds to the ABI1 PP2C to signal ABA-promoted stomatal closure, whereas PLD{alpha}1 and PA interact with the G{alpha} subunit of heterotrimeric G protein to mediate ABA inhibition of stomatal opening. The results reveal a bifurcating signaling pathway that regulates plant water loss.

Department of Biology, University of Missouri, St. Louis, MO 63121, USA, and Donald Danforth Plant Science Center, St. Louis, MO 63132, USA.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: wangxue{at}

The Solanum lycopersicum Zinc Finger2 Cysteine-2/Histidine-2 Repressor-Like Transcription Factor Regulates Development and Tolerance to Salinity in Tomato and Arabidopsis.
I. Hichri, Y. Muhovski, E. Žižkova, P. I. Dobrev, J. M. Franco-Zorrilla, R. Solano, I. Lopez-Vidriero, V. Motyka, and S. Lutts (2014)
Plant Physiology 164, 1967-1990
   Abstract »    Full Text »    PDF »
Abscisic acid signalling determines susceptibility of bundle sheath cells to photoinhibition in high light-exposed Arabidopsis leaves.
M. Gorecka, R. Alvarez-Fernandez, K. Slattery, L. McAusland, P. A. Davey, S. Karpinski, T. Lawson, and P. M. Mullineaux (2014)
Phil Trans R Soc B 369, 20130234
   Abstract »    Full Text »    PDF »
Phosphatidic Acid Interacts with a MYB Transcription Factor and Regulates Its Nuclear Localization and Function in Arabidopsis.
H. Yao, G. Wang, L. Guo, and X. Wang (2013)
PLANT CELL 25, 5030-5042
   Abstract »    Full Text »    PDF »
Difference in Abscisic Acid Perception Mechanisms between Closure Induction and Opening Inhibition of Stomata.
Y. Yin, Y. Adachi, W. Ye, M. Hayashi, Y. Nakamura, T. Kinoshita, I. C. Mori, and Y. Murata (2013)
Plant Physiology 163, 600-610
   Abstract »    Full Text »    PDF »
Can prolonged exposure to low VPD disturb the ABA signalling in stomatal guard cells?.
S. Aliniaeifard and U. van Meeteren (2013)
J. Exp. Bot. 64, 3551-3566
   Abstract »    Full Text »    PDF »
Heterotrimeric G protein signalling in the plant kingdom.
D. Urano, J.-G. Chen, J. R. Botella, and A. M. Jones (2013)
Open Bio 3, 120186
   Abstract »    Full Text »    PDF »
Role and Interrelationship of G{alpha} Protein, Hydrogen Peroxide, and Nitric Oxide in Ultraviolet B-Induced Stomatal Closure in Arabidopsis Leaves.
J.-M. He, X.-G. Ma, Y. Zhang, T.-F. Sun, F.-F. Xu, Y.-P. Chen, X. Liu, and M. Yue (2013)
Plant Physiology 161, 1570-1583
   Abstract »    Full Text »    PDF »
Physiological and molecular responses to drought in Petunia: the importance of stress severity.
J. Kim, A. Malladi, and M. W. van Iersel (2012)
J. Exp. Bot. 63, 6335-6345
   Abstract »    Full Text »    PDF »
Dissecting Arabidopsis G{beta} Signal Transduction on the Protein Surface.
K. Jiang, A. Frick-Cheng, Y. Trusov, M. Delgado-Cerezo, D. M. Rosenthal, J. Lorek, R. Panstruga, F. L. Booker, J. R. Botella, A. Molina, et al. (2012)
Plant Physiology 159, 975-983
   Abstract »    Full Text »    PDF »
Cooperative Function of PLD{delta} and PLD{alpha}1 in Abscisic Acid-Induced Stomatal Closure in Arabidopsis.
M. Uraji, T. Katagiri, E. Okuma, W. Ye, M. A. Hossain, C. Masuda, A. Miura, Y. Nakamura, I. C. Mori, K. Shinozaki, et al. (2012)
Plant Physiology 159, 450-460
   Abstract »    Full Text »    PDF »
Connections between Sphingosine Kinase and Phospholipase D in the Abscisic Acid Signaling Pathway in Arabidopsis.
L. Guo, G. Mishra, J. E. Markham, M. Li, A. Tawfall, R. Welti, and X. Wang (2012)
J. Biol. Chem. 287, 8286-8296
   Abstract »    Full Text »    PDF »
The phosphatidylcholine-hydrolysing phospholipase C NPC4 plays a role in response of Arabidopsis roots to salt stress.
D. Kocourkova, Z. Krckova, P. Pejchar, S. Veselkova, O. Valentova, R. Wimalasekera, G. F. E. Scherer, and J. Martinec (2011)
J. Exp. Bot. 62, 3753-3763
   Abstract »    Full Text »    PDF »
AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction?.
G. F. E. Scherer (2011)
J. Exp. Bot. 62, 3339-3357
   Abstract »    Full Text »    PDF »
Phosphatidic Acid Binds and Stimulates Arabidopsis Sphingosine Kinases.
L. Guo, G. Mishra, K. Taylor, and X. Wang (2011)
J. Biol. Chem. 286, 13336-13345
   Abstract »    Full Text »    PDF »
Molecular, cellular, and physiological responses to phosphatidic acid formation in plants.
C. Testerink and T. Munnik (2011)
J. Exp. Bot. 62, 2349-2361
   Abstract »    Full Text »    PDF »
Heterotrimeric G-protein regulation of ROS signalling and calcium currents in Arabidopsis guard cells.
W. Zhang, B. W. Jeon, and S. M. Assmann (2011)
J. Exp. Bot. 62, 2371-2379
   Abstract »    Full Text »    PDF »
Genome-scale transcriptome analysis of the desert poplar, Populus euphratica.
Q. Qiu, T. Ma, Q. Hu, B. Liu, Y. Wu, H. Zhou, Q. Wang, J. Wang, and J. Liu (2011)
Tree Physiol 31, 452-461
   Abstract »    Full Text »    PDF »
Molecular and Physiological Analysis of Drought Stress in Arabidopsis Reveals Early Responses Leading to Acclimation in Plant Growth.
A. Harb, A. Krishnan, M. M. R. Ambavaram, and A. Pereira (2010)
Plant Physiology 154, 1254-1271
   Abstract »    Full Text »    PDF »
Nicotinate/nicotinamide mononucleotide adenyltransferase-mediated regulation of NAD biosynthesis protects guard cells from reactive oxygen species in ABA-mediated stomatal movement in Arabidopsis.
S.-n. Hashida, T. Itami, H. Takahashi, K. Takahara, M. Nagano, M. Kawai-Yamada, K. Shoji, F. Goto, T. Yoshihara, and H. Uchimiya (2010)
J. Exp. Bot. 61, 3813-3825
   Abstract »    Full Text »    PDF »
Perturbation of Indole-3-Butyric Acid Homeostasis by the UDP-Glucosyltransferase UGT74E2 Modulates Arabidopsis Architecture and Water Stress Tolerance.
V. B. Tognetti, O. Van Aken, K. Morreel, K. Vandenbroucke, B. van de Cotte, I. De Clercq, S. Chiwocha, R. Fenske, E. Prinsen, W. Boerjan, et al. (2010)
PLANT CELL 22, 2660-2679
   Abstract »    Full Text »    PDF »
Nonspecific Phospholipase C NPC4 Promotes Responses to Abscisic Acid and Tolerance to Hyperosmotic Stress in Arabidopsis.
C. Peters, M. Li, R. Narasimhan, M. Roth, R. Welti, and X. Wang (2010)
PLANT CELL 22, 2642-2659
   Abstract »    Full Text »    PDF »
Phosphatidic Acid Inhibits Blue Light-Induced Stomatal Opening via Inhibition of Protein Phosphatase 1.
A. Takemiya and K.-i. Shimazaki (2010)
Plant Physiology 153, 1555-1562
   Abstract »    Full Text »    PDF »
Two Coupled Components of the Mitogen-Activated Protein Kinase Cascade MdMPK1 and MdMKK1 from Apple Function in ABA Signal Transduction.
X. J. Wang, S. Y. Zhu, Y. F. Lu, R. Zhao, Q. Xin, X. F. Wang, and D. P. Zhang (2010)
Plant Cell Physiol. 51, 754-766
   Abstract »    Full Text »    PDF »
Silymarin secretion and its elicitation by methyl jasmonate in cell cultures of Silybum marianum is mediated by phospholipase D-phosphatidic acid.
E. Madrid and P. Corchete (2010)
J. Exp. Bot. 61, 747-754
   Abstract »    Full Text »    PDF »
Function and Expression Pattern of the {alpha} Subunit of the Heterotrimeric G Protein in Rice.
Y. Izawa, Y. Takayanagi, N. Inaba, Y. Abe, M. Minami, Y. Fujisawa, H. Kato, S. Ohki, H. Kitano, and Y. Iwasaki (2010)
Plant Cell Physiol. 51, 271-281
   Abstract »    Full Text »    PDF »
At4g24160, a Soluble Acyl-Coenzyme A-Dependent Lysophosphatidic Acid Acyltransferase.
A. K. Ghosh, N. Chauhan, S. Rajakumari, G. Daum, and R. Rajasekharan (2009)
Plant Physiology 151, 869-881
   Abstract »    Full Text »    PDF »
Phospholipase D{alpha}1 and Phosphatidic Acid Regulate NADPH Oxidase Activity and Production of Reactive Oxygen Species in ABA-Mediated Stomatal Closure in Arabidopsis.
Y. Zhang, H. Zhu, Q. Zhang, M. Li, M. Yan, R. Wang, L. Wang, R. Welti, W. Zhang, and X. Wang (2009)
PLANT CELL 21, 2357-2377
   Abstract »    Full Text »    PDF »
Functional Differentiation of Brassica napus Guard Cells and Mesophyll Cells Revealed by Comparative Proteomics.
M. Zhu, S. Dai, S. McClung, X. Yan, and S. Chen (2009)
Mol. Cell. Proteomics 8, 752-766
   Abstract »    Full Text »    PDF »
The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling.
S. Zhang, Z. Cai, and X. Wang (2009)
PNAS 106, 4543-4548
   Abstract »    Full Text »    PDF »
Disentangling the Complexity of Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling.
A. Pitzschke and H. Hirt (2009)
Plant Physiology 149, 606-615
   Full Text »    PDF »
Multiple PLDs Required for High Salinity and Water Deficit Tolerance in Plants.
B. O. R. Bargmann, A. M. Laxalt, B. t. Riet, B. van Schooten, E. Merquiol, C. Testerink, M. A. Haring, D. Bartels, and T. Munnik (2009)
Plant Cell Physiol. 50, 78-89
   Abstract »    Full Text »    PDF »
Functional Proteomics of Arabidopsis thaliana Guard Cells Uncovers New Stomatal Signaling Pathways.
Z. Zhao, W. Zhang, B. A. Stanley, and S. M. Assmann (2008)
PLANT CELL 20, 3210-3226
   Abstract »    Full Text »    PDF »
F-Box Protein DOR Functions As a Novel Inhibitory Factor for Abscisic Acid-Induced Stomatal Closure under Drought Stress in Arabidopsis.
Y. Zhang, W. Xu, Z. Li, X. W. Deng, W. Wu, and Y. Xue (2008)
Plant Physiology 148, 2121-2133
   Abstract »    Full Text »    PDF »
Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor.
A. Khandelwal, T. Elvitigala, B. Ghosh, and R. S. Quatrano (2008)
Plant Physiology 148, 2050-2058
   Abstract »    Full Text »    PDF »
CsPLD{alpha}1 and CsPLD{gamma}1 are differentially induced during leaf and fruit abscission and diurnally regulated in Citrus sinensis.
A. Malladi and J. K. Burns (2008)
J. Exp. Bot. 59, 3729-3739
   Abstract »    Full Text »    PDF »
Anion Channel Activation and Proton Pumping Inhibition Involved in the Plasma Membrane Depolarization Induced by ABA in Arabidopsis thaliana Suspension Cells are Both ROS Dependent.
J. Trouverie, G. Vidal, Z. Zhang, C. Sirichandra, K. Madiona, Z. Amiar, J.-L. Prioul, E. Jeannette, J.-P. Rona, and M. Brault (2008)
Plant Cell Physiol. 49, 1495-1507
   Abstract »    Full Text »    PDF »
Transgenic Arabidopsis Plants Expressing the Type 1 Inositol 5-Phosphatase Exhibit Increased Drought Tolerance and Altered Abscisic Acid Signaling.
I. Y. Perera, C.-Y. Hung, C. D. Moore, J. Stevenson-Paulik, and W. F. Boss (2008)
PLANT CELL 20, 2876-2893
   Abstract »    Full Text »    PDF »
Comparative Transcriptomics of Arabidopsis Sperm Cells.
F. Borges, G. Gomes, R. Gardner, N. Moreno, S. McCormick, J. A. Feijo, and J. D. Becker (2008)
Plant Physiology 148, 1168-1181
   Abstract »    Full Text »    PDF »
Abscisic acid regulation of guard-cell K+ and anion channels in G{beta}- and RGS-deficient Arabidopsis lines.
L.-M. Fan, W. Zhang, J.-G. Chen, J. P. Taylor, A. M. Jones, and S. M. Assmann (2008)
PNAS 105, 8476-8481
   Abstract »    Full Text »    PDF »
G{gamma}1 + G{gamma}2 != G{beta}: Heterotrimeric G Protein G{gamma}-Deficient Mutants Do Not Recapitulate All Phenotypes of G{beta}-Deficient Mutants.
Y. Trusov, W. Zhang, S. M. Assmann, and J. R. Botella (2008)
Plant Physiology 147, 636-649
   Abstract »    Full Text »    PDF »
An Update on Abscisic Acid Signaling in Plants and More ....
A. Wasilewska, F. Vlad, C. Sirichandra, Y. Redko, F. Jammes, C. Valon, N. F. d. Frey, and J. Leung (2008)
Mol Plant 1, 198-217
   Abstract »    Full Text »    PDF »
Dual Functions of Phospholipase D{alpha}1 in Plant Response to Drought.
Y. Hong, S. Zheng, and X. Wang (2008)
Mol Plant 1, 262-269
   Abstract »    Full Text »    PDF »
Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba.
Z. An, W. Jing, Y. Liu, and W. Zhang (2008)
J. Exp. Bot. 59, 815-825
   Abstract »    Full Text »    PDF »
Phospholipase D{alpha}3 Is Involved in the Hyperosmotic Response in Arabidopsis.
Y. Hong, X. Pan, R. Welti, and X. Wang (2008)
PLANT CELL 20, 803-816
   Abstract »    Full Text »    PDF »
Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1.
C. Testerink, P. B. Larsen, D. van der Does, J. A. J. van Himbergen, and T. Munnik (2007)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling.
C. A. Johnston, J. P. Taylor, Y. Gao, A. J. Kimple, J. C. Grigston, J.-G. Chen, D. P. Siderovski, A. M. Jones, and F. S. Willard (2007)
PNAS 104, 17317-17322
   Abstract »    Full Text »    PDF »
N-Acylethanolamine Metabolism Interacts with Abscisic Acid Signaling in Arabidopsis thaliana Seedlings.
N. D. Teaster, C. M. Motes, Y. Tang, W. C. Wiant, M. Q. Cotter, Y.-S. Wang, A. Kilaru, B. J. Venables, K. H. Hasenstein, G. Gonzalez, et al. (2007)
PLANT CELL 19, 2454-2469
   Abstract »    Full Text »    PDF »
Nitric Oxide Is Critical for Inducing Phosphatidic Acid Accumulation in Xylanase-elicited Tomato Cells.
A. M. Laxalt, N. Raho, A. t. Have, and L. Lamattina (2007)
J. Biol. Chem. 282, 21160-21168
   Abstract »    Full Text »    PDF »
SDIR1 Is a RING Finger E3 Ligase That Positively Regulates Stress-Responsive Abscisic Acid Signaling in Arabidopsis.
Y. Zhang, C. Yang, Y. Li, N. Zheng, H. Chen, Q. Zhao, T. Gao, H. Guo, and Q. Xie (2007)
PLANT CELL 19, 1912-1929
   Abstract »    Full Text »    PDF »
The GCR1, GPA1, PRN1, NF-Y Signal Chain Mediates Both Blue Light and Abscisic Acid Responses in Arabidopsis.
K. M. Warpeha, S. Upadhyay, J. Yeh, J. Adamiak, S. I. Hawkins, Y. R. Lapik, M. B. Anderson, and L. S. Kaufman (2007)
Plant Physiology 143, 1590-1600
   Abstract »    Full Text »    PDF »
BOTANY: A Plant Receptor with a Big Family.
E. Grill and A. Christmann (2007)
Science 315, 1676-1677
   Abstract »    Full Text »    PDF »
Heterotrimeric G protein signaling in the Arabidopsis unfolded protein response.
S. Wang, S. Narendra, and N. Fedoroff (2007)
PNAS 104, 3817-3822
   Abstract »    Full Text »    PDF »
Dual Lipid Modification of Arabidopsis G{gamma}-Subunits Is Required for Efficient Plasma Membrane Targeting.
Q. Zeng, X. Wang, and M. P. Running (2007)
Plant Physiology 143, 1119-1131
   Abstract »    Full Text »    PDF »
Abscisic Acid Antagonizes Ethylene-Induced Hyponastic Growth in Arabidopsis.
J. J. Benschop, F. F. Millenaar, M. E. Smeets, M. van Zanten, L. A.C.J. Voesenek, and A. J.M. Peeters (2007)
Plant Physiology 143, 1013-1023
   Abstract »    Full Text »    PDF »
Early PLD{alpha}-mediated events in response to progressive drought stress in Arabidopsis: a transcriptome analysis.
S. P. Mane, C. Vasquez-Robinet, A. A. Sioson, L. S. Heath, and R. Grene (2007)
J. Exp. Bot. 58, 241-252
   Abstract »    Full Text »    PDF »
The Control of Transpiration. Insights from Arabidopsis.
S. E. Nilson and S. M. Assmann (2007)
Plant Physiology 143, 19-27
   Full Text »    PDF »
The Arabidopsis Tetratricopeptide Repeat-Containing Protein TTL1 Is Required for Osmotic Stress Responses and Abscisic Acid Sensitivity.
A. Rosado, A. L. Schapire, R. A. Bressan, A. L. Harfouche, P. M. Hasegawa, V. Valpuesta, and M. A. Botella (2006)
Plant Physiology 142, 1113-1126
   Abstract »    Full Text »    PDF »
An Arabidopsis Glutathione Peroxidase Functions as Both a Redox Transducer and a Scavenger in Abscisic Acid and Drought Stress Responses.
Y. Miao, D. Lv, P. Wang, X.-C. Wang, J. Chen, C. Miao, and C.-P. Song (2006)
PLANT CELL 18, 2749-2766
   Abstract »    Full Text »    PDF »
Quantitative Profiling of Arabidopsis Polar Glycerolipids in Response to Phosphorus Starvation. Roles of Phospholipases D{zeta}1 and D{zeta}2 in Phosphatidylcholine Hydrolysis and Digalactosyldiacylglycerol Accumulation in Phosphorus-Starved Plants.
M. Li, R. Welti, and X. Wang (2006)
Plant Physiology 142, 750-761
   Abstract »    Full Text »    PDF »
A Golgi-localized Hexose Transporter Is Involved in Heterotrimeric G Protein-mediated Early Development in Arabidopsis.
H. X. Wang, R. R. Weerasinghe, T. D. Perdue, N. G. Cakmakci, J. P. Taylor, W. F. Marzluff, and A. M. Jones (2006)
Mol. Biol. Cell 17, 4257-4269
   Abstract »    Full Text »    PDF »
Enhancement of Abscisic Acid Sensitivity and Reduction of Water Consumption in Arabidopsis by Combined Inactivation of the Protein Phosphatases Type 2C ABI1 and HAB1.
A. Saez, N. Robert, M. H. Maktabi, J. I. Schroeder, R. Serrano, and P. L. Rodriguez (2006)
Plant Physiology 141, 1389-1399
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882