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.


Science 29 September 2000:
Vol. 289. no. 5488, pp. 2338 - 2342
DOI: 10.1126/science.289.5488.2338

Reports

Alteration of Stimulus-Specific Guard Cell Calcium Oscillations and Stomatal Closing in Arabidopsis det3 Mutant

Gethyn J. Allen,1* Sarah P. Chu,1dagger Karin Schumacher,2dagger ddagger Chad T. Shimazaki,1 Dionne Vafeados,2 Andrea Kemper,3 Scott D. Hawke,3 Gary Tallman,3 Roger Y. Tsien,4 Jeffrey F. Harper,5 Joanne Chory,2 Julian I. Schroeder1*

Cytosolic calcium oscillations control signaling in animal cells, whereas in plants their importance remains largely unknown. In wild-type Arabidopsis guard cells abscisic acid, oxidative stress, cold, and external calcium elicited cytosolic calcium oscillations of differing amplitudes and frequencies and induced stomatal closure. In guard cells of the V-ATPase mutant det3, external calcium and oxidative stress elicited prolonged calcium increases, which did not oscillate, and stomatal closure was abolished. Conversely, cold and abscisic acid elicited calcium oscillations in det3, and stomatal closure occurred normally. Moreover, in det3 guard cells, experimentally imposing external calcium-induced oscillations rescued stomatal closure. These data provide genetic evidence that stimulus-specific calcium oscillations are necessary for stomatal closure.

1 Cell and Developmental Biology Section, Division of Biology and Center for Molecular Genetics, University of California, San Diego, La Jolla, CA 92093-0116, USA.
2 Howard Hughes Medical Institute and Plant Biology Laboratory, Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037-1099, USA.
3 Department of Biology, Willamette University, 900 State Street, Salem, OR 97301-3931, USA.
4 Department of Pharmacology and Chemistry and Biochemistry, Howard Hughes Medical Institute and Division of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093-0647, USA.
5 Department of Cell Biology, Scripps Research Institute, BCC283, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
*   To whom correspondence should be addressed. E-mail: gallen{at}biomail.ucsd.edu, julian{at}biomail.ucsd.edu

dagger    These authors contributed equally to this work.

ddagger    Present address: ZMBP-Pflanzenphysiologie, Universitaet Tuebingen, Auf der Morgenstelle 1, 72076 Tuebingen, Germany.


Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Fine-Tuning of the Cytoplasmic Ca2+ Concentration Is Essential for Pollen Tube Growth.
M. Iwano, T. Entani, H. Shiba, M. Kakita, T. Nagai, H. Mizuno, A. Miyawaki, T. Shoji, K. Kubo, A. Isogai, et al. (2009)
Plant Physiology 150, 1322-1334
   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 »
Measurement of Changes in Cytosolic Ca2+ in Arabidopsis Guard Cells and Mesophyll Cells in Response to Blue Light.
A. Harada and K.-i. Shimazaki (2009)
Plant Cell Physiol. 50, 360-373
   Abstract »    Full Text »    PDF »
A Proteomics Study of Brassinosteroid Response in Arabidopsis.
Z. Deng, X. Zhang, W. Tang, J. A. Oses-Prieto, N. Suzuki, J. M. Gendron, H. Chen, S. Guan, R. J. Chalkley, T. K. Peterman, et al. (2007)
Mol. Cell. Proteomics 6, 2058-2071
   Abstract »    Full Text »    PDF »
The V-ATPase from etiolated barley (Hordeum vulgare L.) shoots is activated by blue light and interacts with 14-3-3 proteins.
O. Klychnikov, K. Li, H Lill, and A. de Boer (2007)
J. Exp. Bot. 58, 1013-1023
   Abstract »    Full Text »    PDF »
The coronatine-insensitive 1 Mutation Reveals the Hormonal Signaling Interaction between Abscisic Acid and Methyl Jasmonate in Arabidopsis Guard Cells. Specific Impairment of Ion Channel Activation and Second Messenger Production.
S. Munemasa, K. Oda, M. Watanabe-Sugimoto, Y. Nakamura, Y. Shimoishi, and Y. Murata (2007)
Plant Physiology 143, 1398-1407
   Abstract »    Full Text »    PDF »
Osmo-Sensitive and Stretch-Activated Calcium-Permeable Channels in Vicia faba Guard Cells Are Regulated by Actin Dynamics.
W. Zhang, L.-M. Fan, and W.-H. Wu (2007)
Plant Physiology 143, 1140-1151
   Abstract »    Full Text »    PDF »
Vacuolar transporters and their essential role in plant metabolism.
E. Martinoia, M. Maeshima, and H. E. Neuhaus (2007)
J. Exp. Bot. 58, 83-102
   Abstract »    Full Text »    PDF »
Ca2+-Dependent and -Independent Abscisic Acid Activation of Plasma Membrane Anion Channels in Guard Cells of Nicotiana tabacum.
H. Marten, K. R. Konrad, P. Dietrich, M. R. G. Roelfsema, and R. Hedrich (2007)
Plant Physiology 143, 28-37
   Abstract »    Full Text »    PDF »
The Association Among Gene Expression Responses to Nine Abiotic Stress Treatments in Arabidopsis thaliana.
W. R. Swindell (2006)
Genetics 174, 1811-1824
   Abstract »    Full Text »    PDF »
CO2 signaling in guard cells: Calcium sensitivity response modulation, a Ca2+-independent phase, and CO2 insensitivity of the gca2 mutant.
J. J. Young, S. Mehta, M. Israelsson, J. Godoski, E. Grill, and J. I. Schroeder (2006)
PNAS 103, 7506-7511
   Abstract »    Full Text »    PDF »
Selective Mobility and Sensitivity to SNAREs Is Exhibited by the Arabidopsis KAT1 K+ Channel at the Plasma Membrane.
J.-U. Sutter, P. Campanoni, M. Tyrrell, and M. R. Blatt (2006)
PLANT CELL 18, 935-954
   Abstract »    Full Text »    PDF »
Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications.
S. Shabala, L. Shabala, D. Gradmann, Z. Chen, I. Newman, and S. Mancuso (2006)
J. Exp. Bot. 57, 171-184
   Abstract »    Full Text »    PDF »
Novel CIPK1-Associated Proteins in Arabidopsis Contain an Evolutionarily Conserved C-Terminal Region That Mediates Nuclear Localization.
S. H. Ok, H. J. Jeong, J. M. Bae, J.-S. Shin, S. Luan, and K.-N. Kim (2005)
Plant Physiology 139, 138-150
   Abstract »    Full Text »    PDF »
Cloning and Regulation of a Stress-regulated Pennisetum glaucum Vacuolar ATPase c Gene and Characterization of its Promoter that is Expressed in Shoot Hairs and Floral Organs.
W. Tyagi, D. Rajagopal, S. L. Singla-Pareek, M. K. Reddy, and S. K. Sopory (2005)
Plant Cell Physiol. 46, 1411-1422
   Abstract »    Full Text »    PDF »
A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120.
I. Torrecilla, F. Leganes, I. Bonilla, and F. Fernandez-Pinas (2004)
Microbiology 150, 3731-3739
   Abstract »    Full Text »    PDF »
Ca2+ Dynamics in a Pollen Grain and Papilla Cell during Pollination of Arabidopsis.
M. Iwano, H. Shiba, T. Miwa, F.-S. Che, S. Takayama, T. Nagai, A. Miyawaki, and A. Isogai (2004)
Plant Physiology 136, 3562-3571
   Abstract »    Full Text »    PDF »
The Calcium Conundrum. Both Versatile Nutrient and Specific Signal.
K. D. Hirschi (2004)
Plant Physiology 136, 2438-2442
   Full Text »    PDF »
Differential Expression of Vacuolar H+-ATPase Subunit c Genes in Tissues Active in Membrane Trafficking and Their Roles in Plant Growth as Revealed by RNAi.
S. Padmanaban, X. Lin, I. Perera, Y. Kawamura, and H. Sze (2004)
Plant Physiology 134, 1514-1526
   Abstract »    Full Text »    PDF »
Cytoplasmic Alkalization Precedes Reactive Oxygen Species Production during Methyl Jasmonate- and Abscisic Acid-Induced Stomatal Closure.
D. Suhita, A. S. Raghavendra, J. M. Kwak, and A. Vavasseur (2004)
Plant Physiology 134, 1536-1545
   Abstract »    Full Text »    PDF »
ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells.
R. Desikan, M.-K. Cheung, J. Bright, D. Henson, J. T. Hancock, and S. J. Neill (2004)
J. Exp. Bot. 55, 205-212
   Abstract »    Full Text »    PDF »
Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants.
V. Chinnusamy, K. Schumaker, and J.-K. Zhu (2004)
J. Exp. Bot. 55, 225-236
   Abstract »    Full Text »    PDF »
Urea Transport by Nitrogen-Regulated Tonoplast Intrinsic Proteins in Arabidopsis.
L.-H. Liu, U. Ludewig, B. Gassert, W. B. Frommer, and N. von Wiren (2003)
Plant Physiology 133, 1220-1228
   Abstract »    Full Text »    PDF »
Calcium in Plants.
P. J. WHITE and M. R. BROADLEY (2003)
Ann. Bot. 92, 487-511
   Abstract »    Full Text »    PDF »
Encoding Specificity in Plant Calcium Signalling: Hot-spotting the Ups and Downs and Waves.
C. K.-Y. NG and M. R. MCAINSH (2003)
Ann. Bot. 92, 477-485
   Abstract »    Full Text »    PDF »
Colonization of Flax Roots and Early Physiological Responses of Flax Cells Inoculated with Pathogenic and Nonpathogenic Strains of Fusarium oxysporum.
C. Olivain, S. Trouvelot, M.-N. Binet, C. Cordier, A. Pugin, and C. Alabouvette (2003)
Appl. Envir. Microbiol. 69, 5453-5462
   Abstract »    Full Text »    PDF »
The Arabidopsis cax1 Mutant Exhibits Impaired Ion Homeostasis, Development, and Hormonal Responses and Reveals Interplay among Vacuolar Transporters.
N.-H. Cheng, J. K. Pittman, B. J. Barkla, T. Shigaki, and K. D. Hirschi (2003)
PLANT CELL 15, 347-364
   Abstract »    Full Text »    PDF »
Control of Guard Cell Ion Channels by Hydrogen Peroxide and Abscisic Acid Indicates Their Action through Alternate Signaling Pathways.
B. Kohler, A. Hills, and M. R. Blatt (2003)
Plant Physiology 131, 385-388
   Full Text »    PDF »
Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress.
J. A. Kreps, Y. Wu, H.-S. Chang, T. Zhu, X. Wang, and J. F. Harper (2002)
Plant Physiology 130, 2129-2141
   Abstract »    Full Text »    PDF »
Convergence of Calcium Signaling Pathways of Pathogenic Elicitors and Abscisic Acid in Arabidopsis Guard Cells.
B. Klusener, J. J. Young, Y. Murata, G. J. Allen, I. C. Mori, V. Hugouvieux, and J. I. Schroeder (2002)
Plant Physiology 130, 2152-2163
   Abstract »    Full Text »    PDF »
Disruption of a Guard Cell-Expressed Protein Phosphatase 2A Regulatory Subunit, RCN1, Confers Abscisic Acid Insensitivity in Arabidopsis.
J. M. Kwak, J.-H. Moon, Y. Murata, K. Kuchitsu, N. Leonhardt, A. DeLong, and J. I. Schroeder (2002)
PLANT CELL 14, 2849-2861
   Abstract »    Full Text »    PDF »
Localization, Ion Channel Regulation, and Genetic Interactions during Abscisic Acid Signaling of the Nuclear mRNA Cap-Binding Protein, ABH1.
V. Hugouvieux, Y. Murata, J. J. Young, J. M. Kwak, D. Z. Mackesy, and J. I. Schroeder (2002)
Plant Physiology 130, 1276-1287
   Abstract »    Full Text »    PDF »
Analysis and Effects of Cytosolic Free Calcium Increases in Response to Elicitors in Nicotiana plumbaginifolia Cells.
D. Lecourieux, C. Mazars, N. Pauly, R. Ranjeva, and A. Pugin (2002)
PLANT CELL 14, 2627-2641
   Abstract »    Full Text »    PDF »
Oscillatory Chloride Efflux at the Pollen Tube Apex Has a Role in Growth and Cell Volume Regulation and Is Targeted by Inositol 3,4,5,6-Tetrakisphosphate.
L. Zonia, S. Cordeiro, J. Tupy, and J. A. Feijo (2002)
PLANT CELL 14, 2233-2249
   Abstract »    Full Text »    PDF »
Hypersensitivity of Abscisic Acid-Induced Cytosolic Calcium Increases in the Arabidopsis Farnesyltransferase Mutant era1-2.
G. J. Allen, Y. Murata, S. P. Chu, M. Nafisi, and J. I. Schroeder (2002)
PLANT CELL 14, 1649-1662
   Abstract »    Full Text »    PDF »
Genetic Manipulation of Vacuolar Proton Pumps and Transporters.
R. A. Gaxiola, G. R. Fink, and K. D. Hirschi (2002)
Plant Physiology 129, 967-973
   Full Text »    PDF »
Calcium Signaling through Protein Kinases. The Arabidopsis Calcium-Dependent Protein Kinase Gene Family.
S.-H. Cheng, M. R. Willmann, H.-C. Chen, and J. Sheen (2002)
Plant Physiology 129, 469-485
   Abstract »    Full Text »    PDF »
Abscisic Acid Signaling in Seeds and Seedlings.
R. R. Finkelstein, S. S. L. Gampala, and C. D. Rock (2002)
PLANT CELL 14, S15-45
   Full Text »    PDF »
Calcium at the Crossroads of Signaling.
D. Sanders, J. Pelloux, C. Brownlee, and J. F. Harper (2002)
PLANT CELL 14, S401-417
   Full Text »    PDF »
Hydrogen peroxide homeostasis: Activation of plant catalase by calcium/calmodulin.
T. Yang and B. W. Poovaiah (2002)
PNAS 99, 4097-4102
   Abstract »    Full Text »    PDF »
Abscisic Acid Activation of Plasma Membrane Ca2+ Channels in Guard Cells Requires Cytosolic NAD(P)H and Is Differentially Disrupted Upstream and Downstream of Reactive Oxygen Species Production in abi1-1 and abi2-1 Protein Phosphatase 2C Mutants.
Y. Murata, Z.-M. Pei, I. C. Mori, and J. Schroeder (2001)
PLANT CELL 13, 2513-2523
   Abstract »    Full Text »    PDF »
Combining Genetics and Cell Biology to Crack the Code of Plant Cell Calcium Signaling.
G. J. Allen and J. I. Schroeder (2001)
Sci. STKE 2001, re13
   Abstract »    Full Text »    PDF »
Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump.
R. A. Gaxiola, J. Li, S. Undurraga, L. M. Dang, G. J. Allen, S. L. Alper, and G. R. Fink (2001)
PNAS 98, 11444-11449
   Abstract »    Full Text »    PDF »
Hydrogen Peroxide Is Involved in Abscisic Acid-Induced Stomatal Closure in Vicia faba.
X. Zhang, L. Zhang, F. Dong, J. Gao, D. W. Galbraith, and C.-P. Song (2001)
Plant Physiology 126, 1438-1448
   Abstract »    Full Text »    PDF »
Rapid Low Temperature-Induced Stomatal Closure Occurs in Cold-Tolerant Commelina communis Leaves But Not in Cold-Sensitive Tobacco Leaves, via a Mechanism That Involves Apoplastic Calcium But Not Abscisic Acid.
S. Wilkinson, A. L. Clephan, and W. J. Davies (2001)
Plant Physiology 126, 1566-1578
   Abstract »    Full Text »    PDF »
The Ca2+ Status of the Endoplasmic Reticulum Is Altered by Induction of Calreticulin Expression in Transgenic Plants.
S. Persson, S. E. Wyatt, J. Love, W. F. Thompson, D. Robertson, and W. F. Boss (2001)
Plant Physiology 126, 1092-1104
   Abstract »    Full Text »    PDF »
Inventory of the Superfamily of P-Type Ion Pumps in Arabidopsis.
K. B. Axelsen and M. G. Palmgren (2001)
Plant Physiology 126, 696-706
   Abstract »    Full Text »    PDF »
Pharmacological Analysis of Nod Factor-Induced Calcium Spiking in Medicago truncatula. Evidence for the Requirement of Type IIA Calcium Pumps and Phosphoinositide Signaling.
E. M. Engstrom, D. W. Ehrhardt, R. M. Mitra, and S. R. Long (2002)
Plant Physiology 128, 1390-1401
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)