First published online July 29, 2005; 10.1104/pp.105.061218
Plant Physiology 138:2048-2060 (2005)
© 2005 American Society of Plant Biologists
ENVIRONMENTAL STRESS AND ADAPTATION
Functional Association of Arabidopsis CAX1 and CAX3 Is Required for Normal Growth and Ion Homeostasis1
Ning-Hui Cheng,
Jon K. Pittman2,
Toshiro Shigaki,
Jinesh Lachmansingh,
Sherry LeClere,
Brett Lahner,
David E. Salt and
Kendal D. Hirschi*
United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center (N.-H.C., J.K.P., T.S., J.L., S.L., K.D.H.), and Department of Human and Molecular Genetics (K.D.H.), Baylor College of Medicine, Houston, Texas 77030; Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (B.L., D.E.S.); and Vegetable and Fruit Improvement Center, Texas A&M University, College Station, Texas 77845 (K.D.H.)
Cation levels within the cytosol are coordinated by a network of transporters. Here, we examine the functional roles of calcium exchanger 1 (CAX1), a vacuolar H+/Ca2+ transporter, and the closely related transporter CAX3. We demonstrate that like CAX1, CAX3 is also localized to the tonoplast. We show that CAX1 is predominately expressed in leaves, while CAX3 is highly expressed in roots. Previously, using a yeast assay, we demonstrated that an N-terminal truncation of CAX1 functions as an H+/Ca2+ transporter. Here, we use the same yeast assay to show that full-length CAX1 and full-length CAX3 can partially, but not fully, suppress the Ca2+ hypersensitive yeast phenotype and coexpression of full-length CAX1 and CAX3 conferred phenotypes not produced when either transporter was expressed individually. In planta, CAX3 null alleles were modestly sensitive to exogenous Ca2+ and also displayed a 22% reduction in vacuolar H+-ATPase activity. cax1/cax3 double mutants displayed a severe reduction in growth, including leaf tip and flower necrosis and pronounced sensitivity to exogenous Ca2+ and other ions. These growth defects were partially suppressed by addition of exogenous Mg2+. The double mutant displayed a 42% decrease in vacuolar H+/Ca2+ transport, and a 47% decrease in H+-ATPase activity. While the ionome of cax1 and cax3 lines were modestly perturbed, the cax1/cax3 lines displayed increased PO43–, Mn2+, and Zn2+ and decreased Ca2+ and Mg2+ in shoot tissue. These findings suggest synergistic function of CAX1 and CAX3 in plant growth and nutrient acquisition.
1 This work was supported by the U.S. Department of Agriculture/Agricultural Research Service (under Cooperative Agreement 58–6250–6001) and by the National Science Foundation (grant nos. 020977 and 0077378–DBI to D.E.S.).
2 Present address: Faculty of Life Sciences, University of Manchester, 3.614 Stopford Building, Oxford Road, Manchester M13 9PT, UK.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.061218.
* Corresponding author; e-mail kendalh{at}bcm.tmc.edu; fax 713–798–7078.
Received February 12, 2005;
returned for revision March 29, 2005;
accepted April 25, 2005.
This article has been cited by other articles:
|
|
|
|
 
W.-Y. Lin, S.-I Lin, and T.-J. Chiou
Molecular regulators of phosphate homeostasis in plants
J. Exp. Bot.,
April 1, 2009;
60(5):
1427 - 1438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Zhao, T. Shigaki, H. Mei, Y.-q. Guo, N.-H. Cheng, and K. D. Hirschi
Interaction between Arabidopsis Ca2+/H+ Exchangers CAX1 and CAX3
J. Biol. Chem.,
February 13, 2009;
284(7):
4605 - 4615.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Qudeimat, A. M. C. Faltusz, G. Wheeler, D. Lang, C. Brownlee, R. Reski, and W. Frank
A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens
PNAS,
December 9, 2008;
105(49):
19555 - 19560.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Yu, X. Chen, Y.-Y. Hong, Y. Wang, P. Xu, S.-D. Ke, H.-Y. Liu, J.-K. Zhu, D. J. Oliver, and C.-B. Xiang
Activated Expression of an Arabidopsis HD-START Protein Confers Drought Tolerance with Improved Root System and Reduced Stomatal Density
PLANT CELL,
April 1, 2008;
20(4):
1134 - 1151.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Sundaram, B. Rathinasabapathi, L. Q. Ma, and B. P. Rosen
An Arsenate-activated Glutaredoxin from the Arsenic Hyperaccumulator Fern Pteris vittata L. Regulates Intracellular Arsenite
J. Biol. Chem.,
March 7, 2008;
283(10):
6095 - 6101.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. F. Mills, M. L. Doherty, R. L. Lopez-Marques, T. Weimar, P. Dupree, M. G. Palmgren, J. K. Pittman, and L. E. Williams
ECA3, a Golgi-Localized P2A-Type ATPase, Plays a Crucial Role in Manganese Nutrition in Arabidopsis
Plant Physiology,
January 1, 2008;
146(1):
116 - 128.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Mei, J. Zhao, J. K. Pittman, J. Lachmansingh, S. Park, and K. D. Hirschi
In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1
J. Exp. Bot.,
September 26, 2007;
(2007)
erm190v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. J. Im, I. Y. Perera, I. Brglez, A. J. Davis, J. Stevenson-Paulik, B. Q. Phillippy, E. Johannes, N. S. Allen, and W. F. Boss
Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism in Nicotiana tabacum
PLANT CELL,
May 1, 2007;
19(5):
1603 - 1616.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Martinoia, M. Maeshima, and H. E. Neuhaus
Vacuolar transporters and their essential role in plant metabolism
J. Exp. Bot.,
January 1, 2007;
58(1):
83 - 102.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Park, N. H. Cheng, J. K. Pittman, K. S. Yoo, J. Park, R. H. Smith, and K. D. Hirschi
Increased Calcium Levels and Prolonged Shelf Life in Tomatoes Expressing Arabidopsis H+/Ca2+ Transporters
Plant Physiology,
November 1, 2005;
139(3):
1194 - 1206.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
