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Plant Physiol, September 2002, Vol. 130, pp. 128-137
An Endoplasmic Reticulum-Bound Ca2+/Mn2+
Pump, ECA1, Supports Plant Growth and Confers Tolerance to
Mn2+ Stress1
Zhongyi
Wu,
Feng
Liang,2
Bimei
Hong,
Jeff C.
Young,3
Michael R.
Sussman,
Jeffrey F.
Harper, and
Heven
Sze*
Department of Cell Biology and Molecular Genetics, University of
Maryland, College Park, Maryland 20742 (Z.W., F.L., H.S.); Department
of Cell Biology, Plant Division, The Scripps Research Institute, La
Jolla, California 92037 (B.H., J.F.H.); and Biotechnology Center, 425 Henry Mall, University of Wisconsin, Madison, Wisconsin 53706 (J.C.Y.,
M.R.S.)
Plants can grow in soils containing highly variable amounts
of mineral nutrients, like Ca2+ and Mn2+,
though the mechanisms of adaptation are poorly understood. Here, we
report the first genetic study to determine in vivo functions of a
Ca2+ pump in plants. Homozygous mutants of Arabidopsis
harboring a T-DNA disruption in ECA1 showed a 4-fold reduction in
endoplasmic reticulum-type calcium pump activity. Surprisingly, the
phenotype of mutant plants was indistinguishable from wild type when
grown on standard nutrient medium containing 1.5 mM
Ca2+ and 50 µM Mn2+. However,
mutants grew poorly on medium with low Ca2+ (0.2 mM) or high Mn2+ (0.5 mM). On high
Mn2+, the mutants failed to elongate their root hairs,
suggesting impairment in tip growth processes. Expression of the
wild-type gene (CAMV35S::ECA1) reversed these conditional
phenotypes. The activity of ECA1 was examined by expression in a yeast
(Saccharomyces cerevisiae) mutant, K616, which harbors a
deletion of its endogenous calcium pumps. In vitro assays demonstrated
that Ca2+, Mn2+, and Zn2+
stimulated formation of a phosphoenzyme intermediate, consistent with
the translocation of these ions by the pump. ECA1 provided increased
tolerance of yeast mutant to toxic levels of Mn2+ (1 mM) and Zn2+(3 mM), consistent with
removal of these ions from the cytoplasm. These results show that
despite the potential redundancy of multiple Ca2+ pumps and
Ca2+/H+ antiporters in Arabidopsis, pumping of
Ca2+ and Mn2+ by ECA1 into the endoplasmic
reticulum is required to support plant growth under conditions of
Ca2+ deficiency or Mn2+ toxicity.
1
This work was supported by the
Department of Energy (grant nos. DE-FG02-95ER202200 to H.S. and
DE-FG03-94ER20152 to J.F.H.), by the National Science Foundation
(grant no. DBI 0077378 to J.F.H.), and by Syngenta (to J.F.H.).
2
Present address: Invitrogen Corp., Carlsbad, CA 92008.
3
Present address: Biology Department, Western Washington
University, Bellingham, WA 98225.
*
Corresponding author; e-mail hs29{at}umail.umd.edu; fax
301-314-9081.
© 2002 American Society of Plant Physiologists
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