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J. Biol. Chem., Vol. 283, Issue 6, 3497-3506, February 8, 2008

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A Plant Ca²⁺ Pump, ACA2, Relieves Salt Hypersensitivity in Yeast

MODULATION OF CYTOSOLIC CALCIUM SIGNATURE AND ACTIVATION OF ADAPTIVE Na⁺ HOMEOSTASIS^*

From the National Centre for Biological Sciences, Bangalore 560 065, India

Stress responses in both plants and yeast utilize calcium-mediated signaling. A yeast strain, K616, which lacks Ca²⁺ pumps, requires micromolar Ca²⁺ for growth. In medium containing 100 µM Ca²⁺, K616 can withstand osmotic stress (750 mM sorbitol) and ionic stress (300 mM KCl) but not hypersodic stress (300 mM NaCl). Heterologous expression of the endoplasmic reticulum-located Arabidopsis thaliana Ca²⁺-ATPase, ACA2, permits K616 to grow under NaCl stress even in Ca²⁺-depleted medium. All stresses tested generated transient elevation of cytosolic Ca²⁺ in wild type yeast, K601, whereas NaCl alone induced prolonged elevation of cytosolic Ca²⁺ in K616. Both the Ca²⁺ transient and survival of cultures subjected to NaCl stress was similar for the ACA2 transformant and K601. However, whereas K601 maintained low cytosolic Na⁺ predominantly by pumping it out across the plasma membrane, the transformant sequestered Na⁺ in internal organelles. This sequestration requires the presence of an endomembrane Na⁺/H⁺-antiporter, NHX1, which does not play a significant role in salt tolerance of wild type yeast except at acidic pH. Transcript levels of the plasma membrane Na⁺-ATPase, ENA1, were strongly induced only in K601, whereas NHX1 was strongly induced in both K601 and the ACA2 transformant. The calmodulin kinase inhibitor KN62 significantly reduced the salt tolerance of the ACA2 transformant and the transcriptional induction of NHX1. Thus, the heterologous expression of a plant endomembrane Ca²⁺ pump results in the rapid depletion of cytosolic Ca²⁺ and the activation of an alternate mechanism for surviving saline stress.

Received for publication, January 26, 2007 , and in revised form, December 7, 2007.

^* This work was supported by internal funds of National Centre for Biological Sciences and by a Fast Track grant for Young Scientists, Department of Science and Technology, Government of India (to V. S. A.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement"in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1-3.

¹ To whom correspondence should be addressed: National Centre for Biological Sciences, UAS-GKVK Campus, Bellary Rd., Bangalore 560 065, India. Tel.: 91-80-23636421 (ext. 3270); Fax: 91-80-23636662; E-mail: mathew{at}ncbs.res.in.

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