Cell-Specific Vacuolar Calcium Storage Mediated by CAX1 Regulates Apoplastic Calcium Concentration, Gas Exchange, and Plant Productivity in Arabidopsis
2011
Conn, Simon J. | Gilliham, Matthew | Athman, Asmini | Schreiber, A. W. (Andreas W) | Baumann, Ute | Moller, Isabel | Cheng, Ning-Hui | Stancombe, Matthew A. | Hirschi, Kendal D. | Webb, Alex A.R. | Burton, Rachel | Kaiser, Brent N. | Tyerman, Stephen D. | Leigh, R. A. (Roger A)
The physiological role and mechanism of nutrient storage within vacuoles of specific cell types is poorly understood. Transcript profiles from Arabidopsis thaliana leaf cells differing in calcium concentration ([Ca], epidermis <10 mM versus mesophyll >60 mM) were compared using a microarray screen and single-cell quantitative PCR. Three tonoplast-localized Ca²⁺ transporters, CAX1 (Ca²⁺/H⁺-antiporter), ACA4, and ACA11 (Ca²⁺-ATPases), were identified as preferentially expressed in Ca-rich mesophyll. Analysis of respective loss-of-function mutants demonstrated that only a mutant that lacked expression of both CAX1 and CAX3, a gene ectopically expressed in leaves upon knockout of CAX1, had reduced mesophyll [Ca]. Reduced capacity for mesophyll Ca accumulation resulted in reduced cell wall extensibility, stomatal aperture, transpiration, CO₂ assimilation, and leaf growth rate; increased transcript abundance of other Ca²⁺ transporter genes; altered expression of cell wall-modifying proteins, including members of the pectinmethylesterase, expansin, cellulose synthase, and polygalacturonase families; and higher pectin concentrations and thicker cell walls. We demonstrate that these phenotypes result from altered apoplastic free [Ca²⁺], which is threefold greater in cax1/cax3 than in wild-type plants. We establish CAX1 as a key regulator of apoplastic [Ca²⁺] through compartmentation into mesophyll vacuoles, a mechanism essential for optimal plant function and productivity.
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