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Title: Cell-specific vacuolar calcium storage mediated by "CAX1" regulates apoplastic calcium concentration, gas exchange, and plant productivity in "Arabidopsis"

Author
item CONN, SIMON - University Of Adelaide
item GILLIHAM, MATTHEW - University Of Adelaide
item ATHMAN, ASMINI - University Of Adelaide
item SCHREIBER, ANDREAS - University Of Adelaide
item BAUMANN, UTE - University Of Adelaide
item MOLLER, ISABEL - University Of Melbourne
item CHENG, NING-HUI - Children'S Nutrition Research Center (CNRC)
item STANCOMBE, MATTHEW - University Of Cambridge
item HIRSCHI, KENDAL - Children'S Nutrition Research Center (CNRC)
item WEBB, ALEX - University Of Cambridge
item BURTON, RACHEL - University Of Adelaide
item KAISER, BRENT - University Of Adelaide
item TYERMAN, STEPHEN - University Of Adelaide
item LEIGH, ROGER - University Of Adelaide

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/17/2010
Publication Date: 1/21/2011
Citation: Conn, S.J., Gilliham, M., Athman, A., Schreiber, A.W., Baumann, U., Moller, I., Cheng, N., Stancombe, M.A., Hirschi, K.D., Webb, A.A. 2011. Cell-specific vacuolar calcium storage mediated by "CAX1" regulates apoplastic calcium concentration, gas exchange, and plant productivity in "Arabidopsis". The Plant Cell. 23(1):240-257.

Interpretive Summary: The ability to alter nutrient content in plants may alter growth and the nutritional content of the food. Here we demonstrate that altered expression of calcium transporters can dramatically change calcium concentrations in the plant. We demonstrate a loss of function in two calcium transporters can cause a three-fold increase in the amount of calcium found in the plant circulatory system. This may be due to the fact that plants cannot store the calcium within the cells. This work documents alterations in plant stress responses and development. Future work will establish how these alterations impact nutrient content in foods.

Technical Abstract: 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 Ca (2+) transporters, CAX1 (Ca (2+)/H (+)-antiporter), ACA4, and ACA11 (Ca (2+)-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, CO[2] assimilation, and leaf growth rate; increased transcript abundance of other Ca(2+) 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 [Ca (2+)], which is threefold greater in "cax1/cax3" than in wild-type plants. We establish "CAX1" as a key regulator of apoplastic [Ca (2+)] through compartmentation into mesophyll vacuoles, a mechanism essential for optimal plant function and productivity.