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.
Highlights
Calcium (Ca) is an essential plant macronutrient with unique structural and signaling roles (White and Broadley, 2003)
By equalizing [Ca]apo in cax1/cax3 and Col-0 using LCS, these phenotypes were recovered to Col-0 wild-type levels, but again reappeared when plants were returned to basal nutrient solution (BNS) (RBNS) (Figure 3B)
Three amplifications were performed on three independent plants to those used in Figure 2A, with data presented as mean normalized expression levels + SE. quantitative PCR (qPCR) was performed in triplicate for each biological replicate. (C) Difference in Ca, P, and K concentration in adaxial epidermal and palisade mesophyll cells between the Col-0 parent and T-DNA insertion lines aca4/ aca11 and cax1/cax3
Summary
Calcium (Ca) is an essential plant macronutrient with unique structural and signaling roles (White and Broadley, 2003). Studies of rough lemon (Citrus jambhiri) in which all leaf cells were exposed to strontium ions (as a tracer for Ca2+) or high apoplastic [Ca2+] ([Ca2+]apo) demonstrated that only certain cells had the ability to accumulate significant [Ca]vac (Storey and Leigh, 2004) This suggests transport capabilities of different cell types determine the ability to store Ca2+. Numerous transcripts were identified that were disproportionately expressed between these cell types, but only disruption of CAX expression reduced the ability of mesophyll cells to accumulate Ca2+ within the vacuole This resulted in an increase in apoplastic free [Ca2+] and reductions in transpiration, CO2 assimilation, cell wall extensibility, and growth. We summarize our findings in a model that highlights the mechanisms underpinning cell-specific vacuolar Ca2+ storage as an essential physiological process in maintaining optimal transpiration and CO2 assimilation, cell wall extensibility, and plant productivity
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