A Putative Chloroplast-Localized Ca 2+ /H + Antiporter CCHA1 Is Involved in Calcium and pH Homeostasis and Required for PSII Function in Arabidopsis

Abstract

Calcium is important for chloroplast, not only in its photosynthetic but also nonphotosynthetic functions. Multiple Ca(2+)/H(+) transporters and channels have been described and studied in the plasma membrane and organelle membranes of plant cells; however, the molecular identity and physiological roles of chloroplast Ca(2+)/H(+) antiporters have remained unknown. Here we report the identification and characterization of a member of the UPF0016 family, CCHA1 (a chloroplast-localized potential Ca(2+)/H(+) antiporter), in Arabidopsis thaliana. We observed that the ccha1 mutant plants developed pale green leaves and showed severely stunted growth along with impaired photosystem II (PSII) function. CCHA1 localizes to the chloroplasts, and the levels of the PSII core subunits and the oxygen-evolving complex were significantly decreased in the ccha1 mutants compared with the wild type. In high Ca(2+) concentrations, Arabidopsis CCHA1 partially rescued the growth defect of yeast gdt1Δ null mutant, which is defective in a Ca(2+)/H(+) antiporter. The ccha1 mutant plants also showed significant sensitivity to high concentrations of CaCl2 and MnCl2, as well as variation in pH. Taken these results together, we propose that CCHA1 might encode a putative chloroplast-localized Ca(2+)/H(+) antiporter with critical functions in the regulation of PSII and in chloroplast Ca(2+) and pH homeostasis in Arabidopsis.

An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis

“…However, alternative explanation in the light of the recent finding by Davis et al () could be that the elevated ΔΨ may have enhanced PSII photodamage impacting growth. Wang et al () found that mutants of the same transporter (named CCHA1 in their study) were sensitive to pH changes in the growth media, and had increased pH and higher Ca 2+ concentrations in the cytosol relative to the wild‐type. These observations are not fully consistent with the analyses by Schneider et al (), which pointed to enrichment of Ca 2+ and a less acidic pH in the thylakoid lumen in the light.…”

“…The pam71 mutants did not differ from the wild‐type in organization of chloroplast and thylakoid membranes (Schneider et al ). However, Wang et al () found fewer and smaller chloroplasts with shorter distance between the grana stacks for mutants of the same gene ( ccha1 ). The reasons behind the discrepancy between the results of the two studies are not clear.…”

Calcium transport across plant membranes: mechanisms and functions

“…These transporters were previously defined as AtCAX7–AtCAX11 and encode K + ‐dependent Na + /Ca 2+ exchangers (Maser et al ., ; Shigaki et al ., ). The list is growing; recently a novel chloroplast‐localized potential Ca 2+ /H + antiporter (CCHA1) from the UPF0016 calcium‐proton exchanger family was discovered (Wang et al ., ,b).…”

“…Owing to their important role in regulating both intracellular and apoplastic pH (Cho et al ., ), CAXs are instrumental in a broad range of developmental processes. Both CAX expression levels and activity are highly cell type‐specific (Punshon et al ., ; Wang et al ., ,b) and modulated by various stresses, particularly by heavy metals. Some selected examples depicting the role of specific CAX isoforms in stress‐induced adaptive responses are given in Table S2.…”

Acidic and uncharged polar residues in the consensus motifs of the yeast Ca2+ transporter Gdt1p are required for calcium transport

“…Besides the human TMEM165 or the yeast Gdt1p, extensive studies of diverse members of the UPF0016 family were recently initiated. The Arabidopsis thaliana UPF0016 member CCHA1 has been assumed to act as a chloroplast‐localized Ca 2+ /H + antiporter and to play a critical role in the regulation of photosystem II (Schneider et al, ; Wang et al, ). Furthermore, the transport of divalent cations by the Vibrio cholerae UPF0016 member MneA has been reported by Fisher, Wyckoff, Peng, and Payne ().…”