Extracellular Ca2+ induces desensitized cytosolic Ca2+ rise sensitive to phospholipase C inhibitor which suppresses root growth with Ca2+ dependence

Abstract

Calcium (Ca) is an essential element for all organisms. In animal cells, the plasma membrane-localized Ca receptor CaSR coupled to a phospholipase C (PLC)-dependent signaling cascade monitors extracellular Ca2+ concentrations ([Ca2+]ext) and responds with increases in cytosolic calcium concentrations ([Ca2+]cyt). Plant roots encounter variable soil conditions, but how they sense changes in [Ca2+]ext is largely unknown. In this study, we demonstrate that increasing [Ca2+]ext evokes a transient increase in [Ca2+] in the cytosol, mitochondria, and nuclei of Arabidopsis thaliana root cells. These increases were strongly desensitized to repeat applications of [Ca2+]ext, a typical feature of receptor-mediated cellular signaling in animal and plant cells. Treatment with gadolinium (Gd3+), a CaSR activator in animal cells, induced concentration-dependent increases in [Ca2+]cyt in roots, which showed self-desensitization and cross-desensitization to [Ca2+]ext-induced increases in [Ca2+]cyt (EICC). EICC was sensitive to extracellular H+, K+, Na+, and Mg2+ levels. Treatment with the PLC inhibitor neomycin suppressed EICC and Ca accumulation in roots. The inhibitory effect of neomycin on root elongation was fully rescued by increasing [Ca2+]ext but not [Mg2+] or [K+] in the growth medium. These results suggest that [Ca2+]ext and the movement of Ca2+ into the cytosol of plant roots are regulated by a receptor-mediated signaling pathway involving PLC.