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Calcium ion transporting systems control cytosol Ca2+ levels ([Ca2+]cyt) and generate transient calcium (Ca2+) signatures which are considered to be key to environmental responses. Here, we report an impact of resting [Ca2+]cyt on plants from the functional study of calmodulin regulated Ca2+ pumps or Ca2+-ATPases in Arabidopsis thaliana. The plasma membrane localized pumps ACA8 and ACA10 as well as the vacuole localized pumps ACA4 and ACA11 are found to be critical in maintaining low resting [Ca2+]cyt and be essential for plant survival under chilling and heat-stress conditions. Their loss-of-function mutants aca8 aca10 and aca4 aca11 have autoimmunity at normal temperature, and this deregulated immune activation is enhanced by low temperature leading to chilling lethality. Furthermore, these two mutants have an elevated resting [Ca2+]cyt, and a reduction of external Ca2+ lowers [Ca2+]cyt and represses its autoimmunity and cold susceptibility. The aca8 aca10 and the aca4 aca11 mutants are also susceptible to heat, likely resulting from more closed stomata and higher leaf surface temperature compared to the wild type. These observations support a model in which the regulation of resting [Ca2+]cyt is critical to how plants regulate biotic and abiotic responses.