Calcium efflux systems in stress signaling and adaptation in plants

Transient cytosolic calcium ([Ca²⁺]_cyt) elevation is an ubiquitous denominator of the signaling network when plants are exposed to literally every known abiotic and biotic stress. These stress-induced [Ca²⁺]_cyt elevations vary in magnitude, frequency, and shape, depending on the severity of the stress as well the type of stress experienced. This creates a unique stress-specific calcium “signature” that is then decoded by signal transduction networks. While most published papers have been focused predominantly on the role of Ca²⁺ influx mechanisms to shaping [Ca²⁺]_cyt signatures, restoration of the basal [Ca²⁺]_cyt levels is impossible without both cytosolic Ca²⁺ buffering and efficient Ca²⁺ efflux mechanisms removing excess Ca²⁺ from cytosol, to reload Ca²⁺ stores and to terminate Ca²⁺ signaling. This is the topic of the current review. The molecular identity of two major types of Ca²⁺ efflux systems, Ca²⁺-ATPase pumps and Ca²⁺/H⁺ exchangers, is described, and their regulatory modes are analyzed in detail. The spatial and temporal organization of calcium signaling networks is described, and the importance of existence of intracellular calcium microdomains is discussed. Experimental evidence for the role of Ca²⁺ efflux systems in plant responses to a range of abiotic and biotic factors is summarized. Contribution of Ca²⁺-ATPase pumps and Ca²⁺/H⁺ exchangers in shaping [Ca²⁺]_cyt signatures is then modeled by using a four-component model (plasma- and endo-membrane-based Ca²⁺-permeable channels and efflux systems) taking into account the cytosolic Ca²⁺ buffering. It is concluded that physiologically relevant variations in the activity of Ca²⁺-ATPase pumps and Ca²⁺/H⁺ exchangers are sufficient to fully describe all the reported experimental evidence and determine the shape of [Ca²⁺]_cyt signatures in response to environmental stimuli, emphasizing the crucial role these active efflux systems play in plant adaptive responses to environment.