Cracking the calcium code

Abstract

Cytosolic calcium has long been recognized as a second messenger for many intrinsic or environmental signals in animals and plants. In plant cells, cytosolic calcium elevations can be triggered by hormonal signals, such as abscisic acid (ABA) and auxins; abiotic environmental signals, such as cold or mechanical stimulation; and biotic signals involved in the recognition of pathogens or symbiotic organisms. It is intriguing that, although all these signals use cytosolic calcium as a second messenger, they give rise to different and sometimes even opposite physiological, biochemical or developmental responses. Thus, it has been hypothesized that the calcium signals involved have different features that enable the cells to use the same second messenger to generate distinct downstream responses. Indeed, calcium signals can differ in their amplitude, as well as in their spatial and temporal patterns. Recently, it was shown that calcium signals in Arabidopsis guard cells exhibit stimulus-specific patterns of oscillations and that an oscillating calcium signal is required for stomatal closure. However, until now there has been no evidence that a specific pattern of calcium oscillations is required to control a specific downstream physiological response.In a recent issue of Nature, Gethyn Allen et al. 1xA defined range of guard cell calcium oscillation parameters encodes stomatal movements. Allen, G.J. et al. Nature. 2001; 411: 1053–1057Crossref | PubMed | Scopus (340)See all References1 analyze the relationships between the temporal pattern of calcium oscillations in guard cells and the physiological response of stomatal closure in Arabidopsis. The authors generate cytosolic calcium oscillations with a set frequency and duration by repeatedly switching the guard cells under investigation rapidly from a low-calcium, depolarizing buffer to a high-calcium, hyperpolarizing buffer, to induce calcium influx. In guard cells engineered to express the GFP-based calcium indicator, cameleon, they monitor the stomatal aperture and the intracellular calcium concentration in parallel, observing that a single intracellular calcium elevation is sufficient to trigger fast stomatal closure. However, this ‘calcium-reactive’ closure can only be maintained and lead to long-term stomatal closure if the initial calcium elevation is followed by oscillations with a defined pattern. Using the calcium clamp-buffer system, the authors determine the number, duration and frequency parameters that are optimal to induce long-term ‘calcium programmed’ stomatal closure. Interestingly, these parameters fit with the parameters of calcium oscillations induced by ABA – a physiological signal that induces long-term stomatal closure.Moreover, the authors provide genetic evidence that the frequency and duration parameters of the oscillations are crucial for ABA-induced stomatal closure. They show that ABA triggers cytosolic calcium oscillations in guard cells of the ABA-insensitive mutant, gca2. However, the frequency of the oscillations is higher than in the wild type, the duration of the transients is much shorter and ABA fails to induce long-term ‘calcium programmed’ stomatal closure in this mutant. Nevertheless, long-term stomatal closure can be restored in the guard cells of gca2 by imposing calcium oscillations with a frequency and transient duration that cause long-term closure in the wild type.This study represents a major step towards understanding the specificity of calcium signaling in plant cells because it demonstrates a relationship between a defined pattern of cytosolic calcium oscillations and a downstream physiological response. It should trigger much interest in the analysis of the molecular machinery of calcium channels, pumps and transporters that generate endogenous calcium oscillations in plants, as well as the calcium-dependent pathways that decode the frequency and duration parameters of the calcium oscillations.