Encoding specificity in plant calcium signalling: hot-spotting the ups and downs and waves

Abstract

Calcium ions function as intracellular second messengers in regulating a plethora of cellular processes from acclimative stress responses to survival and programmed cell death. The generation of specificity in Ca2+ signals is dependent on influx and efflux from the extracellular milieu, cytosol and intracellular organelles. One aspect of plant Ca2+ signalling that is currently attracting a great deal of interest is how 'Ca2+-signatures', specific spatio-temporal changes in cytosolic-free Ca2+, encode the necessary information to bring about this range of physiological responses. Here, current information is reviewed on how Ca2+-signatures are generated in plant cells and how stimulus-specific information can be encoded in the form of Ca2+-signatures.

Fig. 1. Elemental Ca²⁺ elevations during Ca²⁺ wave propagation in a Fucus rhizoid cell. (A), Single‐line confocal scans of Ca²⁺ Green fluorescence along the longitudinal axis of the cell during the initation of Ca²⁺ waves are displayed sequentially to show the relative change in fluorescence following hypo‐osmotic treatment (to 50 % sea water). (B), Three‐dimensional plot shows a non‐uniform increase in Ca²⁺ during the onset of the Ca²⁺ wave in the rhizoid apex. (C), Elemental Ca²⁺ elevations in the perinuclear region. (D), Elemental Ca²⁺ events appear to arise repetitively at the same location in perinuclear region. Reproduced, with persmission, from Goddard et al. (2000).

Fig. 2. Spatial heterogeneities in guard cell [Ca²⁺]_cyt in response to 100 nM ABA (A) and 1 mm [Ca²⁺]_ext (B). [Ca²⁺]_cyt levels are colour‐coded; blue indicates low [Ca²⁺]_cyt, red indicates high [Ca²⁺]_cyt. These data suggest that plant cells have the capacity to encode specificity in the Ca²⁺ signal in the form of localized increases in [Ca²⁺]_cyt. Reproduced, with permission, from McAinsh et al. (1992, 1995).

Fig. 3. (Opposite) Elemental Ca²⁺ elevations during Ca²⁺ wave propagation in a Fucus rhizoid cell and patterns of Ca²⁺ elevations following hypo‐osmotic treatment in dividing cells. (A), Elemental Ca²⁺ events in the perinuclear region either occur individually or appeared to cluster into more prolonged elevations. (B), Number of discrete elevations at the rhizoid apex increased initially during the first 1·5 s of wave propagation and then declined with the appearance of more prolonged elevations. (C), Ca²⁺ Green to Teax Red ratio images during the onset of a hypo‐osmotically induced Ca²⁺ waves (100 % sea water to 50 % sea water) shows an initial elevation of Ca²⁺ in the rhizoid apex which declines before the onset of Ca²⁺ elevation arising in the apical nucleus region. (D), A minority of cells shows a variation of the pattern shown in part C where the Ca²⁺ elevations were observed to arise in the subapical nucleus simultaneous with the apical Ca²⁺ elevation. Reproduced, with permission, from Goddard et al. (2000).

Fig. 4. Proposed signalling pathway during hyperosmotic stress in Fucus embryos. Osmotic change is sensed by an unidentified sensor leading to the production of extracellular ROS production (which may be important for strengthening the cell wall). The H₂O₂ formed also diffuses into the cell, leading to localized peripheral intracellular increase. The extracellular H₂O₂ also increases Ca²⁺‐channel activity. This leads to Ca²⁺‐induced Ca²⁺ release from intracellular stores (ER) resulting in Ca²⁺ wave propagation and mitochondrial ROS production. Reproduced, with permission, from Coelho et al. (2002).

Fig. 5. Encoding signalling information in plant Ca²⁺ signatures. (A), In guard cells the strength of the stimulus has been correlated directly with the pattern of [Ca²⁺]_cyt oscillations (i.e. the period, frequency and amplitude) which, in turn, dictates the resultant steady‐state stomatal aperture. (B), Guard cells are able to integrate signalling information from a number of stimuli that induce oscillations in [Ca²⁺]_cyt applied simultaneously to generate a novel Ca²⁺ signature when formulating the final stomatal aperture. Reproduced, with permission, from Evans et al. (2001).