Salt stress-induced Ca ²⁺ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Abstract

Their sessile lifestyle means that plants have to be exquisitely sensitive to their environment, integrating many signals to appropriate developmental and physiological responses. Stimuli ranging from wounding and pathogen attack to the distribution of water and nutrients in the soil are frequently presented in a localized manner but responses are often elicited throughout the plant. Such systemic signaling is thought to operate through the redistribution of a host of chemical regulators including peptides, RNAs, ions, metabolites, and hormones. However, there are hints of a much more rapid communication network that has been proposed to involve signals ranging from action and system potentials to reactive oxygen species. We now show that plants also possess a rapid stress signaling system based on Ca 2+ waves that propagate through the plant at rates of up to ∼400 μm/s. In the case of local salt stress to the Arabidopsis thaliana root, Ca 2+ wave propagation is channeled through the cortex and endodermal cell layers and this movement is dependent on the vacuolar ion channel TPC1. We also provide evidence that the Ca 2+ wave/TPC1 system likely elicits systemic molecular responses in target organs and may contribute to whole-plant stress tolerance. These results suggest that, although plants do not have a nervous system, they do possess a sensory network that uses ion fluxes moving through defined cell types to rapidly transmit information between distant sites within the organism.Ca 2+ signaling | Yellow Cameleon | Two Pore Channel 1 P lants are constantly tailoring their responses to current environmental conditions via a complex array of chemical regulators that integrate developmental and physiological programs across the plant body. Environmental stimuli are often highly localized in nature, but the subsequent plant response is often elicited throughout the entire organism. For example, soil is a highly heterogeneous environment and the root encounters stimuli that are presented in a patchy manner. Thus, factors including dry or waterlogged regions of the soil, variations in the osmotic environment, and stresses such as elevated levels of salt are all likely to be encountered locally by individual root tips, but the information may have to be acted on by the plant as a whole.In animals, long-range signaling to integrate activities across the organism occurs through rapid ionic/membrane potentialdriven signaling through the nervous system in addition to operating via long-distance chemical signaling. Plants have also been proposed to possess a rapid, systemic communication network, potentially mediated through signals ranging from changes in membrane potential/ion fluxes (1-3) and levels of reactive oxygen species (ROS) (4, 5) to altered hydraulics in the vasculature (6). Even so, the molecular mechanisms behind rapid, systemic signaling in plants and whether such signals indeed carry regulatory information remains largely unknown. Suggestions that Ca 2+ channels play a role in signals that occlude sieve tube...

Rapid hyperosmotic-induced Ca 2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters

“…We observed that stimulation of the seedlings by hyperosmotic stress resulted in a rapid, transient rise in [Ca 2+ ] i ( Fig. 1 A-D), consistent with previous reports (5,9,12,15). When seedlings were stimulated by a low-osmolarity solution iso-osmotic to the existing medium, only small responses were observed ( Fig.…”

“…There is some debate about the site of initial generation of rapid hyperosmotic-induced Ca 2+ responses, and the site may depend on experimental conditions. Although some studies show that the Ca 2+ signal first appears in roots (9,12), another indicates that the Ca 2+ signal may occur simultaneously and more strongly in the shoots (15). The Ca 2+ response occurs in many cell types, but it is reported to be largest and to occur earliest within cells of the root epidermis (24,28).…”

“…Individual seedling responses tend to be quite heterogeneous, and the response characteristics show variation depending on the accession or extracellular ionic composition (9,11). It has been demonstrated that, for NaCl stress in particular, Ca 2+ influx first appears in roots and later in shoots (9), and when roots are stimulated with salt stress, the Ca 2+ signal propagates to the leaves in waves (12,13). The root-to-shoot propagation requires the slow vacuolar (SV) channel two-pore calcium channel protein 1 (TPC1), proposed to mediate a Ca 2+ -induced Ca 2+ release mechanism (12).…”

“…It has been demonstrated that, for NaCl stress in particular, Ca 2+ influx first appears in roots and later in shoots (9), and when roots are stimulated with salt stress, the Ca 2+ signal propagates to the leaves in waves (12,13). The root-to-shoot propagation requires the slow vacuolar (SV) channel two-pore calcium channel protein 1 (TPC1), proposed to mediate a Ca 2+ -induced Ca 2+ release mechanism (12). However, TPC1 is not required for the rapid osmotic-induced Ca 2+ response (12).…”

“…The root-to-shoot propagation requires the slow vacuolar (SV) channel two-pore calcium channel protein 1 (TPC1), proposed to mediate a Ca 2+ -induced Ca 2+ release mechanism (12). However, TPC1 is not required for the rapid osmotic-induced Ca 2+ response (12). On a longer time scale, Ca 2+ oscillations have been observed within individual cells (14).…”