Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Proc Natl Acad Sci U S A. 2014 Apr 29;111(17):6497-502. doi: 10.1073/pnas.1319955111. Epub 2014 Mar 24.

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.

Keywords: Ca2+ signaling; Two Pore Channel 1; Yellow Cameleon.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / metabolism
  • Calcium / metabolism
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels
  • Calcium Signaling / drug effects*
  • Calcium Signaling / genetics
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism
  • Gene Expression Regulation, Plant / drug effects
  • Genes, Plant / genetics
  • Meristem / drug effects
  • Meristem / metabolism
  • Mutation / genetics
  • Plant Roots / drug effects
  • Plant Roots / metabolism*
  • Plant Shoots / drug effects
  • Plant Shoots / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Seedlings / drug effects
  • Seedlings / genetics
  • Sodium Chloride / pharmacology*
  • Stress, Physiological / drug effects*
  • Stress, Physiological / genetics
  • Vacuoles / drug effects
  • Vacuoles / metabolism

Substances

  • Arabidopsis Proteins
  • Calcium Channel Blockers
  • Calcium Channels
  • RNA, Messenger
  • TPC1 protein, Arabidopsis
  • Sodium Chloride
  • Calcium