The Ca 2+ Channel CNGC19 Regulates Arabidopsis Defense Against Spodoptera Herbivory

Plant Cell. 2019 Jul;31(7):1539-1562. doi: 10.1105/tpc.19.00057. Epub 2019 May 10.

Abstract

Cellular calcium elevation is an important signal used by plants for recognition and signaling of environmental stress. Perception of the generalist insect, Spodoptera litura, by Arabidopsis (Arabidopsis thaliana) activates cytosolic Ca2+ elevation, which triggers downstream defense. However, not all the Ca2+ channels generating the signal have been identified, nor are their modes of action known. We report on a rapidly activated, leaf vasculature- and plasma membrane-localized, CYCLIC NUCLEOTIDE GATED CHANNEL19 (CNGC19), which activates herbivory-induced Ca2+ flux and plant defense. Loss of CNGC19 function results in decreased herbivory defense. The cngc19 mutant shows aberrant and attenuated intravascular Ca2+ fluxes. CNGC19 is a Ca2+-permeable channel, as hyperpolarization of CNGC19-expressing Xenopus oocytes in the presence of both cyclic adenosine monophosphate and Ca2+ results in Ca2+ influx. Breakdown of Ca2+-based defense in cngc19 mutants leads to a decrease in herbivory-induced jasmonoyl-l-isoleucine biosynthesis and expression of JA responsive genes. The cngc19 mutants are deficient in aliphatic glucosinolate accumulation and hyperaccumulate its precursor, methionine. CNGC19 modulates aliphatic glucosinolate biosynthesis in tandem with BRANCHED-CHAIN AMINO ACID TRANSAMINASE4, which is involved in the chain elongation pathway of Met-derived glucosinolates. Furthermore, CNGC19 interacts with herbivory-induced CALMODULIN2 in planta. Together, our work reveals a key mechanistic role for the Ca2+ channel CNGC19 in the recognition of herbivory and the activation of defense signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis / parasitology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Calcium / metabolism
  • Calcium Channels / genetics
  • Calcium Channels / metabolism*
  • Calcium Signaling / drug effects
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Membrane Permeability / drug effects
  • Cyclic Nucleotide-Gated Cation Channels / genetics
  • Cyclic Nucleotide-Gated Cation Channels / metabolism*
  • Cyclopentanes / pharmacology
  • Cytosol / drug effects
  • Cytosol / metabolism
  • Down-Regulation / drug effects
  • Gene Expression Regulation, Plant / drug effects
  • Glucosinolates / metabolism
  • Herbivory / drug effects
  • Herbivory / physiology*
  • Methionine / metabolism
  • Models, Biological
  • Mutation / genetics
  • Oxylipins / pharmacology
  • Plant Leaves / drug effects
  • Plant Leaves / parasitology
  • Plant Vascular Bundle / drug effects
  • Plant Vascular Bundle / genetics
  • Protein Binding / drug effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction / drug effects
  • Spodoptera / drug effects
  • Spodoptera / physiology*
  • Xenopus

Substances

  • Arabidopsis Proteins
  • At3g17690 protein, Arabidopsis
  • Calcium Channels
  • Cyclic Nucleotide-Gated Cation Channels
  • Cyclopentanes
  • Glucosinolates
  • Oxylipins
  • RNA, Messenger
  • jasmonic acid
  • Methionine
  • Calcium