Reactive oxygen species in signalling the transcriptional activation of WIPK expression in tobacco

Plant Cell Environ. 2014 Jul;37(7):1614-25. doi: 10.1111/pce.12271. Epub 2014 Feb 13.

Abstract

Plant mitogen-activated protein kinases represented by tobacco WIPK (wounding-induced protein kinase) and its orthologs in other species are unique in their regulation at transcriptional level in response to stress and pathogen infection. We previously demonstrated that transcriptional activation of WIPK is essential for induced WIPK activity, and activation of salicylic acid-induced protein kinase (SIPK) by the constitutively active NtMEK2(DD) is sufficient to induce WIPK gene expression. Here, we report that the effect of SIPK on WIPK gene expression is mediated by reactive oxygen species (ROS). Using a combination of pharmacological and gain-of-function transgenic approaches, we studied the relationship among SIPK activation, WIPK gene activation in response to fungal cryptogein, light-dependent ROS generation in chloroplasts, and ROS generated via NADPH oxidase. In the conditional gain-of-function GVG-NtMEK2(DD) transgenic tobacco, induction of WIPK expression is dependent on the ROS generation in chloroplasts. Consistently, methyl viologen, an inducer of ROS generation in chloroplasts, highly activated WIPK expression. In addition to chloroplast-originated ROS, H(2)O(2) generated from the cell-surface NADPH oxidase could also activate WIPK gene expression, and inhibition of cryptogein-induced ROS generation also abolished WIPK gene activation. Our data demonstrate that WIPK gene activation is mediated by ROS, which provides a mechanism by which ROS influence cellular signalling processes in plant stress/defence response.

Keywords: MAPK; NADPH oxidase; ROS; WIPK gene activation; chloroplast; elicitin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chloroplasts / drug effects
  • Chloroplasts / metabolism
  • Dexamethasone / pharmacology
  • Enzyme Activation / drug effects
  • Gene Expression Regulation, Plant* / drug effects
  • Gene Expression Regulation, Plant* / radiation effects
  • Hydrogen Peroxide / pharmacology
  • Light
  • Mitogen-Activated Protein Kinases / genetics*
  • Mitogen-Activated Protein Kinases / metabolism
  • Models, Biological
  • Nicotiana / drug effects
  • Nicotiana / enzymology*
  • Nicotiana / genetics*
  • Nicotiana / radiation effects
  • Photosynthesis / drug effects
  • Photosynthesis / radiation effects
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Proteins / pharmacology
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Signal Transduction / radiation effects
  • Transcriptional Activation / drug effects
  • Transcriptional Activation / genetics*
  • Transcriptional Activation / radiation effects

Substances

  • Plant Proteins
  • Proteins
  • Reactive Oxygen Species
  • elicitin, Phytophthora
  • Dexamethasone
  • Hydrogen Peroxide
  • Mitogen-Activated Protein Kinases
  • SA-induced protein kinase
  • WIPK protein, Nicotiana tabacum