Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots

Proc Natl Acad Sci U S A. 2020 Jun 30;117(26):15322-15331. doi: 10.1073/pnas.2003346117. Epub 2020 Jun 15.

Abstract

Wound healing in plant tissues, consisting of rigid cell wall-encapsulated cells, represents a considerable challenge and occurs through largely unknown mechanisms distinct from those in animals. Owing to their inability to migrate, plant cells rely on targeted cell division and expansion to regenerate wounds. Strict coordination of these wound-induced responses is essential to ensure efficient, spatially restricted wound healing. Single-cell tracking by live imaging allowed us to gain mechanistic insight into the wound perception and coordination of wound responses after laser-based wounding in Arabidopsis root. We revealed a crucial contribution of the collapse of damaged cells in wound perception and detected an auxin increase specific to cells immediately adjacent to the wound. This localized auxin increase balances wound-induced cell expansion and restorative division rates in a dose-dependent manner, leading to tumorous overproliferation when the canonical TIR1 auxin signaling is disrupted. Auxin and wound-induced turgor pressure changes together also spatially define the activation of key components of regeneration, such as the transcription regulator ERF115. Our observations suggest that the wound signaling involves the sensing of collapse of damaged cells and a local auxin signaling activation to coordinate the downstream transcriptional responses in the immediate wound vicinity.

Keywords: ERF115; auxin; cell division; cell expansion; regeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Division
  • Gene Expression Regulation, Plant / drug effects
  • Indoleacetic Acids / antagonists & inhibitors
  • Indoleacetic Acids / metabolism*
  • Kynurenine / pharmacology
  • Lasers
  • Phthalimides / pharmacology
  • Plant Cells / drug effects
  • Plant Cells / physiology*
  • Plant Roots / physiology*
  • Regeneration / drug effects
  • Regeneration / physiology
  • Signal Transduction / physiology
  • Triazoles / pharmacology

Substances

  • 5-(4-chlorophenyl)-4H-1,2,4-triazole-3-thiol
  • Arabidopsis Proteins
  • Indoleacetic Acids
  • Phthalimides
  • Triazoles
  • alpha-naphthylphthalamic acid
  • Kynurenine