A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context

Development. 2020 Mar 30;147(6):dev185710. doi: 10.1242/dev.185710.

Abstract

Aerial organs of plants, being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaves and stems to study the reunion between mechanically disconnected tissues. We show that PLETHORA (PLT) and AINTEGUMENTA (ANT) genes, which encode stem cell-promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. PLT proteins and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed-forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT-mediated regeneration response, leaf ground tissue cells can neither acquire the early vascular identity marker ATHB8, nor properly polarise auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaves. We reveal the mechanisms of vascular regeneration in plants and distinguish between the wound-repair ability of the tissue and its formation during normal development.

Keywords: Arabidopsis; Auxin; CUC2; PIN1; PLT; Vascular regeneration; Wound repair.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Arabidopsis Proteins / physiology
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Gene Expression Regulation, Plant
  • Gene Regulatory Networks / physiology*
  • Indoleacetic Acids / metabolism
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Mixed Function Oxygenases / genetics
  • Mixed Function Oxygenases / metabolism
  • Plant Development / physiology
  • Plant Leaves / genetics
  • Plant Leaves / growth & development
  • Plant Leaves / physiology*
  • Plant Stems / genetics
  • Plant Stems / growth & development
  • Plant Stems / physiology*
  • Plant Vascular Bundle / genetics
  • Plant Vascular Bundle / physiology*
  • Plants, Genetically Modified
  • Promoter Regions, Genetic
  • Regeneration / genetics*
  • Signal Transduction / genetics
  • Transcription Factors / physiology
  • Wound Healing / genetics

Substances

  • AINTEGUMENTA protein, Arabidopsis
  • Arabidopsis Proteins
  • CUC2 protein, Arabidopsis
  • Indoleacetic Acids
  • Intercellular Signaling Peptides and Proteins
  • Transcription Factors
  • Mixed Function Oxygenases
  • YUCCA4 protein, Arabidopsis