High temperature perception in leaves promotes vascular regeneration and graft formation in distant tissues

Development. 2022 Mar 1;149(5):dev200079. doi: 10.1242/dev.200079. Epub 2022 Feb 28.

Abstract

Cellular regeneration in response to wounding is fundamental to maintain tissue integrity. Various internal factors including hormones and transcription factors mediate healing, but little is known about the role of external factors. To understand how the environment affects regeneration, we investigated the effects of temperature upon the horticulturally relevant process of plant grafting. We found that elevated temperatures accelerated vascular regeneration in Arabidopsis thaliana and tomato grafts. Leaves were crucial for this effect, as blocking auxin transport or mutating PHYTOCHROME INTERACTING FACTOR 4 (PIF4) or YUCCA2/5/8/9 in the cotyledons abolished the temperature enhancement. However, these perturbations did not affect grafting at ambient temperatures, and temperature enhancement of callus formation and tissue adhesion did not require PIF4, suggesting leaf-derived auxin specifically enhanced vascular regeneration in response to elevated temperatures. We also found that elevated temperatures accelerated the formation of inter-plant vascular connections between the parasitic plant Phtheirospermum japonicum and host Arabidopsis, and this effect required shoot-derived auxin from the parasite. Taken together, our results identify a pathway whereby local temperature perception mediates long distance auxin signaling to modify regeneration, grafting and parasitism. This article has an associated 'The people behind the papers' interview.

Keywords: Arabidopsis thaliana; Auxin transport; Grafting; Parasitic plants; Regeneration; Temperature sensing; Vascular biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Biological Transport / genetics
  • Cotyledon / genetics
  • Cotyledon / metabolism
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism
  • Gene Expression Regulation, Plant
  • Hot Temperature*
  • Hypocotyl / metabolism
  • Indoleacetic Acids / metabolism
  • Mixed Function Oxygenases / genetics
  • Mixed Function Oxygenases / metabolism
  • Plant Leaves / genetics*
  • Plant Leaves / metabolism*
  • Plants, Genetically Modified
  • Regeneration / genetics*
  • Signal Transduction / genetics*
  • Solanum lycopersicum / physiology

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • Indoleacetic Acids
  • PIF4 protein, Arabidopsis
  • Cytochrome P-450 Enzyme System
  • Mixed Function Oxygenases