High temperature perception in leaves promotes vascular regeneration in distant tissues

Abstract

Cellular regeneration in response to wounding is fundamental to maintain tissue integrity. Various internal factors including hormones and developmental pathways affect wound healing but little is known about how external factors influence regeneration. To better understand how the environment affects regeneration, we investigated the effects of temperature using the horticulturally relevant process of plant grafting. We found that elevated temperatures accelerated vascular regeneration of Arabidopsis thaliana and tomato (Solanum lycopersicum) grafts. Leaves were critical for this effect since blocking auxin transport or mutating PHYTOCHROME INTERACTING FACTOR4 (PIF4) or YUCCA2/5/8/9 in the cotyledons abolished the temperature enhancement. However, these perturbations had no effect upon graft healing at ambient temperatures and mutations in PIF4 did not affect the temperature enhancement of callus formation or tissue adhesion, suggesting that leaf-derived auxin was specific for enhancing vascular regeneration in response to elevated temperatures. Tissue-specific perturbations of auxin response using a BODENLOS (BDL) mutant revealed an asymmetric effect of temperature upon regeneration: the presence of bdl above the cut prevented temperature enhancement whereas the presence of bdl below the cut prevented graft healing regardless of temperature. Promotion of tissue regeneration by elevated temperatures was not specific for graft healing and we found that elevated temperatures accelerated xylem formation between the parasite Phtheirospermum japonicum and host Arabidopsis thaliana, and this effect required shoot-derived auxin from the parasite. Taken together, our results identify a pathway by which elevated temperatures accelerate vascular development which could be of relevance for improving regeneration and better understanding inter-plant vascular connections.