Water availability positions auxin response maxima to determine plant regeneration fates

Abstract Wounding and hormones serve as diverse triggers for regeneration in animals and plants. Despite important advances in understanding various types of regeneration, the mechanism by which plants determine regeneration outcomes remains largely unknown. Here we demonstrate in Arabidopsis that a trade-off between two regeneration fates, wound-induced callus and root regeneration, was driven by distinct molecular pathways related to cambium and root development, respectively. We discovered that local water availability near the wound site determined the early stages of regeneration fates in Arabidopsis and tomato, with high water triggering root fate and low water initiating callus fate. Distinct spatial distributions of auxin response maxima around the wound, shaped by water availability, were critical for determining root or callus fates. We found that, by perturbing auxin response or auxin transport dynamics, we could change regeneration outcomes. Moreover, high water availability enhanced ethylene and jasmonic acid responses, whereas treatments with these hormones could modify auxin transport dynamics or the location of auxin response maxima, thus influencing regeneration fates. We propose that, through stress hormones, water availability modifies the auxin response distribution to control regeneration outcomes, thus allowing environmental control of regeneration and providing a means to improve in vitro regeneration by changing the water potential.