Fungal-induced abscission in trees: endophytic Lasiodiplodia chronic colonization and mango interaction demonstrate a conserved mechanism of induced fruit abscission

Abstract

Abscission is a fundamental developmental process in plants that can also be integrated into a defense strategy to restrict pathogen spread by shedding colonized organs. Members of Botryosphaeriaceae represent a major threat to global agriculture. These hemibiotrophic fungal pathogens colonize the vascular tissues of woody plants as endophytes, eliciting no visual symptoms. Under stress conditions, they switch to a necrotrophic lifestyle, causing destructive diseases such as stem dieback and fruit stem-end rot. Despite their economic significance, the role of the earliest, endophytic chronic colonization in triggering premature fruit drop, or abscission, remains largely unexplored. In this study, we uncover a previously overlooked phenomenon where Lasiodiplodia theobromae endophytically colonizes mango (Mangifera indica) flowers and fruitlets at the abscission zone (AZ), triggering premature abscission through activation of host ethylene-dependent defense responses. This causes the colonized fruitlets to drop prematurely, reducing the overall fruit yield. The presence of fungi initiates a cascade of events at the AZ, reprogramming the AZ cells through oxidative bursts and ethylene biosynthesis. Thereafter, the fungal secretion of ammonia leads to local cytoplasmic alkalization, ultimately accelerating callose deposition, accompanied by a depletion of auxin and cytokinin fluxes, and drives premature fruit detachment. The results elucidate two previously uncharacterized facets of the Botryosphaeriaceae endophytic/chronic colonization stage. We demonstrate that host damage and yield loss initiate before the necrotrophic transition and characterize a novel systemic defense response wherein the tree prematurely drops colonized fruits to limit pathogenic fungi colonization.