Melatonin alleviates apple replant disease by regulating the endophytic microbiome of roots and phloridzin accumulation.

Melatonin administration is an environmentally effective strategy to mitigate apple replant disease (ARD), but its mechanism of action is unknown. This study investigated the protective effect of melatonin on ARD and the underlying mechanism. In field experiments, melatonin significantly reduced phloridzin levels in apple roots and rhizosphere soil. A correlation analysis indicated that a potential antagonistic interaction between melatonin and phloridzin was crucial for improving soil physicochemical properties, increasing the diversity of endophytic bacterial communities in roots of apple seedlings, and promoting mineral element absorption by the plants. Melatonin also reduced the abundance of Fusarium in roots. The ability of melatonin to reduce phloridzin levels both in soil and in plants was also demonstrated in a pot experiment. Azovibrio were specifically recruited in response to melatonin and their abundance was negatively correlated with phloridzin levels. Fusarium species that have a negative impact on plant growth were also inhibited by melatonin. Our results show that melatonin improves the rhizosphere environment as well as the structure of the endophytic microbiota community, by reducing phloridzin levels in rhizosphere soil and roots. These regulatory effects of melatonin support its use to improve the physiological state of plants under ARD conditions and thereby overcome the barriers of perennial cropping systems.