Intracellular Mn mobility and differential response to H2O2 accumulation explain the susceptibility of litchi cultivars to dark pericarp disease

Dark pericarp disease (DPD) in litchi is a physiological disease caused by excess manganese (Mn) in pericarp, impacting fruit appearance and marketability and leading to substantial economic loss. The susceptibility of litchi varieties to DPD differs greatly, but the underlying mechanisms remain vague. In this study, we investigated the discrepancies in physiological and biochemical processes in pericarp of two varieties (Feizixiao and Heiye) resistant to DPD and a susceptible cultivar (Guiwei) during fruit development from the same orchard. Pericarp Mn in Guiwei was significantly lower than that in Feizixiao and slightly higher than that in Heiye through fruit growth. Under Mn stress, Feizixiao and Heiye maintained ROS homeostasis, whereas substantial H 2 O 2 accumulated in Guiwei. Reduced anthocyanins and soluble sugars and increased lignin were observed in diseased Guiwei compared to Feizixiao and Heiye. The expression of genes encoding Mn transporters, light-harvesting antenna complex, ROS scavenging proteins and enzymes involved in anthocyanin synthesis was downregulated, whereas that of genes functioning in H 2 O 2 production and lignin synthesis was upregulated in Guiwei, and that of genes involved in glucose metabolism was altered, suggesting that Mn was poorly transported and sequestrated within Guiwei pericarp cells, and excess Mn boosted H 2 O 2 overproduction. The inhibited anthocyanin synthesis, enhanced lignin accumulation and tuned sugar metabolism conferred Guiwei adaptability to Mn stress. Conclusively, the poor Mn intracellular transferability and variations in response to H 2 O 2 accumulation associated with disturbed photosynthetic energy deliver under excess Mn, are collaboratively responsible for the cultivar-dependent DPD vulnerability in litchi.