Biology, epidemiology, and control of Ramularia spp., agents of dry lenticel rot on apples

Ramularia mali Videira & Crous, causal agent of dry lenticel rot, is an emerging postharvest pathogen affecting apple (Malus × domestica Borkh.) production in Italy, Austria, and France. Postharvest losses in affected lots are ranging from 10% to above 50%. With regional differences, most affected cultivars are Golden Delicious and Ambrosia, with increasing incidences in Bonita, Inored(cov)/Story®, CivM49(cov) / RedPop®, Inored, Gala, Granny Smith and Braeburn. The disease manifests only after 3 to 6 months of cold storage at 1 to 2°C combined with ultra-low oxygen conditions (0.5 to 2% O₂), by developing characteristic black-brown speckled lesions of 1 to 5 mm in diameter on the fruit peel without colonizing underlying tissue. Critically, infected fruits remain asymptomatic at harvest, making early detection and management strategies in the orchard difficult. Ramularia mali exhibits psychrotolerant and hypoxia-tolerant physiological traits, enabling slow but sustained growth under commercial storage conditions. The pathogen demonstrates selective enzymatic capabilities, preferentially degrading pectin in the apple cell wall while showing no capacity for starch utilization. Thus, indicating that post-harvest fruit senescence is a critical factor in disease progression. Comprehensive fungicide screening revealed that chemical control options are severely limited, with only the active substances metiram and prothioconazole achieving complete growth inhibition in vitro. Field trials demonstrated that even the most effective fungicides provided inconsistent control, highlighting the necessity for alternative and integrated management approaches. The ripening inhibitor 1-methylcyclopropene (1-MCP) showed significant disease mitigation potential, reducing disease incidence by up to 82-89% when applied post-harvest. However, the most promising results emerged from treatment combinations: the application of hot water treatment combined with 1-MCP demonstrated superior efficacy through ecological manipulation of the fruit surface microbiome. Metabarcoding analysis revealed that the HW + 1-MCP combination acts as a powerful ecological filter, fundamentally altering fungal community composition. While HW alone suppressed R. mali but paradoxically enabled opportunistic Mucor outbreaks and 1-MCP alone reduced symptoms but failed to prevent R. mali proliferation. The combination treatment reduced symptom development and secondary rot infection to zero. This correlated with stable dominance of yeast Cystobasidium species, where causality needs to be elucidated. These integrated findings establish a mechanistic foundation for sustainable postharvest management of R. mali through combined physical and physiological interventions rather than reliance on chemical synthetic fungicides.