Autophagy, an evolutionarily conserved process for cellular component degradation and recycling, occurs in yeasts, animals, and plants under both stress and normal conditions. However, the functions of autophagy-related genes (ATGs) in watermelon (Citrullus lanatus) remain uncharacterized. In this study, a phylogenetic analysis identified 27 ATGs belonging to 16 subfamilies in the watermelon genome. A promoter analysis revealed that all the ClaATGs contain multiple photo-responsive elements. Tissue-specific expression profiling showed diverse expression patterns of ClaATGs across different tissues, except for the constitutively expressed ClaATG6. Exogenous independent treatments with glucose, naphthalene acetic acid, and 6-benzylaminopurine induced the expression of most ClaATGs, particularly members of the ClaATG8 subfamily, in the graft unions of normal and etiolated seedlings. A sugar application significantly increased autophagosome numbers during the early stages of graft interface healing, accompanied by the upregulation of ClaATG6, ClaATG8b, ClaATG8i, and ClaTOR, as well as the downregulation of ClaSnRK1. These findings elucidate the roles of ATGs in watermelon graft union formation and provide novel insights into the complex functions of autophagy in plant development and stress responses.

Powdery mildew (PM) is a major fungal disease in cucumber (Cucumis sativus L.) cultivation. Grafting serves as an important agricultural practice for improving disease resistance and stress tolerance in scions. This study aimed to determine the effects of different pumpkin rootstocks on PM resistance in grafted cucumber plants. Susceptible ‘Xintai Mici’ cucumber scions were grafted onto 10 different pumpkin rootstock varieties, with self-grafted plants serving as the experimental control. Grafting significantly promoted plant biomass accumulation compared to the self-grafted control, and this enhancement was positively correlated with the rootstock’s root system size. However, grafted plant growth was still negatively affected by PM infection. Among the 10 rootstocks, seedlings grafted onto rootstock GP8 exhibited the lowest disease index, the slowest spore development, and the strongest PM resistance. While some resistant pumpkin rootstocks failed to confer significant PM resistance to their grafted cucumber scions, rootstock GP8 provided consistent PM resistance to its grafted plants. Furthermore, cucumber grafted onto rootstock GP8 showed a significantly enhanced net photosynthetic rate and increased antioxidant enzyme activities (superoxide dismutase, ascorbate peroxidase, and glutathione reductase). Concurrently, these plants accumulated lower levels of superoxide anions and exhibited the smallest increases in malondialdehyde content among all the grafted combinations. Additionally, during PM infection, the expression levels of salicylic acid biosynthesis-related genes (CsICS1 and CsPAL) and downstream disease resistance genes (CsPR1, CsPR5, and CsNPR1) were significantly higher in scions grafted onto rootstock GP8 compared to self-grafted cucumbers. These results suggest that the enhanced PM resistance in grafted cucumber is significantly influenced by the rootstock, potentially through the regulation of photosynthetic performance, reactive oxygen species metabolism, and the expression of genes associated with the salicylic acid signaling pathway in the scion.