Abstract: 【Aim】 This study aims to explore the effects of cucumber mosaic virus (CMV) infection on the aphid resistance of watermelon plants, with a focus on the roles of leaf epidermal resistance, mesophyll tissue resistance, and phloem resistance in regulating CMV-melon aphid (Aphis gossypii) interactions. 【Methods】 The differences in leaf epidermal resistance, such as the density of trichomes, wax content and stomatal number of the CMV-infected (CMV+) and CMV-non-infected (CMV-) watermelon plants were observed with microscope. The differences in the salicylic acid (SA) content, callose content, callose synthase activity and relative expression levels of phenylalanine ammonia-lyase gene ClPAL, pathogenesis-related protein gene ClPR, and callose synthase gene ClCalS7 in the leaves of CMV+ and CMV- watermelon plants were analyzed by high-performance liquid chromatography (HPLC), biochemical method, fluorescence spectrophotometry and real-time fluorescence quantitative PCR, respectively. Furthermore, the impact of CMV infection on the aphid fitness was determined by comparing the numbers of A. gossypii on the CMV+ and CMV- watermelon plants and analyzing their feeding behaviors via electrical penetration graph (EPG) in the laboratory. 【Results】 There were no significant differences in the leaf epidermal structural traits of CMV+ and CMV－ watermelon plants, including wax content in leaves, trichome number per mm² on the abaxial leaf surface and stomatal number per mm² on the abaxial leaf surface. However, CMV infection activated the SA pathway of watermelon plants, causing a 1.09-fold increase in SA content and a 4.77-fold up-regulation of the expression level of ClPR in watermelon leaves. CMV infection also increased the callose content in watermelon leaves by 2.51-fold and callose synthase activity by 3.07-fold, and significantly upregulated the expression level of ClCalS7 by 3.19-fold, respectively. Further experiments showed that CMV infection significantly reduced the number of A. gossypii by 46.14% and shortened the total duration of phloem feeding by 38.78%, while increased the number of potential drop (pd) waveform events by 54.30% and prolonged the total duration of saliva secretion by 31.48%. 【Conclusion】 Taken together, we speculated that CMV infection inhibited the feeding and population growth of A. gossypii by activating the SA signaling pathway and enhancing the callose deposition of watermelon plants, rather than altering the leaf epidermal structural traits. These findings revealed the key resistance pathways in regulating CMV-watermelon plant-melon aphid interactions, providing a scientific basis for understanding their co-evolutionary mechanisms and developing integrated management strategies against CMV and aphids.

Key words: Aphis gossypii, Cucumber mosaic virus, aphid fitness, leaf epidermal resistance, SA-dependent resistance, callose deposition