Comprehensive proteomic profiling of Cucumber mosaic virus infection: identifying key proteins and pathways involved in resistance and susceptibility in melon

Abstract Background Melon (Cucumis melo L.) is the model species of the Cucurbitaceae family and an important crop. However, its yield is primarily affected by viruses. Cucumber mosaic virus (CMV) is particularly significant due to its broad host range, capable of infecting over 100 plant families. Resistance to CMV in the melon accession Songwhan Charmi (SC) is controlled by the recessive gene cmv1, which encodes the Vacuolar Protein Sorting 41, involved in vesicle transport to the vacuole. cmv1 restricts the virus to the bundle sheath cells and impedes viral access to the phloem, preventing a systemic infection. This phenotype depends on the viral movement protein (MP). However, little is known about the broader cellular changes that CMV triggers in melon or the specific biological responses that facilitate or restrict the virus entry into the phloem in susceptible and resistant varieties. Result We profiled the proteomes of CMV-resistant or susceptible melon genotypes inoculated with CMV-LS or FNY strains. Analysis of co-abundance networks revealed the rewiring of central biological pathways during different stages of CMV infection. Upon inoculation, resistant varieties do not trigger any signalling event to the new leaves. Local infection triggers a general depletion in proteins related to translation, photosynthesis and intracellular transport, whereas only in resistant varieties CMV triggers an increase in lipid modification and phloem proteins. During the systemic infection of susceptible melon plants, there is a strong increase in proteins associated with stress responses, such as those involved in the ER-associated degradation (ERAD) and phenylpropanoid pathways, along with a decrease in translation and photosynthesis. Key hub proteins have been identified in these processes. Conclusions This study is the first comprehensive high-throughput proteomic analysis of CMV-infected melon plants, providing a novel and detailed understanding of the proteomic changes associated with CMV infection, highlighting the differential responses between resistant and susceptible genotypes and identifying key proteins that could be potential targets for future research and CMV management strategies.