Comparative transcriptome analysis of resistant and susceptible watermelon genotypes reveals the role of RNAi, callose, proteinase, and cell wall in squash vein yellowing virus resistance

Watermelon (Citrullus lanatus) is the third largest fruit crop in the world in term of production. However, it is susceptible to several viruses. Watermelon vine decline (WVD), caused by whitefly-transmitted squash vein yellowing virus (SqVYV), is a disease that has caused over $60 million in losses in the US and continues to occur regularly in southeastern states. Understanding the molecular mechanisms underlying resistance to SqVYV is important for effective disease management. A time-course transcriptomic analysis was conducted on resistant (392291-VDR) and susceptible (Crimson Sweet) watermelon genotypes inoculated with SqVYV. Significantly higher levels of SqVYV were observed over time in the susceptible compared to the resistant genotype. The plasmodesmata callose binding protein (PDCB) gene, which is responsible for increased callose deposition in the plasmodesmata, was more highly expressed in the resistant genotype than in the susceptible genotype before and after inoculation, suggesting the inhibition of cell-to-cell movement of SqVYV. The potential role of the RNA interference (RNAi) pathway was observed in the resistant genotype based on differential expression of eukaryotic initiation factor (eIF), translin, DICER, ribosome inactivating proteins, RNA-dependent RNA polymerase (RDR), and Argonaute (AGO) genes after inoculation. The significant differential expression of hormone-related genes, including those involved in the ethylene, jasmonic acid, auxin, cytokinin, gibberellin, and salicylic acid signaling pathways, was observed, emphasizing their regulatory roles in the defense response. Genes regulating pectin metabolism, cellulose synthesis, cell growth and development, xenobiotic metabolism, and lignin biosynthesis were overexpressed in the susceptible genotype, suggesting that alterations in cell wall integrity and growth processes result in disease symptom development. These findings will be helpful for further functional studies and the development of SqVYV-resistant watermelon cultivars.