Zucchini yellow mosaic virus-induced hypersensitive response is associated with pathogenesis-related 1 protein expression and confers resistance in watermelon.

Key message: The pathogenesis-related 1 gene of watermelon responds to the infection of ZYMV and contributes to the resistance of its host. Zucchini yellow mosaic virus (ZYMV; family Potyviridae) is a single-stranded positive-sense RNA virus that is a serious threat to cucurbits. Previously, we observed a hypersensitivity response (HR) in the systemic leaves of the 938-16-B watermelon line infected with ZYMV, distinct from the typical HR at infected sites. In this study, we confirmed that ZYMV accumulation in 938-16-B was significantly lower than in the susceptible line H1. Upon inoculation, the entry of ZYMV-eGFP into mesophyll cells is restricted into necrotic spots in leaves, indicating that resistance to ZYMV in 938-16-B is linked to the HR. Further, grafting experiments between 938-16-B and susceptible varieties were performed, and revealed an HR induction in susceptible varieties, suggesting the transfer of resistance signal(s) from 938-16-B to susceptible varieties. Through RNA-sequencing and proteomics analyses of the H1 scions on 938-16-B rootstock, a pathogenesis-related 1 (ClPR1) gene was identified. Specifically, ClPR1 expression is unique to ZYMV-infected 938-16-B. Repression of the expression of ClPR1 prevents an HR in 938-16-B. Conversely, overexpression of ClPR1 in susceptible varieties significantly reduces ZYMV accumulation, but an HR was not induced in susceptible line. Besides the virus, jasmonic acid (JA) can also trigger an HR in 938-16-B. Intriguingly, the expression of ClPR1 (Cla97C02G034020) is induced in both of 938-16-B and H1 by MeJA, rather than salicylic acid. These results suggest that HR is associated with the expression of ClPR1 and contributes to resistance to ZYMV in 938-16-B.