Capsicum annuum TC48 shows both resistance and tolerance to cucumber mosaic virus and is a potential genetic resource for pepper improvement

Pepper ( Capsicum spp.) is a widely grown, economically important crop worldwide. Pepper production is threatened by various diseases, among which cucumber mosaic virus (CMV) is a most severe one. Despite intensive efforts, the CMV resistance in most commercial lines is insufficient. Here, we explored disease responses using Capsicum annuum TC48, which displays minimal disease symptoms during both vegetative and reproductive growth after CMV infection. CMV proliferation and systemic spread in TC48 were limited during early infection, despite the plants showing transcriptional repression of defense-associated genes and activation of photosynthesis- and growth-related genes. By contrast, the susceptible control ST-8 showed CMV proliferation accompanied by transcriptional activation of immune responses and suppression of photosynthesis. During late infection, however, the systemic movement and proliferation of CMV reached comparable levels between TC48 and ST-8, with defense responses transcriptionally activated and photosynthesis repressed in both varieties. Thus, TC48 exhibits bimodal dynamics between growth- and defense-related transcriptional programs that appear to underlie its differential outcome to CMV infection compared to ST-8. Small RNA sequencing (sRNA seq) suggested that 21- and 22-nt miRNAs might regulate these bimodal dynamics, while 24-nt siRNAs are likely dispensable. Bulk segregant analysis revealed several candidate genomic regions underlying CMV responses in TC48. We conclude that CMV damage in TC48 is likely mitigated through a combined strategy of partial resistance and tolerance, making TC48 a promising genetic resource for the production of pepper that can withstand CMV exposure.