Assessing the Impact on Virus Transmission and Insect Vector Behavior of a Viral Mixed Infection in Melon

Abstract

Mixed viral infections in plants are common, and can result in synergistic or antagonistic interactions. Except in complex diseases with severe symptoms, mixed infections frequently remain unnoticed, and their impact on insect vector transmission is largely unknown. In this study, we considered mixed infections of two unrelated viruses commonly found in melon plants, the crinivirus cucurbit yellow stunting disorder virus (CYSDV) and the potyvirus watermelon mosaic virus (WMV), and evaluated their vector transmission by whiteflies and aphids, respectively. Their dynamics of accumulation was analyzed until 60 days postinoculation (dpi) in mixed-infected plants, documenting reduced titers of WMV and much higher titers of CYSDV compared with single infections. At 24 dpi, corresponding to the peak of CYSDV accumulation, similar whitefly transmission rates were obtained when comparing either individual or mixed-infected plants as CYSDV sources, although its secondary dissemination was slightly biased toward plants previously infected with WMV, regardless of the source plant. However, at later time points, mixed-infected plants partially recovered from the initially severe symptoms, and CYSDV transmission became significantly higher. Interestingly, aphid transmission rates both at early and late time points were unaltered when WMV was acquired from mixed-infected plants despite its reduced accumulation. This lack of correlation between WMV accumulation and transmission could result from compensatory effects observed in the analysis of the aphid feeding behavior by electrical penetration graphs. Thus, our results showed that mixed-infected plants could provide advantages for both viruses, directly favoring CYSDV dissemination while maintaining WMV transmission.

The P1 Protein of Watermelon mosaic virus Compromises the Activity as RNA Silencing Suppressor of the P25 Protein of Cucurbit yellow stunting disorder virus

“…Despite the common occurrence of multiple viral infections in plants, in many cases our understanding of the interactions occurring when two or more unrelated viruses share the same plant is still incomplete (Moreno and López-Moya, 2020). As an example, our recent analysis of melon plants co-infected by WMV and CYSDV revealed a complex scenario, with dynamic changes along the progress of the infections, that could even affect the transmissibility of the viruses by their insect vectors: briefly, the initial synergism and boost of CYSDV accumulation was later moderated and accompanied by a sort of recovery phenotype (Domingo-Calap et al, 2020). Intrigued by this peculiar behavior, we have addressed if virus-virus interactions between WMV and CYSDV might help to explain the outcome of the mixed infection.…”

“…Interestingly, the dynamic of accumulation of tagged WMV P1 appeared to be altered in the co-agroinfiltrated samples, with a delayed peak compared with the individually expressed control. Unfortunately, the damage suffered after agroinfiltration precluded longer analysis, but it is tempting to speculate if these changes along this limited time might reflect somehow the peculiar dynamics mentioned to occur during mixed infections (Domingo-Calap et al, 2020).…”

“…CYSDV is a whitefly-transmitted crinivirus (Abrahamian and Abou-Jawdah, 2014;Wintermantel et al, 2017), and less widespread than WMV although lately it is becoming an emergent problem together with other whitefly-transmitted viruses (Navas-Castillo et al, 2011. We have already characterized the dynamic accumulation of these two partner viruses in melon and explored how that influences their vectormediated dissemination (Domingo-Calap et al, 2020), although many molecular details of their interaction remained unaddressed, such as those dealing with RNA silencing processes.…”

Specific and Spillover Effects on Vectors Following Infection of Two RNA Viruses in Pepper Plants

“…Virus–virus interactions following mixed infection in host plants range from antagonism to synergism [ 26 , 29 , 48 , 49 ]. In the current study, TSWV infection appeared to suppress CMV accumulation in mixed infected pepper plants.…”

“…In contrast, an antagonistic interaction is characterized by reduction in the titer of one or both viruses following mixed infection when compared with single virus infection [ 22 , 24 ]. The resultant phenotype following mixed virus infection can sometimes differentially influence the vector preference and/or fitness compared with single virus infection, thereby affecting the transmission of one or both viruses [ 20 , 22 , 26 , 27 , 28 , 29 ]. Very few studies have investigated mixed virus infection-modulated fitness benefits when two diverse vectors are involved [ 20 ].…”