For many crop pathogens including viruses, high genetic variation provides them with potential to adapt to and prevail in a changing environment. Understanding genetic variation in viruses and their significance is a key to elaborate virus epidemiology and evolution. While genetic variation of plant viruses has been documented to impact virus–host interactions, how it affects virus–insect vector interactions remains elusive. Here, we report the impact of mutations in the coat protein of squash leaf curl China virus (SLCCNV), a begomovirus, on the interaction between the virus and its whitefly vectors. We characterized mutations in the coat protein of SLCCNV and found that some residues exhibited higher mutation frequency than the others. We assayed the impact of mutation on infectivity using agroinoculation and found these mutations marginally affect virus infectivity. We further analyze their functions using virus acquisition and transmission trials and found some of mutations resulted in altered transmission of SLCCNV by different species of the whitefly Bemisia tabaci complex. We then identified the key amino acid residue(s) involved by constructing several mutant viruses and found that a single-residue mutation in the coat protein of SLCCNV was sufficient to significantly alter the whitefly transmission characteristics of SLCCNV. We examined the competition between different genotypes of SLCCNV in plant infection and whitefly transmission. We found that mutations in the coat protein did not alter the fitness of SLCCNV in plants, but they rendered the virus more competitive in transmission by certain species of whiteflies. Our findings indicate that mutations in the coat protein may play a key role in both the adaptation of begomoviruses to the changing vector populations and the evolution of begomoviruses.
Recombination is common in plant viruses such as geminiviruses, but the ecological and pathogenic consequences have been explored only in a few cases. Here, we found that a new begomovirus, tomato yellow leaf curl Shuangbai virus (TYLCSbV), probably originated from the recombination of Ageratum yellow vein China virus (AYVCNV) and tobacco curl shoot virus (TbCSV). Agrobacterium‐mediated inoculation showed that TYLCSbV and AYVCNV have similar levels of infectivity on tomato and tobacco plants. However, the two viruses exhibit contrasting specificities for vector transmission, that is, TYLCSbV was efficiently transmitted by the whitefly Bemisia tabaci Mediterranean (MED) rather than by the whitefly B. tabaci Middle East‐Asia Minor 1 (MEAM1), whereas AYVCNV was more efficiently transmitted by MEAM1. We also showed that the transmission efficiencies of TYLCSbV and AYVCNV are positively correlated with the accumulation of the viruses in whitefly whole bodies and organs/tissues. The key coat protein amino acids that determine their accumulation are between positions 147 and 256. Moreover, field surveys suggest that MED has displaced MEAM1 in some regions where TYLCSbV was collected. Viral competition assays indicated that TYLCSbV outcompeted AYVCNV when transmitted by MED, while the outcome was the opposite when transmitted by MEAM1. Our findings suggest that recombination has resulted in a shift of vector specificity that could provide TYLCSbV with a potential selective transmission advantage, and the population shift of whitefly cryptic species could have influenced virus evolution towards an extended trajectory of transmission.
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