Cotton leafroll dwarf virus infection and host range manipulates its vector (Aphis gossypii) behavior and gene expression

Cotton leafroll dwarf virus (CLRDV) is a serious pathogen in cotton production and is transmitted by the cotton/melon aphid, Aphis gossypii, in a persistent, circulative, and non-propagative manner. CLRDV was first reported in the United States in Alabama in 2017, and thereafter in several cotton-producing states. The host range and virus-vector-host interaction of CLRDV is not clear. Among the fourteen plant species in the landscape, including crops, weeds, and ornamentals tested as potential alternate hosts of CLRDV via aphid-mediated transmission assays, prickly sida, hibiscus, and okra were identified as the alternate hosts of CLRDV. The host virus-infection and acquisition of virus by aphids causes direct and indirect effects to aphids. These effects are associated with the differential expression of vector genes. The RNA-seq analysis of aphids feeding on CLRDV-infected and non-infected cotton, hibiscus, okra, and prickly sida plants was conducted to identify differentially expressed genes (DEGs) upon virus acquisition. The number of uniquely identified DEGs were associated with the biological processes classified as: response to stimulus, developmental process, immune system process, and reproduction. The one-way emigration, two-way settling, and biological fitness assays confirmed RNA-seq results and found that both the viruliferous and non-viruliferous aphids preferred non-infected cotton and hibiscus plants compared to CLRDV-infected plants with higher total fecundity on non-infected plants compared to CLRDV-infected ones. Overall, this study demonstrated that plant hosts in the agricultural landscape can serve as CLRDV inoculum sources and manipulates aphid behavior and could possibly play a role in the reoccurring epidemics of CLRDV.