Global phylodynamics of two relevant aphid-transmitted viruses in cucurbit crops: cucurbit aphid-borne yellows virus and watermelon mosaic virus

Abstract Cucurbit aphid-borne yellows virus (CABYV) and watermelon mosaic virus (WMV) are major plant pathogens that cause severe epidemics in cucurbit crops. While there has been an increasing interest in molecular epidemiological studies on both viruses at regional scales, their phylodynamic analysis by using the temporal data at global scale remains unexplored. In this study, we implemented the Nextstrain phylodynamic approach to comprehensively examine the coat protein gene and full-length genome sequences of the CABYV and WMV worldwide populations. Our analyses reconstructed a robust phylogeny of CABYV and confirmed the occurrence of isolates grouped into three clusters (Asian, Mediterranean, and Recombinant). Nextstrain analysis suggested that CABYV epidemics likely originated in Southeast Asia in fourteenth century, while the Mediterranean population emerged in Spain in seventeenth century. We also found a high divergence between Asian and Mediterranean isolates, with low genetic diversity and scarce evidence of selection, as reflected by the lack of gene flow. Moreover, the hierarchical analysis of molecular variance revealed a significant differentiation between CABYV populations grouped by geographical location and plant host. Additionally, the global phylogenetic reconstruction of the WMV population confirmed a clear differentiation among isolates, which grouped into two clusters (classical and emergent), and Nextstrain analysis suggested that WMV epidemics were most probably originated in USA during the sixteenth century. The initial WMV population diverged in the eighteenth century, with the origin of the emergent population in the nineteenth century. Our analysis confirmed that WMV population has a polyphyletic origin, defining an extensive genetic diversity. Overall, this work provides insights into the CABYV and WMV origin and evolutionary dynamics, gaining an understanding of the global spread of both viral diseases. Additionally, the integration of all spatio-temporal CABYV and WMV data, along with their genome sequence data by open access ( https://github.com/PiR92 ) and the Nextstrain approach, provides a valuable tool for compiling and sharing current knowledge of these viral diseases in cucurbit crops.