Molecular phylogenetics and evolutionary analysis of a highly recombinant begomovirus, Cotton leaf curl Multan virus, and associated satellites

Cotton leaf curl Multan virus (CLCuMuV) and its associated satellites are a major part of the cotton leaf curl disease (CLCuD) caused by the begomovirus species complex. Despite the implementation of potential disease management strategies, the incessant resurgence of resistance-breaking variants of CLCuMuV imposes a continuous threat to cotton production. Here, we present a focused effort to map the geographical prevalence, genomic diversity, and molecular evolutionary endpoints that enhance disease complexity by facilitating the successful adaptation of CLCuMuV populations to the diversified ecosystems. Our results demonstrate that CLCuMuV populations are predominantly distributed in China, while the majority of alphasatellites and betasatellites exist in Pakistan. We demonstrate that together with frequent recombination, an uneven genetic variation mainly drives CLCuMuV and its satellite’s virulence and evolvability. However, the pattern and distribution of recombination breakpoints greatly vary among viral and satellite sequences. The CLCuMuV, Cotton leaf curl Multan alphasatellite, and Cotton leaf curl Multan betasatellite populations arising from distinct regions exhibit high mutation rates. Although evolutionarily linked, these populations are independently evolving under strong purifying selection. These findings will facilitate to comprehensively understand the standing genetic variability and evolutionary patterns existing among CLCuMuV populations across major cotton-producing regions of the world.