Evolution of ssDNA plant viruses in the natural environment - a journey through time

Begomoviruses pose a major threat to food security, particularly in developing countries. These small ssDNA viruses exhibit substitution rates comparable to those of RNA viruses. The temporal dynamics of begomoviruses in non-agricultural environments have been largely overlooked, and little is known about how these viruses evolve in the absence of anthropogenic influence. In this study, we investigated the temporal dynamics of begomoviruses in a small fragment of regenerating Atlantic Forest area in the state of Minas Gerais, Brazil. Samples of Sida acuta, a wild plant native from South America, were collected at the same location over a 12-year period (2011-2022). Five distinct begomoviruses were detected infecting this host: OxYVV, SiYLCV, SimMV, MaYVV, and SiMV. OxYVV and SimMV were subdivided into multiple variants, revealing their potential as reservoirs of viral biodiversity. Several shifts in species and variant composition were observed in the viral community over time, with the most drastic change occurring in 2016, when SiYLCV outnumbered OxYVV. The reasons behind this turnover remain uncertain, but the most compelling clues point to a population expansion of SiYLCV. We detected a strong temporal signal in two of the most abundant viruses (OxYVV and SiYLCV), which allowed us to calibrate molecular clocks and estimate substitution rates for both of them. Our results indicate that, even in the natural environment, begomoviruses can evolve at rates similar to those reported in agricultural systems.