Geminiviruses and their satellites: genomic diversity, evolutionary insights, and emerging models

Abstract

Geminiviruses infect a wide range of economically important crops, including tomato, cassava, cotton, common bean, and maize, and are characterized by twinned icosahedral particles containing circular single-stranded DNA (ssDNA) genomes. Their genomes have undergone extensive diversification through mutation, recombination and association with satellite molecules. Depending on the genus, geminiviruses are transmitted by hemipteran vectors, including whiteflies, leafhoppers, aphids, and treehoppers, and replicate in plant cell nuclei using host replication machinery, which complicates disease management. Recent taxonomic updates by the International Committee on Taxonomy of Viruses (ICTV) in MSL41 recognize 549 species distributed across 15 genera, with Begomovirus accounting for most of the documented species diversity and Mastrevirus representing the second-largest genus. Analysis of documented records across eight geographic regions revealed the highest documented geminivirus species richness in the Indian subcontinent. Current evidence indicates that geminivirus diversification is shaped by multiple interacting evolutionary mechanisms, with recombination and modular genetic exchange contributing substantially to the formation of mosaic genomes, while host compatibility and vector ecology impose important ecological and functional constraints on their persistence and diversification. The discovery of previously unrecognized geminivirus lineages, endogenous geminivirus-related sequences, and additional genomic diversity through high-throughput sequencing indicates that the currently recognized diversity of geminiviruses remains incomplete. The evolutionary origin of geminiviruses remains partly unresolved because replication-associated and capsid-associated components show distinct evolutionary histories. Based on comparative genomic, phylogenetic, and recombination evidence, we propose a modular evolutionary model in which replication-associated and capsid-associated components followed distinct evolutionary trajectories, followed by genome-level assembly and diversification associated with the emergence of bipartite genome organization. Overall, the emerging view is that geminiviruses represent genetically and ecologically dynamic lineages shaped by interacting evolutionary processes rather than a single evolutionary trajectory. Broader sampling of hosts and vectors, comparative genomics and functional validation will be essential for resolving their origin and evolutionary relationships.