Virome analysis uncovers the tomato virosphere and a novel recombinant begomovirus-alphasatellite complex causing leaf curl disease in India.
TL;DR
A complex tomato virome associated with leaf curl disease in Tamil Nadu is revealed, driven by mixed viral infections and recombination and emphasizes the need for continued virome surveillance and integrated disease management in tomato production systems.
Abstract
Background
Begomoviruses are circular single-stranded DNA viruses transmitted by the whitefly Bemisia tabaci and are major causal agents of leaf curl disease in tomato (Solanum lycopersicum L.). The present study aimed to comprehensively characterize the virome associated with symptomatic tomato plants collected from major agro-ecological regions of Tamil Nadu, India, using high-throughput sequencing (HTS).
Results
HTS based virome analysis of tomato plants exhibiting severe leaf curl symptoms revealed a complex viral community. The virosphere includes multiple begomoviruses, namely tomato leaf curl New Delhi virus (ToLCNDV), tomato leaf curl Bangalore virus (ToLCBaV), tomato leaf curl Karnataka virus, and chilli leaf curl virus (ChiLCV), along with associated alpha- and betasatellites. In addition, RNA viruses including pepper virus A (PepVA), chilli veinal mottle virus (ChiVMoV), and tomato chlorosis virus (ToCV) were also identified, indicating frequent occurrence of mixed infections. Full-length or coding-complete genome sequences were recovered for most viral components, whereas partial contigs were obtained for Southern tomato virus (STV) and tobacco vein distorting virus (TVDV). Notably, a novel recombinant monopartite begomovirus, tentatively named tomato leaf curl Dindigul virus (ToLCDiV), showed < 89.82% nucleotide identity with known begomovirus sequences. In addition, a distinct alphasatellite, tomato leaf curl Madurai alphasatellite (ToLCMdA) showed 86.74% nucleotide identity with known alphasatellites, supporting its distinctiveness based on ICTV species demarcation criteria. Recombination analysis suggested that ToLCDiV may have originated from parental lineages related to ToLCBaV and tomato leaf curl Gujarat virus (ToLCGV), with recombination breakpoints in the AC1, AC4, and intergenic regions.
Conclusion
This study revealed a complex tomato virome associated with leaf curl disease in Tamil Nadu, driven by mixed viral infections and recombination. The detection of the putative novel recombinant begomovirus ToLCDiV and distinct alphasatellite ToLCMdA highlights the emergence of new virus-satellite components and emphasizes the need for continued virome surveillance and integrated disease management in tomato production systems.