Viral and Host Factors Involved in Host Gain and Host Loss by Tomato Leaf Curl Begomoviruses in Tomato and Cucumbers

Begomoviruses transmitted by whiteflies cause severe crop losses worldwide. Individual strains or isolates have a narrower host range, but collectively begomoviruses infect a wide range of plants. Begomovirus genomes undergo frequent recombination and mutations that confer a selective advantage in interactions with specific host factors facilitating host range adaptation, resulting in the rapid emergence of new strains with adapted host range. In this study, we examined the processes by which the begomoviruses can acquire and lose hosts by exchanging fragments of the viral genomes between a variant of tomato leaf curl New Delhi virus only infecting cucumber (ToLCNDV-C), tomato leaf curl Karnataka virus only infecting tomato (ToLCKV-T), and a ToLCNDV strain infecting both tomato and cucumber (ToLCNDV-T&C). We mapped the region responsible for tomato host loss to a 63 nucleotide (nt) region in the C-terminal of the transcriptional activator/replication enhancer protein (TrAP/REn) regions of ToLCNDV. We tested known host proteins reported to interact with this region using the yeast two-hybrid approach and found divergence in interactions with host proteins PCNA and AGO1. Finally, we found that the TrAP/REn region of DNA-A in conjunction with DNA-B can confer ToLCKV-T the ability to weakly infect its non-host, cucumber, and ToLCNDV-C to infect its non-host, tomato. Our studies reveal that multiple complex intra-virus interactions between viral proteins and virus-host interactions govern infectivity, virus accumulation and symptom severity.