Pepper yellow leaf curl Aceh virus: a recombinant replacing the parental begomovirus is highly virulent and breaks Ty-1-mediated resistance in tomato

Begomovirus infections have threatened the global production of multiple crops, including Solanaceae species. Recombination, a frequent phenomenon in begomoviruses, has profound effects on viral populations, allowing them to adapt to changing environments. We previously isolated pepper yellow leaf curl Aceh virus (PepYLCAV) from pepper (Capsicum annuum), tomato (Solanum lycopersicum), and tobacco (Nicotiana tabacum) plants in Aceh Province, Indonesia, and determined that it is a recombinant of the widespread pepper yellow leaf curl Indonesia virus (PepYLCIV). To compare PepYLCAV with its major putative parent PepYLCIV in terms of virulence, multiple solanaceous species (Nicotiana benthamiana, pepper, and tomato) were inoculated with the two viruses. Symptom severity, growth inhibition, and viral DNA levels were greater with PepYLCAV than with PepYLCIV infection in N. benthamiana and tomato plants. In pepper plants, PepYLCAV caused severe leaf distortion rather than yellowing and greater growth inhibition than PepYLCIV did but with no increase in viral DNA. Inoculation with PepYLCAV compromised Ty-1-mediated resistance in tomato, resulting in moderate symptoms, which were not present in plants infected with PepYLCIV. A re-analysis of samples collected from fields in Indonesia from 2012 to 2019 using PCR showed that PepYLCAV rather than PepYLCIV has been the predominant species since 2017. The recombinant bipartite begomovirus PepYLCAV is more widespread and more virulent than its major putative parent PepYLCIV and can overcome the Ty-1-mediated resistance of commercial F1 hybrid tomato cultivars.