The selection-driven emergence of an unusual Tomato yellow leaf curl virus recombinant that displaced its parental viruses

TYLCV-IS76 (IS76) is a recombinant from Morocco generated between representatives of the Israel strain of Tomato yellow leaf curl virus (TYLCV-IL) and the Spanish strain of Tomato yellow leaf curl Sardinia virus (TYLCSV-ES). Unlike the previously reported TYLCV/TYLCSV recombinants, IS76 has a non-canonical recombination profile and has replaced its parental viruses in Southern Morocco (Belabess et al. 2015, Virology 486, 291-306). As its emergence coincided with the deployment of Ty-1-tolerant tomato cultivars, it was thought that IS76 may have a selective advantage in tolerant plants. This prediction was tested by comparing the fitness of agro-infectious clones of IS76 and representatives of its parental viruses in tomato plants harboring or not the Ty-1 gene. IS76 DNA accumulation was significantly higher than that of TYLCV-IL and TYLCSV-ES in the plants of the tolerant cultivar. The fitness advantage did not incur any accumulation cost in the susceptible plants. Interestingly, the IS76 selective advantage was associated with a dramatic negative impact of IS76 on TYLCV-IL accumulation which was shown to be determined by the recombinant nature of IS76. As the fitness results are consistent with the selection of IS76 by tolerant tomato plants, it was intriguing that IS76 has emerged only in Morocco and not in other countries where Ty-1-tolerant tomato cultivars were similarly deployed. It was hypothesized that the emergence of IS76 requires an extremely rare combination of circumstances which occurred by chance in Morocco. The monitoring of the population of TYLCV/TYLCSV recombinants generated in 10 Ty-1-tolerant and 10 nearly isogenic susceptible plants co-infected with parental viruses, confirmed this hypothesis. Indeed, although 100% of the coinfected plants were positive for TYLCV-IL/TYLCSV-ES recombinants from 60 days post inoculation (dpi), IS76-type recombinants were generated in only 5 susceptible and 1 tolerant plants and they remained among the rarest recombinants even at 365 dpi. (Texte intégral