The non-canonical tomato yellow leaf curl virus recombinant that displaced its parental viruses in southern Morocco exhibits a high selective advantage in experimental conditions.

ABSTRACT

Recombination events are frequently inferred from the increasing number of sequenced viral genomes, but their impact on natural viral populations has rarely been evidenced. TYLCV-IS76 is a recombinant (Begomovirus,Geminiviridae) between the Israel strain of tomato yellow leaf curl virus (TYLCV-IL) and the Spanish strain of tomato yellow leaf curl Sardinia virus (TYLCSV-ES) that was generated most probably in the late 1990s in southern Morocco (Souss). Its emergence in the 2000s coincided with the increasing use of resistant tomato cultivars bearing the Ty-1 gene, and led eventually to the entire displacement of both parental viruses in the Souss. Here, we provide compelling evidence that this viral population shift was associated with selection of TYLCV-IS76 viruses in tomato plants and particularly in Ty-1-bearing cultivars. Real-time quantitative PCR (qPCR) monitoring revealed that TYLCV-IS76 DNA accumulation in Ty-1-bearing plants was significantly higher than that of representatives of the parental virus species in single infection or competition assays. This advantage of the recombinant in Ty-1-bearing plants was not associated with a fitness cost in a susceptible, nearly isogenic, cultivar. In competition assays in the resistant cultivar, the DNA accumulation of the TYLCV-IL clone - the parent less affected by the Ty-1 gene in single infection - dropped below the qPCR detection level at 120 days post-infection (p.i.) and below the whitefly vector (Bemisia tabaci) transmissibility level at 60 days p.i. The molecular basis of the selective advantage of TYLCV-IS76 is discussed in relation to its non-canonical recombination pattern, and the RNA-dependent RNA polymerase encoded by the Ty-1 gene.