Agroecological and evolutionary factors driving the success emergence of a non-canonical tomato yellow leaf curl virus recombinant

Background & Objectives TYLCV-IS76 (IS76) is a peculiar 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 entirely displaced its parental viruses in the Souss (Southern Morocco), possibly because of its positive selection by tomato cultivars bearing the Ty-1 tolerant gene 1. This prediction was tested under laboratory conditions. Materials & Methods The fitness of IS76 was estimated in a Ty-1 tolerant cultivar, and in a susceptible nearly isogenic line, in single or mixed infections with parental viruses TYLCV-IL and TYLCSV-ES. Viral DNA intra plant accumulation was measured with real time PCR (qPCR) and used as a proxy of fitness. An artificial TYLCV-IS76 recombinant (IS76') was constructed by site-directed mutagenesis to analyze the molecular determinant of the potential fitness advantage. Results IS76 DNA accumulation was significantly higher than that of TYLCV-IL and TYLCSV-ES in the tolerant cultivar, both in single or mixed infections. The fitness advantage of IS76 in the tolerant plants did not pay any accumulation cost in the susceptible plants in which IS76 accumulation was similar or higher than that of both parental viruses. Interestingly the IS76 selective advantage was associated with a dramatic negative impact on TYLCV-IL accumulation, which was shown to be determined by the recombination nature of IS76. Conclusions Our results support the positive selection of IS76 by the Ty-1 gene and validate the selective hypothesis to explain its emergence and the entire displacement of its parents in the Souss. It is expected that the fitness advantage of IS76 may involve gene silencing because the Ty-1 gene codes for an RdRp 1 and because the short TYLCSV derived region of IS76 is located in a region which has been reported for two begomoviruses to be one of the favored target of siRNA and methylation 2. (Résumé d'auteur