Evolution of populations of cucurbit-infecting potyviruses in France: insights into the mechanisms of plant virus emergence

Watermelon mosaic virus (WMV) and Zucchini yellow mosaic virus (ZYMV) are among the major cucurbit-infecting viruses worldwide. In France, WMV has a high prevalence every year throughout the growing season; ZYMV, although it can present locally a very high agronomic impact, induces epidemics that are very irregular both in spatial distribution and timing of infection. Large-scale epidemiological surveys followed by molecular analysis of all collected samples were performed during 5 years in France, and revealed the recent appearance of new, “emerging” (EM) isolates of both viruses in south-eastern France. In the case of WMV, four subgroups of EM isolates were defined, probably resulting from several recent introductions. They presented a strong geographic structure that remained stable over 5 years, and tended to replace rapidly the original “classic” isolates in areas where both types of strains were present. For ZYMV, at least two subgroups of new isolates were also detected in the last years, although the geographic structure of infections and evolution of populations was less obvious than for WMV. In order to characterize the evolution of viral populations and study the mechanisms favouring or limiting viral emergence and spread, several complementary approaches were developed: multilocal and multiscale epidemiological studies, molecular analyses and population genetics, as well as estimation of viral fitness in experimental condition and modeling. The risks of emergence of recombinants between “classic” and EM populations in the few years following their contact were also assessed.