No abstract

Watermelon mosaic virus (WMV, genus Potyvirus, family Potyviridae) was reported for the first time in France in 1974, and it is now the most prevalent virus in cucurbit crops. In 2000, new strains referred as 'emerging' (EM) strains were detected in South-eastern France. EM strains are generally more severe and phylogenetically distinct from those previously reported in this country and referred as 'classic' (CL) strains. Since 2000, EM strains have been progressively replacing CL strains in several areas where they co-exist. In order to explain this rapid shift in virus populations, the biological properties of a set of 17 CL and EM WMV isolates were compared. No major differences were observed when comparing a limited host range including 48 different plant species or cultivars. Only two species were differential; Chenopodium quinoa was systemically infected by CL and not by EM isolates whereas Ranunculus sardous was systemically infected by EM and not by CL isolates. A considerable variability was observed in aphid transmission efficiencies but this could not be correlated to the CL or EM types. Two subsets of five isolates of each group were used to compare aphid transmission efficiencies from single and double (CL-EM) infections using six different cucurbit and non-cucurbit hosts. EM isolates were generally better transmitted from mixed CL-EM infections than CL isolates and CL transmission rates were significantly lower from double than from single infections. Cross-protection was only partial between CL and EM strains leading to frequent double infections, and only a slight asymmetry was observed in cross-protection efficiencies. Since double infections occur very commonly in fields, the preferential transmission of EM from mixed CL-EM infections could be one of the factors leading to the displacement of CL isolates by EM isolates.

Since their introduction in southeastern France around 1999, new, 'emerging' (EM) strains of watermelon mosaic virus (WMV) coexist with the 'classic' (CL) strains present for more than 40 years. This situation constitutes a unique opportunity to estimate the frequency of recombinants appearing in the few years following introduction of new strains of a plant RNA virus. Molecular analyses performed on more than 1000 isolates from epidemiological surveys (2004-2008) and from experimental plots (2009-2010), and targeting only recombinants that became predominant in at least one plant, revealed at least seven independent CL/EM or EM/EM recombination events. The frequency of recombinants involving at least one EM parent in the natural populations tested was on the order of 1 %. No new recombinant was detected for more than 1 year, and none but one in more than one location. In tests comparing host range and aphid transmissibility, the new recombinants did not display a better fitness than their 'parental' isolates. No recombinant was detected from artificial mixed infections of CL and EM isolates of various hosts after testing more than 1500 subcultures obtained after single-aphid transmission. These results constitute one of the first estimations of the frequency of recombinants in natural conditions for a plant RNA virus. This suggests that although viable recombinants of WMV are not rare, and although recombination may potentially lead to new highly damaging strains, the new recombinants observed so far had a lower fitness than the parental strains and did not emerge durably in the populations. The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this study are shown in Table 1.

Since 1999, "emerging" (EM) strains of Watermelon mosaic virus (WMV) have been detected in cucurbit crops of southeastern France, probably as a result of recent introductions. Population genetic approaches were used to study the structure of EM isolates in southeastern France and to identify factors involved in their spatial distribution. A population clustering method (SAMOVA) and a maximum-difference algorithm (Monmonier's algorithm) were combined to visualize and quantify barriers to gene flow between populations. Both methods yielded similar results and two main barriers were identified. A North/South oriented barrier may be related to physical obstacles to gene flow (Rhône River, presence of an area with few cucurbit crops). Although the barrier was very strong, some "crossing" events were detected. A second barrier, oriented Northwest to Southeast, was not correlated with obvious geographical features. The two methods used here are complementary and confirm the limited spread of WMV-EM isolates. This approach can be useful in epidemiology studies to characterize the structure of viral populations and identify barriers to gene flow.