BackgroundAphids are serious pest on crops. By probing with their stylets, they interact with the plant, they vector viruses and when they reach the phloem they start a continuous ingestion. Many plant resistances to aphids have been identified, several have been deployed. However, some resistances breaking down have been observed. In the melon, a gene that confers resistance to aphids has been deployed in some melon-producing areas, and aphid colony development on Vat-carrying plants has been observed in certain agrosystems. The Vat gene is a NBS-LRR gene that confers resistance to the aphid species Aphis gossypii and exhibits the unusual characteristic of also conferring resistance to non-persistently transmitted viruses when they are inoculated by the aphid. Thus, we characterized patterns of resistance to aphid and virus using the aphid diversity and we investigated the mechanisms by which aphids and viruses may adapt to the Vat gene.ResultsUsing a Vat-transgenic line built in a susceptible background, we described the Vat- spectrum of resistance to aphids, and resistance to viruses triggered by aphids using a set of six A. gossypii biotypes. Discrepancies between both resistance phenotypes revealed that aphid adaptation to Vat-mediated resistance does not occur only via avirulence factor alterations but also via adaptation to elicited defenses. In experiments conducted with three virus species serially inoculated by aphids from and to Vat plants, the viruses did not evolve to circumvent Vat-mediated resistance.We confirmed discrepancies between both resistance phenotypes by testing each aphid biotype with a set of thirteen melon accessions chosen to reflect the natural diversity of the melon. Inheritance studies revealed that patterns of resistance to virus triggered by aphids are controlled by different alleles at the Vat locus and at least another locus located at a short genetic distance. Therefore, resistance to viruses triggered by aphids is controlled by a gene cluster.ConclusionsUnder the Flor model, changes in the avirulence gene determine the ability of the pathogen to overcome the resistance conferred by a plant gene. The Vat gene belongs to a resistance gene family that fits this pest/pathogen–plant interaction, and we revealed an additional mechanism of aphid adaptation that potentially exists in other interactions between plants and pests or pathogens.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-016-0708-5) contains supplementary material, which is available to authorized users.

Aphis gossypii and Bemisia tabaci are severe hemipteran pests of melon crops and breeding for resistance to both insects is required to reduce pesticide use. Resistance was evaluated for its effect on behaviour and biotic potential of both hemipterans in a population of recombinant inbred lines (RILs) derived from the cross Védrantais x PI 161375. Insect variability was considered using two A. gossypii clones and two B. tabaci populations. Two additive QTLs affected the whiteflies. Four additive QTLs and two couples of epistatic QTLs affected the aphids. Amongst them, a major QTL affects both behaviour and biotic potential of A. gossypii and therefore a same R gene induces both antixenosis and antibiosis. This major QTL colocalizes with the Vat gene belonging to the NBS-LRR gene family. No loci affected both aphids and whiteflies contrary to what was observed for the Mi1.2 gene, a NBS-LRR gene in tomato. Original populations with different allelic compositions at QTLs affecting A. gossypii were built by one inter-crossing of RILs used for the mapping process. The genetic background was shown homogeneous between these populations what allowed validating QTLs and investigating the effect of allelic combinations at QTLs. Effects of QTLs were stronger than expected and some QTLs had a wider spectrum than expected. This strategy of validation appeared rapid and low cost.

BackgroundHost plants exert considerable selective pressure on aphids because the plants constitute their feeding, mating and oviposition sites. Therefore, host specialisation in aphids evolves through selection of the behavioural and chemical mechanisms of host-plant location and recognition, and through metabolic adaptation to the phloem content of the host plant. How these adaptive traits evolve in an aphid species depends on the complexity of the annual life cycle of that species. The purpose of this field study was to determine how winged spring-migrant populations contribute to the evolution and maintenance of host specialisation in Aphis gossypii through host-plant choice and acceptance. We also assessed whether host-specialised genotypes corresponded exclusively to anholocyclic lineages regardless of the environmental conditions.ResultsThe spring populations of cotton-melon aphids visiting newly planted melon crops exhibited an unexpectedly high level of genetic diversity that contrasted with the very low diversity characterising the host-specialised populations of this aphid species. This study illustrated in natura host-plant-selection pressure by showing the great differences in genetic diversity between the spring-migrant populations (alate aphids) and the melon-infesting populations (the apterous offspring of the alate aphids). Moreover, an analysis of the genetic composition of these alate and apterous populations in four geographic regions suggested differences in life-history strategies, such as host choice and reproductive mode, and questioned the common assertion that A. gossypii is an anholocyclic species throughout its distribution area, including Europe.ConclusionsOur results clearly demonstrate that the melon plant acts as a selective filter against the reproduction of non-specialised individuals. We showed that olfactory cues are unlikely to be decisive in natura for host recognition by spring-migrant aphid populations that are not specialised on Cucurbitaceae. The agroecosystem structure and history of the four studied regions may have partially shaped the genetic structure of the spring-migrant populations of A. gossypii. Cucurbitaceae-specialised genotypes corresponded exclusively to anholocyclic lineages, regardless of the environmental conditions. However, some genotypes that were genetically close to the host-specialised genotypes and some genotypes that probably originated from wild plants had never been previously sampled; both were holocylic.

Development of molecular markers has allowed the characterization of several host-aphid interactions.We investigated the usefulness of microsatellite markers to characterize the plant-resistance interaction in the model Aphis gossypii/Cucumis melo. Six aphid clones, collected in different localities and years and belonging to two multilocus genotypes (MLGs) based on eight microsatellite markers were phenotyped on a set of 33 melon accessions, some of them known to carry the Vat gene.Three parameters were used: acceptance of plant, ability to colonize the plant and resistance to virus when inoculated by aphids. Concordance and correlation analyses showed that aphid clones sharing a same MLG exhibited a very agreeable phenotype on the set of accessions for acceptance of plant and resistance to virus when inoculated by aphids. From host point of view, melon accessions were grouped in four clear categories, resistant to aphids of both MLGs, only resistant to the NM1 MLG, only resistant to the C9 MLG, susceptible to both MLGs and another group of unclear characteristics.The four categories revealed different patterns of virulence for NM1 and C9 MLGs, that are likely controlled by a single avirulence gene in accordance with a gene for gene interaction. In contrast, the ability to colonize the plant appeared slightly variable among clones sharing a same MLG. We hypothesize it is due to the putative polygenic control of this aphid trait. Because the phenotypic variability of Aphis gossypii matched the genetic variability revealed by eight microsatellite markers, these markers could be used to infer the frequency of biotypes in field experiments and help to elucidate the allele diversity of melon resistance genes.

Resistance breakdown has been observed following the deployment of plant cultivars resistant to pests. Assessing the durability of a resistance requires long‐term experiments at least at a regional scale. We collected such data for melon resistance conferred by the Vat gene cluster to melon aphids. We examined landscape‐level populations of Aphis gossypii collected in 2004–2015, from melon‐producing regions with and without the deployment of Vat resistance and with different climates. We conducted demo‐genetic analyses of the aphid populations on Vat and non‐Vat plants during the cropping seasons. The Vat resistance decreased the density of aphid populations in all areas and changed the genetic structure and composition of these populations. Two bottlenecks were identified in the dynamics of adapted clones, due to the low levels of production of dispersal morphs and winter extinction. Our results suggest that (i) Vat resistance will not be durable in the Lesser Antilles, where no bottleneck affected the dynamics of adapted clones, (ii) Vat resistance will be durable in south‐west France, where both bottlenecks affected the dynamics of adapted clones and (iii) Vat resistance will be less durable in south‐east France, where only one of the two bottlenecks was observed.