NBS-LRR-mediated resistance triggered by aphids: viruses do not adapt; aphids adapt via different mechanisms

Abstract

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.

Impact of Vat resistance in melon on viral epidemics and genetic structure of virus populations

“…Second, many aphids in addition to A. gossypii species visit the melon crops (Schoeny, unpublished data) and do not trigger the resistance to CMV, as previously shown (Lecoq et al, 1979. Interestingly, the Vat resistance to CMV appears to be highly durable as suggested by the absence of CMV evolution toward overcoming the gene (Boissot et al, 2016b). Moreover the 18 low variability of CMV observed in this study (data not shown) also suggests that in fields, Vat resistance did not lead to selection of particular CMV isolates.…”

“…(Auteur de correspondance), Desbiez, C., Millot, P., Wipf-Scheibel, C., Nozeran, K., Gognalons, P., Vat (Boissot et al, 2016a). Although adapted clones have been characterized (Boissot et al, 2016b), these cultivars still represent an efficient option to control A. gossypii. On the contrary, the 'virus side' of Vat pleiotropic phenotype is seldom regarded as an asset for virus control.…”

“…On the contrary, the 'virus side' of Vat pleiotropic phenotype is seldom regarded as an asset for virus control. In controlled conditions, Vat was shown to confer resistance to CMV, WMV and ZYMV when inoculated by A. gossypii (Lecoq et al, 1979Boissot et al, 2016b) but Vat-carrying plants remained susceptible when viruses were inoculated mechanically or by other aphid species including A. craccivora, A. fabae and Myzus persicae (Lecoq et al, 1979. The effect of Vat on virus epidemics in the field has been poorly documented so far (Boissot et al, 2016a).…”

“…(Auteur de correspondance), Desbiez, C., Millot, P., Wipf-Scheibel, C., Nozeran, K., Gognalons, P., Lecoq (Boissot et al, 2016b). They may explain why CABYV development was not totally controlled in R plots.…”

“…Vat had no effect on the development of WMV epidemics, and it was shown that WMV, like CMV, could not adapt to Vat-mediated resistance under experimental conditions (Boissot et al, 2016b).…”