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

Abstract

Background: Aphids 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.

Results: Using 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.

Conclusions: Under 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.

Fig. 1

Scoring for three traits of 2 references lines x 9 aphid clones combinations. a Percentage of melon plants with CMV symptoms after inoculation by nine clones of A. gossypii. Group: significant difference (p = 0.05) based on pairwise comparison by χ² statistics with Bonferroni correction (p_cor = 0.0006). Score: score for each combination. b Acceptance = number of aphids on the plant 72 h after infestation by 10 aphids. Group: significant difference (p = 0.05) after a non-parametric test (Steel-Dwass-Critchlow-Fligner procedure) with Bonferroni correction. Score: score for each combination. c. Ability to colonize observed 7 days after infestation by 10 aphids. Group: significant difference (p = 0.05) after a non-parametric test (Steel-Dwass-Critchlow-Fligner procedure) with Bonferroni correction. Score: score for each combination

Fig. 2

Relationship between resistance to A. gossypii and resistance to virus triggered by A. gossypii. Distribution of 123 interactions (melon accession/aphid clone) according to aphid a Acceptance and b Colonization, and interactions exhibiting either a resistant or susceptible phenotype after CMV inoculation by aphids

Fig. 3

Experimental evolution of WMV, ZYMV and CMV on Vat plants. Number of Vat plants exhibiting symptoms/number of tested plants after virus inoculation by the NM1 and C9 A. gossypii clones. For the primary inoculations, aphids acquired viruses from susceptible infected plants. For the following inoculations, aphids acquired viruses from previously infected Vat plants. (Control: number of Védrantais plants exhibiting symptoms/number tested)

Fig. 4

Model for A. gossypii/Vat-melon plant interaction: the 3 cases observed, a resistance to aphids and viruses, b susceptibility to aphids and resistance to viruses, c susceptibility to aphids and viruses, d resistance to aphids and susceptibility to viruses, which was not observed