Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Abstract

The structural pattern of infectivity matrices, which contains infection data resulting from inoculations of a set of hosts by a set of parasites, is a key parameter for our understanding of biological interactions and their evolution. This pattern determines the evolution of parasite pathogenicity and host resistance, the spatiotemporal distribution of host and parasite genotypes, and the efficiency of disease control strategies. Two major patterns have been proposed for plant-virus genotype infectivity matrices. In the gene-for-gene model, infectivity matrices show a nested pattern, where the host ranges of specialist virus genotypes are subsets of the host ranges of less specialized viruses. In contrast, in the matching-allele (MA) model, each virus genotype is specialized to infect one (or a small set of) host genotype(s). The corresponding infectivity matrix shows a modular pattern where infection is frequent for plants and viruses belonging to the same module but rare for those belonging to different modules. We analyzed the structure of infectivity matrices between Potato virus Y (PVY) and plant genotypes in the family Solanaceae carrying different eukaryotic initiation factor 4E (eIF4E)-coding alleles conferring recessive resistance. Whereas this system corresponds mechanistically to an MA model, the expected modular pattern was rejected based on our experimental data. This was mostly because PVY mutations involved in adaptation to a particular plant genotype displayed frequent pleiotropic effects, conferring simultaneously an adaptation to additional plant genotypes with different eIF4E alleles. Such effects should be taken into account for the design of strategies of sustainable control of PVY through plant varietal mixtures or rotations. IMPORTANCEThe interaction pattern between host and virus genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. We found that the structure of the interaction between Potato virus Y (PVY) variants and host plants in the family Solanaceae departs significantly from the current model of interaction considered for these organisms because of frequent pleiotropic effects of virus mutations. These mutational effects allow the virus to expand rapidly its range of host plant genotypes, make it very difficult to predict the effects of mutations in PVY infectivity factors, and raise concerns about strategies of sustainable management of plant genetic resistance to viruses. T he interaction pattern between host and parasite genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. This pattern determines to a large extent the maintenance of genetic diversity in host and parasite populations (1), the structure of these populations in space and time (2, 3), and the evolution of parasite pathogenicity and host resistance (4).Different models of host-parasite interaction and coevolution have been proposed (3, 5) (F...

Diversity of genetic backgrounds modulating the durability of a major resistance gene. Analysis of a core collection of pepper landraces resistant to Potato virus Y

“…For PI369940 and G4, all infected plants were checked for the presence of RB mutations in the PVY VPg cistron: total RNA was extracted and the PVY VPg cistron was amplified by reverse transcription‐polymerase chain reaction (RT‐PCR) and sequenced according to Moury et al . (). For one and four infected plants of G4 and PI369940, respectively, we failed to sequence the PVY VPg cistron.…”

“…was not, or rarely, broken down (RB frequency ≤ 5%) and for the two accessions, PI369940 and G4, the pvr2 3/4 resistance was frequently broken down (40% and 52.5%, respectively). For PI369940 and G4, all infected plants were checked for the presence of RB mutations in the PVY VPg cistron: total RNA was extracted and the PVY VPg cistron was amplified by reverse transcription-polymerase chain reaction (RT-PCR) and sequenced according to Moury et al (2014). For one and four infected plants of G4 and PI369940, respectively, we failed to sequence the PVY VPg cistron.…”

“…The sequence of the eukaryotic initiation factor 4E (eIF4E) protein encoded by these two pvr2 alleles differs only by one amino acid substitution at position 205 (a glycine for pvr2 3 and an aspartic acid for pvr2 4 ). They displayed the same resistance specificity towards seven different PVY variants and were easily broken down compared with other pvr2 alleles (Ayme et al, 2007;Charron et al, 2008;Moury et al, 2014). To further test the durability of the pvr2 alleles in these different genetic backgrounds, we selected the accessions which were homozygous for pvr2 3 (16 accessions) or pvr2 4 (four accessions), whilst discarding the closely related accessions with identical genotypes at the tested simple sequence repeat (SSR) loci (Nicolaï et al, 2013), resulting in a final set of 20 C. annuum inbred lines issued from American, African and Asian pepper landraces (Table 1).…”

Specialization for resistance in wild host-pathogen interaction networks

“…The underlying genetic architecture of the interaction has also been predicted to be important in generating patterns of specificity and hence network structure (Flores et al, 2012 ; Moury et al, 2014 ). Several different models that describe the genetic nature of host-pathogen interactions have been proposed, the most important of which are the gene-for-gene (GFG) and matching allele (MA) models (see Thrall et al this issue for review).…”

Survey of viruses infecting open‐field pepper crops in Côte d'Ivoire and diversity of Pepper veinal mottle virus and Cucumber mosaic virus

“…The central part of the VPg of PVY shows a large amino acid diversity and evidence of positive selection at some amino acid positions (Ben Khalifa et al, 2012;Moury et al, 2014). The high rate of amino acid substitutions in this small region was explained by the selection of virulence properties against eIF4E-mediated recessive resistance in several crops belonging to the family Solanaceae including pepper (Ayme et al, 2006;Ben Khalifa et al, 2012;Moury et al, 2014). The observation of a similarly high level of amino acid diversity and evidence of positive selection in the corresponding region of PVMV VPg is surprising because PVMV-resistant pepper cultivars are rarely grown.…”