Benoît Moury

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 betweenPotato virus Y(PVY) and plant genotypes in the familySolanaceaecarrying 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 betweenPotato virus Y(PVY) variants and host plants in the familySolanaceaedeparts 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.

Summary: Taxonomy: P otato virus Y ( PVY ) is the type member of the genus P otyvirus in the family P otyviridae . Virion and genome properties: PVY virions have a filamentous, flexuous form, with a length of 730 nm and a diameter of 12 nm. The genomic RNA is single stranded, messenger sense, with a length of 9.7 kb, covalently linked to a viral‐encoded protein ( VPg ) at the 5’ end and to a 3’ polyadenylated tail. The genome is expressed as a polyprotein of approximately 3062 amino acid residues, processed by three virus‐specific proteases into 11 mature proteins. Hosts: PVY is distributed worldwide and has a broad host range, consisting of cultivated solanaceous species and many solanaceous and nonsolanaceous weeds. It is one of the most economically important plant pathogens and causes severe diseases in cultivated hosts, such as potato, tobacco, tomato and pepper, as well as in ornamental plants. Transmission: PVY is transmitted from plant to plant by more than 40 aphid species in a nonpersistent manner and, in potato, by planting contaminated seed tubers. Diversity: Five major clades, named C1 , C2 , C hile, N and O , have been described within the PVY species. In recent decades, a strong increase in prevalence of N × O recombinant isolates has been observed worldwide. A correlation has been observed between PVY phylogeny and certain pathogenicity traits. Genetic control of PVY: Resistance genes against PVY have been used widely in breeding programmes and deployed in the field. These resistance genes show a large diversity of spectrum of action, durability and genetic determinism. Notably, recessive and dominant major resistance genes show highly contrasting patterns of interaction with PVY populations, displaying rapid co‐evolution or stable relationships, respectively.

Adaptation of populations to new environments is frequently costly due to trade‐offs between life history traits, and consequently, parasites are expected to be locally adapted to sympatric hosts. Also, during adaptation to the host, an increase in parasite fitness could have direct consequences on its aggressiveness (i.e. the quantity of damages caused to the host by the virus). These two phenomena have been observed in the context of pathogen adaptation to host's qualitative and monogenic resistances. However, the ability of pathogens to adapt to quantitative polygenic plant resistances and the consequences of these potential adaptations on other pathogen life history traits remain to be evaluated. Potato virus Y and two pepper genotypes (one susceptible and one with quantitative resistance) were used, and experimental evolutions showed that adaptation to a quantitative resistance was possible and resulted in resistance breakdown. This adaptation was associated to a fitness cost on the susceptible cultivar, but had no consequence either in terms of aggressiveness, which could be explained by a high tolerance level, or in terms of aphid transmission efficiency. We concluded that quantitative resistances are not necessarily durable but management strategies mixing susceptible and resistant cultivars in space and/or in time should be useful to preserve their efficiency.

SUMMARY: Evolutionary processes responsible for parasite adaptation to their hosts determine our capacity to manage sustainably resistant plant crops. Most plant–parasite interactions studied so far correspond to gene‐for‐gene models in which the nature of the alleles present at a plant resistance locus and at a pathogen pathogenicity locus determine entirely the outcome of their confrontation. The interaction between the pepper pvr2 resistance locus and Potato virus Y (PVY) genome‐linked protein VPg locus obeys this kind of model. Using synthetic chimeras between two parental PVY cDNA clones, we showed that the viral genetic background surrounding the VPg pathogenicity locus had a strong impact on the resistance breakdown capacity of the virus. Indeed, recombination of the cylindrical inclusion (CI) coding region between two PVY cDNA clones multiplied by six the virus capacity to break down the pvr2 ³ ‐mediated resistance. High‐throughput sequencing allowed the exploration of the diversity of PVY populations in response to the selection pressure of the pvr2 ³ resistance. The CI chimera, which possessed an increased resistance breakdown capacity, did not show an increased mutation accumulation rate. Instead, selection of the most frequent resistance‐breaking mutation seemed to be more efficient for the CI chimera than for the parental virus clone. These results echoed previous observations, which showed that the plant genetic background in which the pvr2 ³ resistance gene was introduced modified strongly the efficiency of selection of resistance‐breaking mutations by PVY. In a broader context, the PVY CI coding region is one of the first identified genetic factors to determine the evolvability of a plant virus.

SUMMARY: Understanding the factors driving pathogen emergence and re‐emergence is a major challenge, particularly in agriculture, where the use of resistant plant cultivars imposes strong selective pressures on plant pathogen populations and leads frequently to ‘resistance breakdown’. Presently, durable resistances are only identified after a long period of large‐scale cultivation of resistant cultivars. We propose a new predictor of the durability of plant resistance. Because resistance breakdown involves modifications in the avirulence factors of pathogens, we tested for correlations between the evolutionary constraints acting on avirulence factors or their diversity and the durability of the corresponding resistance genes in the case of plant–virus interactions. An analysis performed on 20 virus species–resistance gene combinations revealed that the selective constraints applied on amino acid substitutions in virus avirulence factors correlate with the observed durability of the corresponding resistance genes. On the basis of this result, a model predicting the potential durability of resistance genes as a function of the selective constraints applied on the corresponding avirulence factors is proposed to help breeders to select the most durable resistance genes.

The genetic structure of Potato virus Y (PVY) populations was investigated in naturally‐infected pepper ( Capsicum annuum ) fields, collected at eight different localities in northern Tunisia, where 23% of the sampled plants were homozygous for the pvr2 ¹ recessive resistance allele, while the other plants carried the dominant susceptibility allele pvr2 ⁺ . Restriction fragment length polymorphism analysis at three PVY genome segments revealed a high level of viral diversity, with a majority of cases showing co‐infection of individual plants by several PVY haplotypes and a strong genetic differentiation of viral populations collected in the different localities. Geographic distances affected the differentiation of PVY populations and isolation by distance among these populations was significant. However, the occurrence of the pvr2 ¹ resistance allele did not contribute to the structure of viral populations, suggesting that the virulence properties of the virus did not significantly affect its fitness. Consequently, greater deployment of the pvr2 ¹ gene would probably not be a suitable strategy to control PVY, and other resistance genes should be preferred.

The recessive resistance genes pot-1 and pvr2 in Lycopersicon hirsutum and Capsicum annuum, respectively, control Potato virus Y (PVY) accumulation in the inoculated leaves. Infectious cDNA molecules from two PVY isolates differing in their virulence toward these resistances were obtained using two different strategies. Chimeras constructed with these cDNA clones showed that a single nucleotide change corresponding to an amino acid substitution (Arg119His) in the central part of the viral protein genome-linked (VPg) was involved in virulence toward the pot-1 resistance. On the other hand, 15 nucleotide changes corresponding to five putative amino acid differences in the same region of the VPg affected virulence toward the pvr2¹ and pvr2² resistances. Substitution models identified six and five codons within the central and C terminal parts of the VPg for PVY and for the related potyvirus Potato virus A, respectively, which undergo positive selection. This suggests that the role of the VPg-encoding region is determined by the protein and not by the viral RNA apart from its protein-encoding capacity.

Cucumber mosaic virus (CMV) has an extremely broad plant-host range, a large number of vector species, and a wide geographical distribution. CMV is, therefore, a model by which to understand plant virus adaptation. The selective constraints exerted on the five proteins expressed from the CMV genome were evaluated by application of newly developed maximum-likelihood algorithms to analyze sequences available in data banks. The ratio between nonsynonymous and synonymous substitution rates (ω) was used to detect positive selection on particular codon sites. Amino acid sequences were conserved with ω ranging from 0.07 to 0.60 in different proteins. However, a small proportion of amino acids in proteins 1a, 2a, and 3b, the coat protein (CP), were positively selected (ω > 1). Moreover, the evolution of the CP in the three subgroups of CMV strains revealed different selection profiles along the sequence and significantly different speed of evolution at many positions. Constraints exerted by aphid transmission, rather than plant adaptation, seemed to be responsible for these patterns of evolution in the CP.