Genetic background matters: a plant–virus gene‐for‐gene interaction is strongly influenced by genetic contexts

Montarry, Josselin; Doumayrou, Juliette; Simon, Vincent; Moury, Benoît

doi:10.1111/j.1364-3703.2011.00724.x

Cited by 32 publications

(55 citation statements)

References 53 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Sequence comparisons indicated that the S101G and D119G substitutions in the VPg of PVY SON41p allowed the breakdown of the va 2 resistance allele in tobacco. These two substitutions also allowed the breakdown of the pvr2 3 allele (14,42), displaying consequently a cross-infectivity effect between the va 2 and pvr2 3 alleles in tobacco and pepper cultivars, respectively (Fig. 3).…”

Section: Discussionmentioning

confidence: 99%

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

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

Self Cite

View full text Add to dashboard Cite

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...

show abstract

Section: Discussionmentioning

confidence: 99%

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

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

Self Cite

View full text Add to dashboard Cite

show abstract

“…However, the breakdown capacity of the 'CI chimera' was shown to be highly correlated with that of SON41p when inoculated to a large range of pepper genotypes (Quenouille et al, 2013). The 'CI chimera' and SON41p were not infectious per se in plants carrying pvr2 3 -that is, in these plants, the 'CI chimera' showed very weak accumulation detected through reverse transcriptase-polymerase chain reaction but not enzyme-linked immunosorbent assay (ELISA) and suggesting that the RB mutation occurred in the resistant plant (Montarry et al, 2011), whereas mutants of the 'CI chimera' possessing single non-synonymous substitutions in the VPg cistron could be detected at high concentration in systemically infected leaves. In addition, the CI chimera showed the same distributions of RB mutations when inoculated on plants carrying pvr2 3 when compared with SON41p.…”

Section: Virus Materialsmentioning

confidence: 99%

“…For evaluation of RB frequencies, we used a PVY chimera between PVY clones SON41p and LYE84.2 (Montarry et al, 2011). This PVY chimera, named 'CI chimera' , differs from SON41p only by the CI cistron, which was replaced by that of LYE84.2.…”

Section: Virus Materialsmentioning

confidence: 99%

“…The rest of the genome and more particularly the region directly involved in pvr2 3 RB (the VPg cistron) are strictly identical between the two PVY clones. This 'CI chimera' was chosen because of its higher ability to break the pvr2 3 resistance down compared with the parental clones (Montarry et al, 2011). However, the breakdown capacity of the 'CI chimera' was shown to be highly correlated with that of SON41p when inoculated to a large range of pepper genotypes (Quenouille et al, 2013).…”

Section: Virus Materialsmentioning

confidence: 99%

See 1 more Smart Citation

Quantitative trait loci from the host genetic background modulate the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants

Quenouille

Paulhiac

Moury³

et al. 2014

Heredity

View full text Add to dashboard Cite

The combination of major resistance genes with quantitative resistance factors is hypothesized as a promising breeding strategy to preserve the durability of resistant cultivar, as recently observed in different pathosystems. Using the pepper (Capsicum annuum)/Potato virus Y (PVY, genus Potyvirus) pathosystem, we aimed at identifying plant genetic factors directly affecting the frequency of virus adaptation to the major resistance gene pvr2 3 and at comparing them with genetic factors affecting quantitative resistance. The resistance breakdown frequency was a highly heritable trait (h 2 ¼ 0.87). Four loci including additive quantitative trait loci (QTLs) and epistatic interactions explained together 70% of the variance of pvr2 3 breakdown frequency. Three of the four QTLs controlling pvr2 3 breakdown frequency were also involved in quantitative resistance, strongly suggesting that QTLs controlling quantitative resistance have a pleiotropic effect on the durability of the major resistance gene. With the first mapping of QTLs directly affecting resistance durability, this study provides a rationale for sustainable resistance breeding. Surprisingly, a genetic trade-off was observed between the durability of PVY resistance controlled by pvr2 3 and the spectrum of the resistance against different potyviruses. This trade-off seemed to have been resolved by the combination of minor-effect durability QTLs under long-term farmer selection.

show abstract

“…Less attention has been given to plant-infecting viruses; several studies have been carried out using Sanger amplicon sequencing of a limited number of molecular clones (6)(7)(8)(9)(10). All NGS in-depth within-plant virus population studies reported to date employed amplicon sequencing, focusing on only a particular part of the viral genome (11)(12)(13)(14). However, different parts of the viral genome can be subjected to different selection pressures (15,16); thus, whole-genome characterization of virus populations would give a more complete picture.…”

mentioning

confidence: 99%

Deep Sequencing of Virus-Derived Small Interfering RNAs and RNA from Viral Particles Shows Highly Similar Mutational Landscapes of a Plant Virus Population

Kutnjak

Rupar

Gutiérrez-Aguirre

et al. 2015

J Virol

View full text Add to dashboard Cite

RNA viruses exist within a host as a population of mutant sequences, often referred to as quasispecies. Within a host, sequences of RNA viruses constitute several distinct but interconnected pools, such as RNA packed in viral particles, double-stranded RNA, and virus-derived small interfering RNAs. We aimed to test if the same representation of within-host viral population structure could be obtained by sequencing different viral sequence pools. Using ultradeep Illumina sequencing, the diversity of two coexisting Potato virus Y sequence pools present within a plant was investigated: RNA isolated from viral particles and virus-derived small interfering RNAs (the derivatives of a plant RNA silencing mechanism). The mutational landscape of the within-host virus population was highly similar between both pools, with no notable hotspots across the viral genome. Notably, all of the singlenucleotide polymorphisms with a frequency of higher than 1.6% were found in both pools. Some unique single-nucleotide polymorphisms (SNPs) with very low frequencies were found in each of the pools, with more of them occurring in the small RNA (sRNA) pool, possibly arising through genetic drift in localized virus populations within a plant and the errors introduced during the amplification of silencing signal. Sequencing of the viral particle pool enhanced the efficiency of consensus viral genome sequence reconstruction. Nonhomologous recombinations were commonly detected in the viral particle pool, with a hot spot in the 3= untranslated and coat protein regions of the genome. We stress that they present an important but often overlooked aspect of virus population diversity. IMPORTANCEThis study is the most comprehensive whole-genome characterization of a within-plant virus population to date and the first study comparing diversity of different pools of viral sequences within a host. We show that both virus-derived small RNAs and RNA from viral particles could be used for diversity assessment of within-plant virus population, since they show a highly congruent portrayal of the virus mutational landscape within a plant. The study is an important baseline for future studies of virus population dynamics, for example, during the adaptation to a new host. The comparison of the two virus sequence enrichment techniques, sequencing of virus-derived small interfering RNAs and RNA from purified viral particles, shows the strength of the latter for the detection of recombinant viral genomes and reconstruction of complete consensus viral genome sequence. RNA viruses are one of the fastest-evolving biological entities known. Due to their high mutation and recombination rates, viral populations exist within hosts as a cloud of nonidentical but similar sequences, often referred to as viral quasispecies (1). The generated variability, coupled with natural selection, population bottlenecks, and stochasticity, shape the structure of virus populations, which was shown to have important implications in virus fitness and pathogenicity (1). With the...

show abstract

Genetic background matters: a plant–virus gene‐for‐gene interaction is strongly influenced by genetic contexts

Cited by 32 publications

References 53 publications

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

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

Quantitative trait loci from the host genetic background modulate the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants

Deep Sequencing of Virus-Derived Small Interfering RNAs and RNA from Viral Particles Shows Highly Similar Mutational Landscapes of a Plant Virus Population

Contact Info

Product

Resources

About