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1. A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of Potato virus Y Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in Capsicum annuum .

Author

Moury B, Michon T, Simon V, and Palloix A

Subjects
RNA-Dependent RNA Polymerase genetics, RNA-Dependent RNA Polymerase metabolism, Phylogeny, Antiviral Agents, Plant Diseases, Capsicum, Potyvirus, Solanum tuberosum metabolism
Abstract

The dominant Pvr4 gene in pepper ( Capsicum annuum ) confers resistance to members of six potyvirus species, all of which belong to the Potato virus Y (PVY) phylogenetic group. The corresponding avirulence factor in the PVY genome is the NIb cistron (i.e., RNA-dependent RNA polymerase). Here, we describe a new source of potyvirus resistance in the Guatemalan accession C. annuum cv. PM949. PM949 is resistant to members of at least three potyvirus species, a subset of those controlled by Pvr4 . The F 1 progeny between PM949 and the susceptible cultivar Yolo Wonder was susceptible to PVY, indicating that the resistance is recessive. The segregation ratio between resistant and susceptible plants observed in the F 2 progeny matched preferably with resistance being determined by two unlinked recessive genes independently conferring resistance to PVY. Inoculations by grafting resulted in the selection of PVY mutants breaking PM949 resistance and, less efficiently, Pvr4 -mediated resistance. The codon substitution E 472 K in the NIb cistron of PVY, which was shown previously to be sufficient to break Pvr4 resistance, was also sufficient to break PM949 resistance, a rare example of cross-pathogenicity effect. In contrast, the other selected NIb mutants showed specific infectivity in PM949 or Pvr4 plants. Comparison of Pvr4 and PM949 resistance, which share the same target in PVY, provides interesting insights into the determinants of resistance durability.

Published
2023
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2. Estimating virus effective population size and selection without neutral markers.

Author

Rousseau E, Moury B, Mailleret L, Senoussi R, Palloix A, Simon V, Valière S, Grognard F, and Fabre F

Subjects
Evolution, Molecular, Genetic Drift, Genetic Markers, Genotype, High-Throughput Nucleotide Sequencing, Models, Genetic, Potyvirus physiology, Selection, Genetic, Capsicum virology, Plant Diseases virology, Potyvirus genetics
Abstract

By combining high-throughput sequencing (HTS) with experimental evolution, we can observe the within-host dynamics of pathogen variants of biomedical or ecological interest. We studied the evolutionary dynamics of five variants of Potato virus Y (PVY) in 15 doubled-haploid lines of pepper. All plants were inoculated with the same mixture of virus variants and variant frequencies were determined by HTS in eight plants of each pepper line at each of six sampling dates. We developed a method for estimating the intensities of selection and genetic drift in a multi-allelic Wright-Fisher model, applicable whether these forces are strong or weak, and in the absence of neutral markers. This method requires variant frequency determination at several time points, in independent hosts. The parameters are the selection coefficients for each PVY variant and four effective population sizes Ne at different time-points of the experiment. Numerical simulations of asexual haploid Wright-Fisher populations subjected to contrasting genetic drift (Ne ∈ [10, 2000]) and selection (|s| ∈ [0, 0.15]) regimes were used to validate the method proposed. The experiment in closely related pepper host genotypes revealed that viruses experienced a considerable diversity of selection and genetic drift regimes. The resulting variant dynamics were accurately described by Wright-Fisher models. The fitness ranks of the variants were almost identical between host genotypes. By contrast, the dynamics of Ne were highly variable, although a bottleneck was often identified during the systemic movement of the virus. We demonstrated that, for a fixed initial PVY population, virus effective population size is a heritable trait in plants. These findings pave the way for the breeding of plant varieties exposing viruses to stronger genetic drift, thereby slowing virus adaptation.

Published
2017
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3. High prevalence of poleroviruses in field-grown pepper in Turkey and Tunisia.

Author

Buzkan N, Arpaci BB, Simon V, Fakhfakh H, and Moury B

Subjects
Enzyme-Linked Immunosorbent Assay, Mediterranean Region, Phylogeny, Plant Diseases statistics & numerical data, RNA, Viral, Reverse Transcriptase Polymerase Chain Reaction, Tunisia epidemiology, Turkey epidemiology, Capsicum virology, Luteoviridae genetics, Luteoviridae isolation & purification, Plant Diseases virology
Abstract

Open-field pepper crops were sampled in 2011 in Turkey and Tunisia and surveyed for the major pepper-infecting viruses. As expected, potato virus Y and cucumber mosaic virus (in both countries), and tobacco etch virus (in Turkey only) were quite frequent. However, poleroviruses were the most common viruses, with prevalences above 70 %. Partial sequence analyses revealed the occurrence of poleroviruses resembling either beet western yellows virus (BWYV) or pepper vein yellows virus in the sampled areas, with BWYV being predominant in Turkey but in the minority in Tunisia. Poleroviruses should therefore be taken into account in disease control of pepper crops in the Mediterranean area.

Published
2013
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4. Modelling the evolutionary dynamics of viruses within their hosts: a case study using high-throughput sequencing.

Author

Fabre F, Montarry J, Coville J, Senoussi R, Simon V, and Moury B

Subjects
Capsicum virology, Evolution, Molecular, Models, Biological, Plant Diseases virology, Potyvirus physiology, Nicotiana virology
Abstract

Uncovering how natural selection and genetic drift shape the evolutionary dynamics of virus populations within their hosts can pave the way to a better understanding of virus emergence. Mathematical models already play a leading role in these studies and are intended to predict future emergences. Here, using high-throughput sequencing, we analyzed the within-host population dynamics of four Potato virus Y (PVY) variants differing at most by two substitutions involved in pathogenicity properties. Model selection procedures were used to compare experimental results to six hypotheses regarding competitiveness and intensity of genetic drift experienced by viruses during host plant colonization. Results indicated that the frequencies of variants were well described using Lotka-Volterra models where the competition coefficients β(ij) exerted by variant j on variant i are equal to their fitness ratio, r(j)/r(i). Statistical inference allowed the estimation of the effect of each mutation on fitness, revealing slight (s = -0.45%) and high (s = -13.2%) fitness costs and a negative epistasis between them. Results also indicated that only 1 to 4 infectious units initiated the population of one apical leaf. The between-host variances of the variant frequencies were described using Dirichlet-multinomial distributions whose scale parameters, closely related to the fixation index F(ST), were shown to vary with time. The genetic differentiation of virus populations among plants increased from 0 to 10 days post-inoculation and then decreased until 35 days. Overall, this study showed that mathematical models can accurately describe both selection and genetic drift processes shaping the evolutionary dynamics of viruses within their hosts.

Published
2012
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5. Genetic background matters: a plant-virus gene-for-gene interaction is strongly influenced by genetic contexts.

Author

Montarry J, Doumayrou J, Simon V, and Moury B

Subjects
Capsicum genetics, DNA, Complementary, Disease Resistance genetics, Plant Diseases genetics, Plant Diseases microbiology, Plant Proteins genetics, Potyvirus genetics, Protein Binding, Viral Proteins genetics, Capsicum metabolism, Capsicum virology, Plant Proteins metabolism, Potyvirus metabolism, Potyvirus pathogenicity, Viral Proteins metabolism
Abstract

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., (Molecular Plant Pathology © 2011 BSPP and Blackwell Publishing Ltd. No Claim to Original US Government Works.)

Published
2011
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6. Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants

Author

Rousseau, Elsa, Tamisier, Lucie, Fabre, Frédéric, Simon, Vincent, Szadkowski, Marion, Bouchez, Olivier, Zanchetta, Catherine, Girardot, Gregory, Mailleret, Ludovic, Grognard, Frédéric, Palloix, Alain, Moury, Benoit, Unité de Pathologie Végétale (PV), Institut National de la Recherche Agronomique (INRA), Biological control of artificial ecosystems (BIOCORE), Inria Sophia Antipolis - Méditerranée (CRISAM), Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de la Recherche Agronomique (INRA)-Laboratoire d'océanographie de Villefranche (LOV), Institut national des sciences de l'Univers (INSU - CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Génétique et Amélioration des Fruits et Légumes (GAFL), Santé et agroécologie du vignoble (UMR SAVE), Institut National de la Recherche Agronomique (INRA)-Université de Bordeaux (UB)-Institut des Sciences de la Vigne et du Vin (ISVV)-Ecole Nationale Supérieure des Sciences Agronomiques de Bordeaux-Aquitaine (Bordeaux Sciences Agro), Biologie du fruit et pathologie (BFP), Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Université Sciences et Technologies - Bordeaux 1 (UB), Génome et Transcriptome - Plateforme Génomique (GeT-PlaGe), Institut National de la Recherche Agronomique (INRA)-Plateforme Génome & Transcriptome (GET), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA), SMaCH metaprogramme, 'Investissement d’avenir' program managed by Agence Nationale pour la Recherche (contract ANR-10-INBS-09), BAP (Biologie et Amélioration des Plantes) department, Région Provence-Alpes-Côte d’Azur (PACA), Station de Pathologie Végétale (AVI-PATHO), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Unité de recherche Génétique et amélioration des fruits et légumes (GALF), Santé et agroécologie du vignoble (SAVE), Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Université Sciences et Technologies - Bordeaux 1, GeT PlaGe, Genotoul, Université Côte d'Azur (UCA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), and Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3)

Subjects
Models, Genetic, resistance breakdown, Potyvirus, [SDV.SA.AGRO]Life Sciences [q-bio]/Agricultural sciences/Agronomy, food and beverages, selection, Original Articles, Haploidy, Adaptation, Physiological, Biological Evolution, viral load, [SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics, eIF4E, Host-Pathogen Interactions, Linear Models, plant breeding, genetic drift, Selection, Genetic, Capsicum, ComputingMilieux_MISCELLANEOUS, effective population size, Disease Resistance, Plant Diseases, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

We thank the staff of the INRAE Experimental facilities of the Plant Pathology research unit (IEPV, https://doi.org/10.15454/8DGF-QF70) for their involvement in field experiments; International audience; The efficiency of plant major resistance genes is limited by the emergence and spread of resistance‐breaking mutants. Modulating the evolutionary forces acting on pathogen populations constitutes a promising way to increase the durability of these genes. We studied the effect of four plant traits affecting these evolutionary forces on the rate of resistance breakdown (RB) by a virus. Two of those traits correspond to virus effective population sizes (Ne), either at plant inoculation or during infection. The third trait corresponds to differential selection exerted by the plant on the virus population. Finally, the fourth trait corresponds to within‐plant virus accumulation (VA). These traits were measured experimentally on Potato virus Y (PVY) and a set of 84 pepper doubled‐haploid lines, all carrying the same pvr23 resistance gene but having contrasted genetic backgrounds. The lines showed extensive variation for the rate of pvr23 RB by PVY and for the four other traits of interest. A generalized linear model showed that three of these four traits, with the exception of Ne at inoculation, and several of pairwise interactions between them had significant effects on RB. RB increased when Ne during plant infection or VA increased. The effect of differential selection was more complex because of a strong interaction with VA. When VA was high, RB increased as the differential selection increased. An opposite relationship between RB and differential selection was observed when VA was low. This study provides a framework to select plants with appropriate virus‐evolution‐related traits to avoid or delay resistance breakdown.

Published
2018

7. Estimating virus effective population size and selection without neutral markers

Author

Rousseau, Elsa, Moury, Benoît, Mailleret, Ludovic, Senoussi, Rachid, Palloix, Alain, Simon, Vincent, Valière, Sophie, Grognard, Frédéric, Fabre, Frédéric, Unité de Pathologie Végétale (PV), Institut National de la Recherche Agronomique (INRA), Biological control of artificial ecosystems (BIOCORE), Laboratoire d'océanographie de Villefranche (LOV), Observatoire océanologique de Villefranche-sur-mer (OOVM), Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Villefranche-sur-mer (OOVM), Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Inria Sophia Antipolis - Méditerranée (CRISAM), Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de la Recherche Agronomique (INRA), Institut Sophia Agrobiotech (ISA), Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Recherche Agronomique (INRA), Biostatistique et Processus Spatiaux (BioSP), Génétique et Amélioration des Fruits et Légumes (GAFL), Biologie du fruit et pathologie (BFP), Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Université Sciences et Technologies - Bordeaux 1, Génome et Transcriptome - Plateforme Génomique (GeT-PlaGe), Institut National de la Recherche Agronomique (INRA)-Plateforme Génome & Transcriptome (GET), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Unité Animalerie Rongeurs (UAR), Unité Mixte de Recherche en Santé Végétale (INRA/ENITA) (UMRSV), Institut National de la Recherche Agronomique (INRA)-École Nationale d'Ingénieurs des Travaux Agricoles - Bordeaux (ENITAB)-Institut des Sciences de la Vigne et du Vin (ISVV), SMaCH (Sustainable Management of Crop Health) metaprogramme of INRA, grant over-seen by the French National Research Agency (ANR) as part of the 'Blanc2013' program (ANR-13-BSV7- 0011, FunFit project), Station de Pathologie Végétale (AVI-PATHO), Institut National de la Recherche Agronomique (INRA)-Inria Sophia Antipolis - Méditerranée (CRISAM), Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire d'océanographie de Villefranche (LOV), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech [Sophia Antipolis] (ISA), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), Biostatistique et Processus Spatiaux (BIOSP), Unité de recherche Génétique et amélioration des fruits et légumes (GALF), GeT PlaGe, Genotoul, Unité Mixte de Recherche en Santé Végétale (INRA/ENITA) (UMR SAVE), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Observatoire océanologique de Villefranche-sur-mer (OOVM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Inria Sophia Antipolis - Méditerranée (CRISAM), Institut National de la Recherche Agronomique (INRA)-Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS), Université Bordeaux Segalen - Bordeaux 2-Institut National de la Recherche Agronomique (INRA)-Université Sciences et Technologies - Bordeaux 1 (UB), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), and Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
lcsh:Immunologic diseases. Allergy, Evolutionary Genetics, Genetic Markers, Leaves, Evolutionary Processes, Heredity, Genotype, Population Size, [SDV]Life Sciences [q-bio], Potyvirus, Variant Genotypes, Plant Science, Microbiology, Viral Evolution, Evolution, Molecular, [SPI]Engineering Sciences [physics], Population Metrics, Effective Population Size, Virology, [INFO.INFO-AU]Computer Science [cs]/Automatic Control Engineering, Genetics, Selection, Genetic, [MATH]Mathematics [math], lcsh:QH301-705.5, Plant Diseases, Evolutionary Biology, Population Biology, Models, Genetic, Plant Anatomy, Genetic Drift, Biology and Life Sciences, High-Throughput Nucleotide Sequencing, food and beverages, Organismal Evolution, Genetic Mapping, lcsh:Biology (General), Microbial Evolution, lcsh:RC581-607, Capsicum, Population Genetics, Research Article
Abstract

By combining high-throughput sequencing (HTS) with experimental evolution, we can observe the within-host dynamics of pathogen variants of biomedical or ecological interest. We studied the evolutionary dynamics of five variants of Potato virus Y (PVY) in 15 doubled-haploid lines of pepper. All plants were inoculated with the same mixture of virus variants and variant frequencies were determined by HTS in eight plants of each pepper line at each of six sampling dates. We developed a method for estimating the intensities of selection and genetic drift in a multi-allelic Wright-Fisher model, applicable whether these forces are strong or weak, and in the absence of neutral markers. This method requires variant frequency determination at several time points, in independent hosts. The parameters are the selection coefficients for each PVY variant and four effective population sizes Ne at different time-points of the experiment. Numerical simulations of asexual haploid Wright-Fisher populations subjected to contrasting genetic drift (Ne ∈ [10, 2000]) and selection (|s| ∈ [0, 0.15]) regimes were used to validate the method proposed. The experiment in closely related pepper host genotypes revealed that viruses experienced a considerable diversity of selection and genetic drift regimes. The resulting variant dynamics were accurately described by Wright-Fisher models. The fitness ranks of the variants were almost identical between host genotypes. By contrast, the dynamics of Ne were highly variable, although a bottleneck was often identified during the systemic movement of the virus. We demonstrated that, for a fixed initial PVY population, virus effective population size is a heritable trait in plants. These findings pave the way for the breeding of plant varieties exposing viruses to stronger genetic drift, thereby slowing virus adaptation., Author summary A growing number of experimental evolution studies are using an “evolve-and-resequence” approach to observe the within-host dynamics of pathogen variants of biomedical or ecological interest. The resulting data are particularly appropriate for studying the effects of evolutionary forces, such as selection and genetic drift, on the emergence of new pathogen variants. However, it remains challenging to unravel the effects of selection and genetic drift in the absence of neutral markers, a situation frequently encountered for microbes, such as viruses, due to their small constrained genomes. Using such an approach on a plant virus, we observed that the same set of virus variants displayed highly diverse dynamics in closely related plant genotypes. We developed and validated a method that does not require neutral markers, for estimating selection coefficients and effective population sizes from these experimental evolution data. We found that the viruses experienced considerable diversity in genetic drift regimes, depending on host genotype. Importantly, genetic drift experienced by virus populations was shown to be a heritable plant trait. These findings pave the way for the breeding of plant varieties exposing viruses to strong genetic drift, thereby slowing virus adaptation.

Published
2017

8. The durability of a major resistance gene is affected by quantitative trait loci which also confer quantitative resistance to virus

Author

Quenouille-Lederer, Julie, Paulhiac, Estelle, Mistral, Pascale, Nemouchi, Ghislaine, Sage-Palloix, Anne-Marie, Savio, Bruno, Simon, Vincent, Moury, Benoit, Palloix, Alain, Génétique et Amélioration des Fruits et Légumes (GAFL), Institut National de la Recherche Agronomique (INRA), and Unité de Pathologie Végétale (PV)

Subjects
virus phytopathogène, cartographie de qtl, durabilité des résistances, résistance quantitative, qtl de résistance, Virologie, Virology, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, gène de résistance, pathologie végétale, virus y de la pomme de terre, ComputingMilieux_MISCELLANEOUS, Resistance durability, quantitative resistance, resistance breakdown, Capsicum, Potato virus Y, major resistance gene, QTL analysis, eukaryotic translation initiation factor 4E
Abstract

National audience

Published
2012

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

Author

Doumayrou, Juliette, Simon, Vincent, Montarry, Josselin, and Moury, Benoit

Subjects
piment, virus phytopathogène, séquence nucleique, plante légumière, capsicum, virus, lutte génétique, mutation, résistance durable, virus y de la pomme de terre, dna complementary, plant proteins, viral proteins, plant sciences
Abstract

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 pvr23-mediated resistance. High-throughput sequencing allowed the exploration of the diversity of PVY populations in response to the selection pressure of the pvr23 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 pvr23 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.

Published
2011

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

Author

Montarry, Josselin, Doumayrou, Juliette, Simon, Vincent, Moury, Benoit, Unité de Pathologie Végétale (PV), Institut National de la Recherche Agronomique (INRA), This study was supported by an AIP Bio-Resources from the Institut National de la Recherche Agronomique (INRA). We gratefully acknowledge Isabelle Bornard for electron microscopy observations, Mireille Jacquemond, Frederic Fabre and Alain Palloix for useful discussions of the present work, and Mark Tepfer for raising our awareness of the high-throughput sequencing technology. Josselin Montarry was the recipient of an INRA postdoctoral fellowship., Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, UR0407, Pathologie Végétale, Santé des plantes et environnement, Centre de Recherche PACA, Station de Pathologie Végétale (AVI-PATHO), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
DNA, Complementary, genetic control, séquence nucleique, [SDV]Life Sciences [q-bio], Potyvirus, plant sciences, virus, piment, phytopathogenic virus, potato virus y, lutte génétique, Disease Resistance, Plant Diseases, virus phytopathogène, nucleic sequence, sustainable resistance, Original Articles, virus y de la pomme de terre, viral proteins, dna complementary, plante légumière, chilli pepper, capsicum, mutation, résistance durable, plant proteins, Protein Binding
Abstract

International audience; 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 pvr23-mediated resistance. High-throughput sequencing allowed the exploration of the diversity of PVY populations in response to the selection pressure of the pvr23 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 pvr23 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.

Published
2011

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