Genome-wide association mapping of QTLs implied in potato virus Y population sizes in pepper: evidence for widespread resistance QTL pyramiding

Tamisier, lucie; Szadkowski, M.; Nemouchi, G.; Lefebvre, V.; Szadkowski, E.; Duboscq, R.; Santoni, S.; Sarah, G.; Sauvage, C.; Palloix, A.; Moury, B.

doi:10.1111/mpp.12874

Article (Scientific journals)

Genome-wide association mapping of QTLs implied in potato virus Y population sizes in pepper: evidence for widespread resistance QTL pyramiding

Tamisier, lucie; Szadkowski, M.; Nemouchi, G. et al.

2020 • In Molecular Plant Pathology, 21 (1), p. 3-16

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/262220

DOI
10.1111/mpp.12874

PubMed
31605444

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

mpp.12874.pdf

Publisher postprint (1.05 MB)

Download

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Capsicum annuum; Potato virus Y; Potyvirus; Capsicum; Chromosome Mapping; Chromosomes, Plant; Disease Resistance; Eukaryotic Initiation Factor-4E; Genome-Wide Association Study; Genotype; Plant Diseases; Polymorphism, Single Nucleotide; Quantitative Trait Loci

Abstract :

[en] In this study, we looked for genetic factors in the pepper (Capsicum annuum) germplasm that control the number of potato virus Y (PVY) particles entering the plant (i.e. effective population size at inoculation) and the PVY accumulation at the systemic level (i.e. census population size). Using genotyping-by-sequencing (GBS) in a core collection of 256 pepper accessions, we obtained 10 307 single nucleotide polymorphisms (SNPs) covering the whole genome. Genome-wide association studies (GWAS) detected seven SNPs significantly associated with the virus population size at inoculation and/or systemic level on chromosomes 4, 6, 9 and 12. Two SNPs on chromosome 4 associated with both PVY population sizes map closely to the major resistance gene pvr2 encoding the eukaryotic initiation factor 4E. No obvious candidates for resistance were identified in the confidence intervals for the other chromosomes. SNPs detected on chromosomes 6 and 12 colocalized with resistance quantitative trait loci (QTLs) previously identified with a biparental population. These results show the efficiency of GBS and GWAS in C. annuum, indicate highly consistent results between GWAS and classical QTL mapping, and suggest that resistance QTLs identified with a biparental population are representative of a much larger collection of pepper accessions. Moreover, the resistance alleles at these different loci were more frequently combined than expected by chance in the core collection, indicating widespread pyramiding of resistance QTLs and widespread combination of resistance QTLs and major effect genes. Such pyramiding may increase resistance efficiency and/or durability. © 2019 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Tamisier, lucie ; Université de Liège - ULg

Szadkowski, M.; GAFL, INRA, Montfavet, 84140, France, Pathologie Végétale, INRA, Montfavet, 84140, France

Nemouchi, G.; GAFL, INRA, Montfavet, 84140, France

Lefebvre, V.; GAFL, INRA, Montfavet, 84140, France

Szadkowski, E.; GAFL, INRA, Montfavet, 84140, France

Duboscq, R.; GAFL, INRA, Montfavet, 84140, France

Santoni, S.; UMR AGAP, INRA, Montpellier, F-34060, France

Sarah, G.; UMR AGAP, INRA, Montpellier, F-34060, France

Sauvage, C.; GAFL, INRA, Montfavet, 84140, France

Palloix, A.; GAFL, INRA, Montfavet, 84140, France

Moury, B.; Pathologie Végétale, INRA, Montfavet, 84140, France

Language :

English

Title :

Genome-wide association mapping of QTLs implied in potato virus Y population sizes in pepper: evidence for widespread resistance QTL pyramiding

Publication date :

2020

Journal title :

Molecular Plant Pathology

ISSN :

1464-6722

eISSN :

1364-3703

Publisher :

Blackwell, Oxford, United Kingdom

Volume :

Issue :

Pages :

3-16

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

INRA - Institut National de la Recherche Agronomique

Available on ORBi :

since 22 July 2021

Statistics

Number of views

94 (3 by ULiège)

Number of downloads

33 (3 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Aulchenko, Y.S., Ripke, S., Isaacs, A. and Van Duijn, C.M. (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics, 23, 1294–1296.
Ayme, V., Souche, S., Caranta, C., Jacquemond, M., Chadœuf, J., Palloix, A. and Moury, B. (2006) Different mutations in the genome-linked protein VPg of Potato virus Y confer virulence on the pvr23 resistance in pepper. Mol. Plant–Microbe Interact. 19, 557–563.
Brachi, B., Morris, G.P. and Borevitz, J.O. (2011) Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol. 12, 232.
Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y. and Buckler, E.S. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.
Brown, J.K. (2015) Durable resistance of crops to disease: a Darwinian perspective. Annu. Rev. Phytopathol. 53, 513–539.
Brun, H., Chèvre, A.-M., Fitt, B.D., Powers, S., Besnard, A.-L., Ermel, M., Huteau, V., Marquer, B., Eber, F., Renard, M. and Andrivon, D. (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol. 185, 285–299.
Ching, A., Caldwell, K.S., Jung, M., Dolan, M., Smith, O., Tingey, S., Morgante, M. and Rafalski, A.J. (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet. 3, 19.
Cormier, F., Le Gouis, J., Dubreuil, P., Lafarge, S. and Praud, S. (2014) A genome-wide identification of chromosomal regions determining nitrogen use efficiency components in wheat (Triticum aestivum L.). Theor. Appl. Genet. 127, 2679–2693.
Earl, D.A. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361.
Elena, S.F. and Sanjuán, R. (2007) Virus evolution: insights from an experimental approach. Annu. Rev. Ecol. Evol. Syst. 38, 27–52.
Ersoz, E.S., Yu, J. and Buckler, E.S. (2007) Applications of linkage disequilibrium and association mapping in crop plants. In: Genomics-Assisted Crop improvements (Varshney, R.K. and Tuberosa, R., eds), pp. 97–119. Berlin, Germany: Springer.
Evanno, G., Regnaut, S. and Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.
Flint-Garcia, S.A., Thornsberry, J.M. and Buckler, E.S. IV (2003) Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol. 54, 357–374.
Fournet, S., Kerlan, M.C., Renault, L., Dantec, J.P., Rouaux, C. and Montarry, J. (2013) Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence: Local adaptation and cross-virulence in Globodera pallida. Plant Pathol. 62, 184–193.
García-Arenal, F. and McDonald, B.A. (2003) An analysis of the durability of resistance to plant viruses. Phytopathology, 93, 941–952.
Gouesnard, B., Bataillon, T.M., Decoux, G., Rozale, C., Schoen, D.J. and David, J.L. (2001) MSTRAT: an algorithm for building germ plasm core collections by maximizing allelic or phenotypic richness. J. Hered. 92, 93–94.
Hamblin, M.T., Buckler, E.S. and Jannink, J.-L. (2011) Population genetics of genomics-based crop improvement methods. Trends Genet. 27, 98–106.
Han, K., Lee, H., Ro, N., Hur, O., Lee, J., Kwon, J. and Kang, B. (2018) QTL mapping and GWAS reveal candidate genes controlling capsaicinoid content in Capsicum. Plant Biotechnol. J. 16, 1546–1558.
Hayes, B. (2013) Overview of statistical methods for genome-wide association studies (GWAS). Methods Mol. Biol. 1019, 149–169.
Kim, S., Park, M., Yeom, S.-I., Kim, Y.-M., Lee, J.M., Lee, H.-A., Seo, E., Choi, J., Cheong, K., Kim, K.-T., Jung, K., Lee, G.-W., Oh, S.-K., Bae, C., Kim, S.-B., Lee, H.-Y., Kim, S.-Y., Kim, M.-S., Kang, B.-C., Jo, Y.D., Yang, H.-B., Jeong, H.-J., Kang, W.-H., Kwon, J.-K., Shin, C., Lim, J.Y., Park, J.H., Huh, J.H., Kim, J.-S., Kim, B.-D., Cohen, O., Paran, I., Suh, M.C., Lee, S.B., Kim, Y.-K., Shin, Y., Noh, S.-J., Park, J., Seo, Y.S., Kwon, S.-Y., Kim, H.A., Park, J.M., Kim, H.-J., Choi, S.-B., Bosland, P.W., Reeves, G., Jo, S.-H., Lee, B.-W., Cho, H.-T., Choi, H.-S., Lee, M.-S., Yu, Y., Do Choi, Y., Park, B.-S., van Deynze, A., Ashrafi, H., Hill, T., Kim, W.T., Pai, H.-S., Ahn, H.K., Yeam, I., Giovannoni, J.J., Rose, J.K.C., Sørensen, I., Lee, S.-J., Kim, R.W., Choi, I.-Y., Choi, B.-S., Lim, J.-S., Lee, Y.-H. and Choi, D. (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46, 270–278.
Korte, A. and Farlow, A. (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods, 9, 29.
Lafforgue, G., Tromas, N., Elena, S.F. and Zwart, M.P. (2012) Dynamics of the establishment of systemic potyvirus infection: independent yet cumulative action of primary infection sites. J. Virol. 86, 12912–12922.
Li, H. (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv Preprint. https://arxiv.org/abs/1303.3997v2.
Lipka, A.E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P.J., Gore, M.A., Buckler, E.S. and Zhang, Z. (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics, 28, 2397–2399.
Mangin, B., Siberchicot, A., Nicolas, S., Doligez, A., This, P. and Cierco-Ayrolles, C. (2012) Novel measures of linkage disequilibrium that correct the bias due to population structure and relatedness. Heredity, 108, 285.
Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10.
McDonald, B.A. and Linde, C. (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349–379.
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. and DePristo, M.A. (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303.
Moury, B., Morel, C., Johansen, E., Guilbaud, L., Souche, S., Ayme, V., Caranta, C., Palloix, A. and Jacquemond, M. (2004) Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol. Plant–Microbe Interact. 17, 322–329.
Mundt, C. (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40, 381–410.
Nicolaï, M., Pisani, C., Bouchet, J.-P., Vuylsteke, M. and Palloix, A. (2012) Short communication discovery of a large set of SNP and SSR genetic markers by high-throughput sequencing of pepper (Capsicum annuum). Genet. Mol. Res. 11, 2295–2300.
Nicolaï, M., Cantet, M., Lefebvre, V., Sage-Palloix, A.-M. and Palloix, A. (2013) Genotyping a large collection of pepper (Capsicum spp.) with SSR loci brings new evidence for the wild origin of cultivated C. annuum and the structuring of genetic diversity by human selection of cultivar types. Genet. Resour. Crop Evol. 60, 2375–2390.
Pagny, G., Paulstephenraj, P.S., Poque, S., Sicard, O., Cosson, P., Eyquard, J.P., Caballero, M., Chague, A., Gourdon, G., Negrel, L. and Candresse, T. (2012) Family-based linkage and association mapping reveals novel genes affecting Plum pox virus infection in Arabidopsis thaliana. New Phytol. 196, 873–886.
Palloix, A., Ayme, V. and Moury, B. (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol. 183, 190–199.
Peakall, R. and Smouse, P. (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28, 2537e2539.
Perrier, X. and Jacquemoud-Collet, J. (2006) DARwin (http://darwin.cirad.fr/darwin). Accessed 26 September 2019.
Peterson, B.K., Weber, J.N., Kay, E.H., Fisher, H.S. and Hoekstra, H.E. (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7, e37135.
Pink, D.A. (2002) Strategies using genes for non-durable disease resistance. Euphytica, 124, 227–236.
Pritchard, J.K., Stephens, M. and Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
Quenouille, J., Montarry, J., Palloix, A. and Moury, B. (2013a) Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown: Mechanisms of polygenic resistance durability. Mol. Plant Pathol. 14, 109–118.
Quenouille, J., Vassilakos, N. and Moury, B. (2013b) Potato virus Y: a major crop pathogen that has provided major insights into the evolution of viral pathogenicity. Mol. Plant Pathol. 14, 439–452.
Quenouille, J., Paulhiac, E., Moury, B. and Palloix, A. (2014) Quantitative trait loci from the host genetic background modulate the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants. Heredity, 112, 579–587.
Quenouille, J., Saint-Felix, L., Moury, B. and Palloix, A. (2015) 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. Mol. Plant Pathol. 17, 296–302.
Remington, D.L., Thornsberry, J.M., Matsuoka, Y., Wilson, L.M., Whitt, S.R., Doebley, J., Kresovich, S., Goodman, M.M. and Buckler, E.S. (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl. Acad. Sci. USA. 98, 11479–11484.
Rodrigo, G., Zwart, M.P. and Elena, S.F. (2014) Onset of virus systemic infection in plants is determined by speed of cell-to-cell movement and number of primary infection foci. J. R. Soc. Interface, 11, 20140555.
Rousseau, E., Tamisier, L., Fabre, F., Simon, V., Szadkowski, M., Bouchez, O., Zanchetta, C., Girardot, G., Mailleret, L., Grognard, F., Palloix, A. and Moury, B. (2018) Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants. Mol. Plant Pathol., 12, 2575–2589.
Ruffel, S., Gallois, J.-L., Moury, B., Robaglia, C., Palloix, A. and Caranta, C. (2006) Simultaneous mutations in translation initiation factors eIF4E and eIF (iso) 4E are required to prevent pepper veinal mottle virus infection of pepper. J. Gen. Virol. 87, 2089–2098.
Sage-Palloix, A.-M., Jourdan, F., Phaly, T., Némouchi, G., Lefebvre, V. and Palloix, A. (2007) Analysis of diversity in pepper genetic resources: distribution of horticultural and resistance traits in the INRA pepper germplasm. In: Progress in Research on Capsicum & Eggplant (Niemirowicz-Szczytt, K., ed), pp. 33–42. Poland: Warsaw University of Life Sciences Press.
Segura, V., Vilhjálmsson, B.J., Platt, A., Korte, A., Seren, Ü., Long, Q. and Nordborg, M. (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat. Genet. 44, 825.
Sonah, H., O’Donoughue, L., Cober, E., Rajcan, I. and Belzile, F. (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol. J. 13, 211–221.
Stekhoven, D.J. and Bühlmann, P. (2011) MissForest – non-parametric missing value imputation for mixed-type data. Bioinformatics, 28, 112–118.
Tamisier, L., Rousseau, E., Barraillé, S., Nemouchi, G., Szadkowski, M., Mailleret, L., Grognard, F., Fabre, F., Moury, B. and Palloix, A. (2017) Quantitative trait loci in pepper control the effective population size of two RNA viruses at inoculation. J. Gen. Virol. 98, 1923–1931.
Taranto, F., D’Agostino, N., Greco, B., Cardi, T. and Tripodi, P. (2016) Genome-wide SNP discovery and population structure analysis in pepper (Capsicum annuum) using genotyping by sequencing. BMC Genom. 17, 943.
Tenaillon, M.I., Sawkins, M.C., Long, A.D., Gaut, R.L., Doebley, J.F. and Gaut, B.S. (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc. Natl. Acad. Sci. USA. 98, 9161–9166.
VanRaden, P.M. (2008) Efficient methods to compute genomic predictions. J. Dairy Sci. 91, 4414–4423.
Zhan, J., Thrall, P.H., Papaïx, J., Xie, L. and Burdon, J.J. (2015) Playing on a pathogen’s weakness: using evolution to guide sustainable plant disease control strategies. Annu. Rev. Phytopathol. 53, 19–43.
Zhang, Z., Ersoz, E., Lai, C.-Q., Todhunter, R.J., Tiwari, H.K., Gore, M.A., Bradbury, P.J., Yu, J., Arnett, D.K., Ordovas, J.M. and Buckler, E.S. (2010) Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355.
Zwart, M.P., Daròs, J.-A. and Elena, S.F. (2011) One is enough: in vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog. 7, e1002122.