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Fine mapping of Ae-Ps4.5, a major locus for resistance to pathotype III of Aphanomyces euteiches in pea

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Abstract

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QTL mapping and recombinant screening confirmed the major effect of QTL Ae-Ps4.5 on pea resistance to pathotype III of Aphanomyces euteiches and fine-mapped the QTL to a 3.06-Mb interval.

Abstract

Aphanomyces root rot, caused by Aphanomyces euteiches, is the most important disease of pea (Pisum sativum L.) worldwide. The development of pea-resistant varieties is a major challenge to control the disease. Previous linkage studies identified seven main resistance quantitative trait loci (QTL), including the QTL Ae-Ps4.5 associated with partial resistance in US nurseries infested by the pea pathotype III of A. euteiches. This study aimed to confirm the major effect of Ae-Ps4.5 on A. euteiches pathotype III, refine its interval, and identify candidate genes underlying the QTL. QTL mapping on an updated genetic map from the Puget × 90-2079 pea recombinant inbred line population identified Ae-Ps4.5 in a 0.8-cM confidence interval with a high effect (R2 = 89%) for resistance to the Ae109 reference strain of A. euteiches (pathotype III) under controlled conditions. However, the QTL mapping did not detect Ae-Ps4.5 for resistance to the RB84 reference strain of A. euteiches (pathotype I). Screening 224-pea BC5F2 plant progeny derived from three near-isogenic lines (NILs) carrying the 90-2079 allele at Ae-Ps4.5 in the Puget genetic background with 26 SNP markers identified 15 NILs showing recombination in the QTL interval. Phenotyping of the recombinant lines for resistance to the Ae109 strain of A. euteiches reduced the QTL to a physical interval of 3.06 Mb, containing 50 putative annotated genes on the Caméor pea genome V1a among which three candidate genes highlighted. This study provides closely linked SNP markers and putative candidate genes to accelerate pea breeding for resistant varieties to Aphanomyces root rot.

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Heritability of each trait, genotyping and phenotyping information, linkage information, and QTL profiles are available in the main manuscript or as supplementary data.

References

  • Aubert G, Kreplak J, Leveugle M, Duborjal H, Klein A, Boucherot K, Vieille E, Chabert-Martinello M, Cruaud C, Bourion V, Lejeune-Hénaut I, Pilet-Nayel ML, Bouchenak-Khelladi Y, Francillonne N, Tayeh N, Pichon JP, Rivière N, Burstin J (2023) SNP discovery by exome capture and resequencing in a pea genetic resource collection. Peer Commun J. https://doi.org/10.24072/pcjournal.332

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Boutet G, Alves-Carvalho S, Falque M, Peterlongo P, Lhuillier E, Bouchez O, Lavaud C, Pilet-Nayel ML, Riviere N, Baranger A (2016) SNP discovery and genetic mapping using genotyping by sequencing of whole genome genomic DNA from a pea RIL population. BMC Genom 17:121

    Article  Google Scholar 

  • Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  PubMed  Google Scholar 

  • Camborde L, Kiselev A, Pel MJC, Le Ru A, Jauneau A, Pouzet C, Dumas B, Gaulin E (2022) An oomycete effector targets a plant RNA helicase involved in root development and defense. New Phytol 233:2232–2248

    Article  CAS  PubMed  Google Scholar 

  • Davis DW, Fritz VA, Pfleger FL, Percich JA, Malvick DK (1995) MN 144, MN 313, and MN 314—garden pea lines resistant to root-rot caused by Aphanomyces-euteiches drechs. HortScience 30:639–640

    Article  Google Scholar 

  • Desgroux A, L’Anthoëne V, Roux-Duparque M, Rivière JP, Aubert G, Tayeh N, Moussart A, Mangin P, Vetel P, Piriou C, McGee RJ, Coyne CJ, Burstin J, Baranger A, Manzanares-Dauleux M, Bourion V, Pilet-Nayel ML (2016) Genome-wide association mapping of partial resistance to Aphanomyces euteiches in pea. BMC Genom 17:124

    Article  Google Scholar 

  • Duarte J, Riviere N, Baranger A, Aubert G, Burstin J, Cornet L, Lavaud C, Lejeune-Henaut I, Martinant JP, Pichon JP, Pilet-Nayel ML, Boutet G (2014) Transcriptome sequencing for high throughput SNP development and genetic mapping in Pea. BMC Genom 15(126)

  • Figueiredo J, Sousa Silva M, Figueiredo A (2018) Subtilisin-like proteases in plant defence: the past, the present and beyond. Mol Plant Pathol 19:1017–1028

    Article  CAS  PubMed  Google Scholar 

  • Gibert S, Edel-Hermann V, Moussa Mcolo R, Gautheron E, Michel J, Bernaud E, Gautheron N, Sol J-M, Capelle G, Galland R, Bardon-Debats A, Lambert C, Steinberg C (2021) Risk assessment of Aphanomyces euteiches root rot disease: quantification of low inoculum densities in field soils using droplet digital PCR. Eur J Plant Pathol 161:503–528

    Article  CAS  Google Scholar 

  • Gou M, Balint-Kurti P, Xu M, Yang Q (2023) Quantitative disease resistance: multifaceted players in plant defense. J Integr Plant Biol 65:594–610

    Article  CAS  PubMed  Google Scholar 

  • Graves S, Piepho HP, Selzer L, Dorai-Raj S (2019) MultcompView: visualizations of paired comparisons. R package version 0.1–8, http://CRAN.R-project.org/package=multcompView

  • Gritton ET (1990) Registration of 5 root-rot resistant germplasm lines of processing pea. Crop Sci 30:1166–1167

    Article  Google Scholar 

  • Hamon C, Baranger A, Coyne CJ, McGee RJ, Le Goff I, L’Anthoene V, Esnault R, Riviere JP, Klein A, Mangin P, McPhee KE, Roux-Duparque M, Porter L, Miteul H, Lesne A, Morin G, Onfroy C, Moussart A, Tivoli B, Delourme R, Pilet-Nayel ML (2011) New consistent QTL in pea associated with partial resistance to Aphanomyces euteiches in multiple French and American environments. Theor Appl Genet 123:261–281

    Article  PubMed  Google Scholar 

  • Hamon C, Coyne CJ, McGee RJ, Lesne A, Esnault R, Mangin P, Herve M, Le Goff I, Deniot G, Roux-Duparque M, Morin G, McPhee KE, Delourme R, Baranger A, Pilet-Nayel ML (2013) QTL meta-analysis provides a comprehensive view of loci controlling partial resistance to Aphanomyces euteiches in four sources of resistance in pea. BMC Plant Biol 13:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrell FE, Dupont C (2019) Hmisc: harrell miscellaneous. R Package Version 4.2-0, https://CRAN.R-project.org/package=Hmisc

  • Hughes TJ, Grau CR (2007) Aphanomyces root rot or common root rot of legumes. Plant Health Instructor. https://doi.org/10.1094/PHI-I-2007-0418-01

    Article  Google Scholar 

  • John F, Sanford W (2019) An {R} companion to applied regression, third edition ed. Sage Publications. http://CRAN.R-project.org/package=car

  • Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kourelis J, van der Hoorn RAL (2018) Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraft JM (1992) Registration of 90–2079, 90–2131, and 90–2322 pea germplasms. Crop Sci 32:1076–1076

    Article  Google Scholar 

  • Kreplak J, Madoui MA, Cápal P, Novák P, Labadie K, Aubert G, Bayer PE, Gali KK, Syme RA, Main D, Klein A, Bérard A, Vrbová I, Fournier C, d’Agata L, Belser C, Berrabah W, Toegelová H, Milec Z, Vrána J, Lee H, Kougbeadjo A, Térézol M, Huneau C, Turo CJ, Mohellibi N, Neumann P, Falque M, Gallardo K, McGee R, Tar’an B, Bendahmane A, Aury JM, Batley J, Le Paslier MC, Ellis N, Warkentin TD, Coyne CJ, Salse J, Edwards D, Lichtenzveig J, Macas J, Doležel J, Wincker P, Burstin J (2019) A reference genome for pea provides insight into legume genome evolution. Nat Genet 51:1411–1422

    Article  CAS  PubMed  Google Scholar 

  • Lavaud C, Lesné A, Piriou C, Le Roy G, Boutet G, Moussart A, Poncet C, Delourme R, Baranger A, Pilet-Nayel ML (2015) Validation of QTL for resistance to Aphanomyces euteiches in different pea genetic backgrounds using near-isogenic lines. Theor Appl Genet 128:2273–2288

    Article  CAS  PubMed  Google Scholar 

  • Le May C, Onfroy C, Moussart A, Andrivon D, Baranger A, Pilet-Nayel ML, Vandemark G (2018) Genetic structure of Aphanomyces euteiches populations sampled from United States and France pea nurseries. Eur J Plant Pathol 150:275–286

    Article  Google Scholar 

  • Lenth RV (2023) Estimated marginal means, aka least-squares means. R package version 1.8.5, https://cran.r-project.org/web/packages/emmeans/index.html

  • Leprévost T, Boutet G, Lesné A, Rivière JP, Vetel P, Glory I, Miteul H, Le Rat A, Dufour P, Regnault-Kraut C, Sugio A, Lavaud C, Pilet-Nayel ML (2023) An overview of the diversity of QTL and haplotypes for resistance to aphanomyces root rot in pea (Pisum sativum), by integrating QTL, GWAS and new advanced backcross population studies. Front Plant Sci 14:1189289

  • Lockwood JL, Ballard JC (1960) Evaluation of pea introductions for resistance to aphanomyces and fusarium root rots. Michigan Q Bull 42(4):704–713

    Google Scholar 

  • Malvick DK, Grau CR, Percich JA (1998) Characterization of Aphanomyces euteiches strains based on pathogenicity tests and random amplified polymorphic DNA analyses. Mycol Res 102:465–475

    Article  CAS  Google Scholar 

  • Malvick DK, Percich JA (1998) Genotypic and pathogenic diversity among pea-infecting strains of Aphanomyces euteiches from the central and western United States. Phytopathology 88:915–921

    Article  CAS  PubMed  Google Scholar 

  • McGee RJ, Coyne CJ, Pilet-Nayel M-L, Moussart A, Tivoli B, Baranger A, Hamon C, Vandemark G, McPhee K (2012) Registration of pea germplasm lines partially resistant to aphanomyces root rot for breeding fresh or freezer pea and dry pea types. J Plant Regist 6:203

    Article  Google Scholar 

  • Moussart A (2022) Management of Aphanomyces root of pea in France, 8th International Legume Root Diseases workshop. https://workshop.inrae.fr/ilrd8/layout/set/print/Submission/Management-of-Aphanomyces-root-rot-of-pea-in-France/(offset)/1

  • Moussart A, Even MN, Tivoli B (2008) Reaction of genotypes from several species of grain and forage legumes to infection with a French pea isolate of the oomycete Aphanomyces euteiches. Eur J Plant Pathol 122:321–333

    Article  Google Scholar 

  • Moussart A, Onfroy C, Lesne A, Esquibet M, Grenier E, Tivoli B (2007) Host status and reaction of Medicago truncatula accessions to infection by three major pathogens of pea (Pisum sativum) and alfalfa (Medicago sativa). Eur J Plant Pathol 117:57–69

    Article  Google Scholar 

  • Moussart A, Wicker E, Duparque M, Rouxel F (2001) Development of an efficient screening test for pea resistance to Aphanomyces euteiches. In: AEP (Ed.), 4th Eur Conf Grain Legumes. July 8–12th, Cracow, Poland

  • Mundt CC (2018) Pyramiding for resistance durability: theory and practice. Phytopathology 108:792–802

    Article  CAS  PubMed  Google Scholar 

  • Papavizas GC, Ayers WA (1974) Aphanomyces species and their root diseases in pea and sugarbeet: a review. US Dep Agric Tech Bull 1485, 158

  • Pilet-Nayel ML, Muehlbauer FJ, McGee RJ, Kraft JM, Baranger A, Coyne CJ (2002) Quantitative trait loci for partial resistance to Aphanomyces root rot in pea. Theor Appl Genet 106:28–39

    Article  CAS  PubMed  Google Scholar 

  • Pilet-Nayel ML, Muehlbauer FJ, McGee RJ, Kraft JM, Baranger A, Coyne CJ (2005) Consistent quantitative trait loci in pea for partial resistance to Aphanomyces euteiches isolates from the United States and France. Phytopathology 95:1287–1293

    Article  CAS  PubMed  Google Scholar 

  • Quillévéré-Hamard A, Le Roy G, Lesné A, Le May C, Pilet-Nayel ML (2021) Aggressiveness of diverse french Aphanomyces euteiches isolates on pea near isogenic lines differing in resistance quantitative trait loci. Phytopathology 111:695–702

    Article  PubMed  Google Scholar 

  • Quillévéré-Hamard A, Le Roy G, Moussart A, Baranger A, Andrivon D, Pilet-Nayel ML, Le May C (2018) Genetic and pathogenicity diversity of Aphanomyces euteiches populations from pea-growing regions in France. Front Plant Sci 9:1673

    Article  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from http://www.R-project.org

  • Roux-Duparque M, Boitel C, Decaux B, Moussart A, Alamie J, Pilet-Nayel ML, Muel F (2004) Breeding peas for resistance to Aphanomyces root rot : current main outputs of three breeding programmes. In: 5th Eur Conf Grain Legumes. June 7–11th, Dijon, France

  • Searle SR, Speed FM, Milliken GA (1980) Population marginal means in the linear model: an alternative to least squares means. Am Stat 34:216–221

    MathSciNet  Google Scholar 

  • Sherwood R, Hagedorn D (1962) Studies on biology of Aphanomyces euteiches. Phytopathology 52:150

    Google Scholar 

  • Singh H, Kaur J, Bala R, Srivastava P, Sharma A, Grover G, Dhillon GS, Singh RP, Chhuneja P, Bains NS (2022) Residual effect of defeated stripe rust resistance genes/QTLs in bread wheat against prevalent pathotypes of Puccinia striiformis f. sp. tritici. PLOS ONE 17:e0266482

  • Sivachandra Kumar NT, Caudillo-Ruiz KB, Chatterton S, Banniza S (2021) Characterization of Aphanomyces euteiches pathotypes infecting peas in western Canada. Plant Dis 105:4025–4030

    Article  PubMed  Google Scholar 

  • Tayeh N, Aluome C, Falque M, Jacquin F, Klein A, Chauveau A, Bérard A, Houtin H, Rond C, Kreplak J, Boucherot K, Martin C, Baranger A, Pilet-Nayel ML, Warkentin TD, Brunel D, Marget P, Le Paslier M-C, Aubert G, Burstin J (2015) The GenoPea Infinium® BeadChip allowed the construction of a high-density highresolution gene-based consensus genetic map in pea and provided an overview on the genome organization. Plant J 84:1257–1273

    Article  CAS  PubMed  Google Scholar 

  • Wicker E, Moussart A, Duparque M, Rouxel F (2003) Further contributions to the development of a differential set of pea cultivars (Pisum sativum) to investigate the virulence of isolates of Aphanomyces euteiches. Eur J Plant Pathol 109:47–60

    Article  CAS  Google Scholar 

  • Wicker E, Rouxel F (2001) Specific behaviour of French Aphanomyces euteiches Drechs. Populations for virulence and aggressiveness on pea, related to isolates from Europe, America and New Zealand. Eur J Plant Pathol 107:919–929

    Article  Google Scholar 

  • Wu L, Fredua-Agyeman R, Hwang SF, Chang KF, Conner RL, McLaren DL, Strelkov SE (2021) Mapping QTL associated with partial resistance to Aphanomyces root rot in pea (Pisum sativum L.) using a 13.2 K SNP array and SSR markers. Theor Appl Genet 134:2965–2990

    Article  PubMed  Google Scholar 

  • Wu L, Fredua-Agyeman R, Strelkov SE, Chang KF, Hwang SF (2022) Identification of novel genes associated with partial resistance to aphanomyces root rot in field pea by BSR-seq analysis. Int J Mol Sci 23:9744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang T, Liu R, Luo Y, Hu S, Wang D, Wang C, Pandey MK, Ge S, Xu Q, Li N, Li G, Huang Y, Saxena RK, Ji Y, Li M, Yan X, He Y, Liu Y, Wang X, Xiang C, Varshney RK, Ding H, Gao S, Zong X (2022) Improved pea reference genome and pan-genome highlight genomic features and evolutionary characteristics. Nat Genet 54:1553–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Greenhouse-Experimental Facilities platform of IGEPP, for its contribution to plant material production and experimentation in controlled conditions. We acknowledge Limagrain Europe, FR, for the genotyping of plant material. We are grateful to Isabelle Glory for her contribution to the plant production, Gilles Boutet for his contribution to marker selection, and Rémi Ollivier for his help in the analysis of allelic variants.

Funding

This work was supported by the French PEAMAS project, which was supported by the FASO (Fonds d’Action Stratégique des Oléoprotéagineux), managed by SOFIPROTEOL, as well as by the PeaMUST project (ANR-11-BTBR-0002), which received funding from the French Government, managed by the Research National Agency (ANR) under the Investments for the Future.

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  1. IGEPP, INRAE, Institut Agro, Univ Rennes, 35653, Le Rheu, France

    Clément Lavaud, Angélique Lesné, Théo Leprévost & Marie-Laure Pilet-Nayel

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  1. Clément Lavaud
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  2. Angélique Lesné
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  4. Marie-Laure Pilet-Nayel
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Contributions

CL generated the phenotypic and genotypic data of the RIL and NIL recombinant populations, carried out statistical and genetic analyses, and drafted the manuscript. AL coordinated and participated to the construction of the NIL recombinant populations and participated in the phenotypic and genotypic data acquisition. TL participated in the QTL detection, the comparative QTL/GWA analyses, and contributed to draft the manuscript. MLPN supervised the study and the draft of the manuscript. All authors approved the final draft of the manuscript.

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Correspondence to Marie-Laure Pilet-Nayel.

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Communicated by Janila Pasupuleti.

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Lavaud, C., Lesné, A., Leprévost, T. et al. Fine mapping of Ae-Ps4.5, a major locus for resistance to pathotype III of Aphanomyces euteiches in pea. Theor Appl Genet 137, 47 (2024). https://doi.org/10.1007/s00122-024-04548-6

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