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A key QTL cluster is conserved among accessions and exhibits broad-spectrum resistance to Phytophthora capsici: a valuable locus for pepper breeding

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Abstract

Developing cultivars carrying effective resistance against destructive pathogens has become a priority for breeders. While little is currently known about the genetic basis of durable resistance, it is generally associated with polygenic and broad-spectrum resistance. In this study, we assessed the spectrum of resistance to Phytophthora capsici conferred by a major effect quantitative trait locus (QTL) that has been detected in all of the resistant pepper accessions studied to date. After adding new markers derived from tomato sequences and those from pepper reported in the literature to three maps of pepper chromosome P5, we detected a QTL cluster involved in P. capsici resistance. By means of meta-analyses, we determined the occurrence of these QTLs in different genetic backgrounds and with different P. capsici isolates. Comparative mapping with tomato and potato highlighted a complex mosaic of Phytophthora resistance loci on colinear chromosome segments. We tested different lines with and without one of these QTLs, Pc5.1, with four isolates that we determined to be genetically distinct. Our data demonstrate that Pc5.1 is active against 12 isolates from different geographical origins and that it is conserved in all of the resistant accessions tested. We propose that this QTL is a key element responsible for the broad-spectrum resistance to P. capsici and, therefore, is a valuable locus for improving the effective resistance of pepper to P. capsici.

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References

  • Alimi N, Bink M, Dieleman J, Nicolaï M, Wubs M, Heuvelink E, Magan J, Voorrips R, Jansen J, Rodrigues P, van der Heijden G, Vercauteren A, Vuylsteke M, Song Y, Glasbey C, Barocsi A, Lefebvre V, Palloix A, van Eeuwijk F (2013) Genetic and QTL analyses of yield and a set of physiological traits in pepper. Euphytica 190(2):181–201. doi:10.1007/s10681-012-0767-0

    Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. doi:10.1093/nar/25.17.3389

    Article  PubMed  CAS  Google Scholar 

  • Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20(14):2324–2326

    Article  PubMed  CAS  Google Scholar 

  • Ayliffe M, Singh R, Lagudah E (2008) Durable resistance to wheat stem rust needed. Curr Opin Plant Biol 11(2):187–192. doi:10.1016/j.pbi.2008.02.001

    Article  PubMed  CAS  Google Scholar 

  • Barchi L, Bonnet J, Boudet C, Signoret P, Nagy I, Lanteri S, Palloix A, Lefebvre V (2007) A high-resolution, intraspecific linkage map of pepper (Capsicum annuum L.) and selection of reduced recombinant inbred line subsets for fast mapping. Genome 50(1):51–60

    Article  PubMed  CAS  Google Scholar 

  • Barchi L, Lefebvre V, Sage-Palloix A-M, Lanteri S, Palloix A (2009) QTL analysis of plant development and fruit traits in pepper and performance of selective phenotyping. TAG Theor Appl Genet 118:1157–1171

    Google Scholar 

  • Basten CJ, Weir BS, Zeng Z-B (1997) QTL CARTOGRAPHER: a reference manual and tutorial for QTL mapping, 1.17 edn. Department of Statistics, North Carolina State University, Raleigh

  • Bonnet J, Danan S, Boudet C, Barchi L, Sage-Palloix A-M, Caromel B, Palloix A, Lefebvre V (2007) Are the polygenic architectures of resistance to Phytophthora capsici and P. parasitica independent in pepper? TAG. Theor Appl Genet 115(2):253–264

    Article  PubMed  Google Scholar 

  • Brouwer DJ, Jones ES, St Clair DA (2004) QTL analysis of quantitative resistance to Phytophthora infestans (late blight) in tomato and comparisons with potato. Genome 47(3):475–492

    Article  PubMed  CAS  Google Scholar 

  • Danan S, Veyrieras J-B, Lefebvre V (2011) Construction of a potato consensus map and QTL meta-analysis offer new insights into the genetic architecture of late blight resistance and plant maturity traits. BMC Plant Biol 11(1):16

    Article  PubMed  Google Scholar 

  • Darvasi A, Soller M (1997) A simple method to calculate resolving power and confidence interval of QTL map location. Behav Genet 27(2):125–132. doi:10.1023/a:1025685324830

    Article  PubMed  CAS  Google Scholar 

  • Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. American Phytopathological Society, St. Paul

    Google Scholar 

  • Foolad M, Merk H, Ashrafi H (2008) Genetics, Genomics and Breeding of Late Blight and Early Blight Resistance in Tomato. Crit Rev Plant Sci 27(2):75–107

    Article  CAS  Google Scholar 

  • Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9(3):385–402. doi:10.1111/j.1364-3703.2007.00465.x

    Article  PubMed  Google Scholar 

  • Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323(5919):1357–1360. doi:10.1126/science.1166289

    Article  PubMed  CAS  Google Scholar 

  • Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325(5943):998–1001. doi:10.1126/science.1175550

    Article  PubMed  CAS  Google Scholar 

  • Govers F (2001) Misclassification of pest as ‘fungus’ puts vital research on wrong track. Nature 411(6838):633

    Article  PubMed  CAS  Google Scholar 

  • Guerrero-Moreno A, Laborde J (1980) Current status of pepper breeding for resistance to Phytophthora capsici in Mexico. In: Synopses IVth Eucarpia meeting capsicum working group, Wageningen, pp 52–56

  • Haldane JBS (1919) The combination of linkage values, and the calculation of distance between the loci of linked factors. J Genet 8:299–309

    Article  Google Scholar 

  • Hausbeck MK, Lamour KH (2004) Phytophthora capsici vegetable crops: research progress and management challenges. Plant Dis 88(12):1292–1303

    Article  Google Scholar 

  • Hu KM, Qiu DY, Shen XL, Li XH, Wang SP (2008) Isolation and manipulation of quantitative trait loci for disease resistance in rice using a candidate gene approach. Mol Plant 1(5):786–793. doi:10.1093/mp/ssn039

    Article  PubMed  CAS  Google Scholar 

  • Johnson R (1981) Durable resistance: definition of genetic control, and attainment in plant breeding. Phytopathology 71(6):567–568

    Article  Google Scholar 

  • Jørgensen IH (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63(1–2):141–152

    Article  Google Scholar 

  • Kamoun S (2001) Nonhost resistance to Phytophthora: novel prospects for a classical problem. Curr Opin Plant Biol 4(4):295–300

    Article  PubMed  CAS  Google Scholar 

  • Kim H-J, Nahm S-H, Lee H-R, Yoon G-B, Kim K-T, Kang B-C, Choi D, Kweon O, Cho M-C, Kwon J-K, Han J-H, Kim J-H, Park M, Ahn J, Choi S, Her N, Sung J-H, Kim B-D (2008) BAC-derived markers converted from RFLP linked to Phytophthora capsici resistance in pepper (Capsicum annuum L.). Theor Appl Genet 118(1):15–27

    Article  PubMed  CAS  Google Scholar 

  • Kimble KA, Grogan RG (1960) Resistance to Phytophthora root rot in pepper. Plant Dis Rep 44(11):872–873

    Google Scholar 

  • Kou YJ, Wang SP (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13(2):181–185. doi:10.1016/j.pbi.2009.12.010

    Article  PubMed  CAS  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323(5919):1360–1363. doi:10.1126/science.1166453

    Article  PubMed  CAS  Google Scholar 

  • Lamour KH, Finley L, Hurtado-Gonzales O, Gobena D, Tierney M, Meijer HJG (2006) Targeted gene mutation in Phytophthora spp. Mol Plant Microbe Interact 19(12):1359–1367. doi:10.1094/mpmi-19-1359

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1(2):174–181

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre V, Palloix A (1996) Both epistatic and additive effects of QTLs are involved in polygenic induced resistance to disease: a case study, the interaction pepper—Phytophthora capsici Leonian. Theor Appl Genet 93(4):503–511

    Article  CAS  Google Scholar 

  • Lefebvre V, Pflieger S, Thabuis A, Caranta C, Blattes A, Chauvet JC, Daubèze AM, Palloix A (2002) Towards the saturation of the pepper linkage map by alignment of three intraspecific maps including known-function genes. Genome 45(5):839–854

    Article  PubMed  CAS  Google Scholar 

  • Leonian LH (1922) Stem and fruit blight of peppers caused by Phytophthora capsici sp. nov. Phytopathology 12:401–408

    Google Scholar 

  • Li J, Liu L, Bai Y, Finkers R, Wang F, Du Y, Yang Y, Xie B, Visser R, van Heusden A (2011) Identification and mapping of quantitative resistance to late blight (Phytophthora infestans) in Solanum habrochaites LA1777. Euphytica 179(3):427–438. doi:10.1007/s10681-010-0340-7

    Article  Google Scholar 

  • Lincoln S, Daly M, Lander E (1992) Constructing genetic maps with MAPMAKER/EXP version 3.0, 3rd edn. Whitehead Institute Technical Report, Cambridge

  • Lindhout P (2002) The perspectives of polygenic resistance in breeding for durable disease resistance. Euphytica 124(2):217–226. doi:10.1023/a:1015686601404

    Article  CAS  Google Scholar 

  • Livingstone KD, Lackney VK, Blauth JR, van Wijk R, Jahn MK (1999) Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152(3):1183–1202

    PubMed  CAS  Google Scholar 

  • Lokossou AA, Park TH, van Arkel G, Arens M, Ruyter-Spira C, Morales J, Whisson SC, Birch PRJ, Visser RGF, Jacobsen E, van der Vossen EAG (2009) Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Mol Plant Microbe Interact 22(6):630–641. doi:10.1094/mpmi-22-6-0630

    Article  CAS  Google Scholar 

  • Minamiyama Y, Tsuro M, Kubo T, Hirai M (2007) QTL analysis for resistance to Phytophthora capsici in pepper using a high density SSR-based map. Breed Sci 57(2):129–134. doi:10.1270/jsbbs.57.129

    Article  CAS  Google Scholar 

  • Ogundiwin EA, Berke TF, Massoudi M, Black LL, Huestis G, Choi D, Lee S, Prince JP (2005) Construction of 2 intraspecific linkage maps and identification of resistance QTLs for Phytophthora capsici root-rot and foliar-blight diseases of pepper (Capsicum annuum L.). Theor Appl Genet 48(4):698–711

    CAS  Google Scholar 

  • Palloix A, Ayme V, 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(1):190–199

    Article  PubMed  CAS  Google Scholar 

  • Perrier X, Jacquemoud-Collet JP (2006) DARwin software http://darwin.cirad.fr/darwin

  • Pflieger S, Lefebvre V, Caranta C, Blattes A, Goffinet B, Palloix A (1999) Disease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions. Genome 42(6):1100–1110

    Article  PubMed  CAS  Google Scholar 

  • Pflieger S, Palloix A, Caranta C, Blattes A, Lefebvre V (2001) Defense response genes co-localize with quantitative disease resistance loci in pepper. Theor Appl Genet 103(6–7):920–929

    Article  CAS  Google Scholar 

  • Pozueta-Romero J, Klein M, Houlné G, Schantz M-L, Meyer B, Schantz R (1995) Characterization of a family of genes encoding a fruit-specific wound-stimulated protein of bell pepper (Capsicum annuum): identification of a new family of transposable elements. Plant Mol Biol 28(6):1011–1025

    Article  PubMed  CAS  Google Scholar 

  • Quirin EA, Ogundiwin EA, Prince JP, Mazourek M, Briggs MO, Chlanda TS, Kim K-T, Falise M, Kang B-C, Jahn MM (2005) Development of sequence characterized amplified region (SCAR) primers for the detection of Phyto.5.2, a major QTL for resistance to Phytophthora capsici Leon. in pepper. Theor Appl Genet 110(4):605–612

    Article  PubMed  CAS  Google Scholar 

  • Rhoné B, Raquin AL, Goldringer I (2007) Strong linkage disequilibrium near the selected Yr17 resistance gene in a wheat experimental population. Theor Appl Genet 114(5):787–802. doi:10.1007/s00122-006-0477-x

    Article  PubMed  Google Scholar 

  • Ristaino JB (1990) Intraspecific variation among isolates of Phytophthora capsici from pepper and cucurbit fields in North Carolina. Phytopathology 80(11):1253–1259. doi:10.1094/Phyto-80-1253

    Article  Google Scholar 

  • Rizzo DM, Garbelotto M, Hansen EA (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Ann Rev Phytopathol 43:309–335

    Article  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Smith PG, Kimble KA, Grogan RG, Millet AH (1967) Inheritance of resistance in peppers to Phytophthora root rot. Phytopathology 57:377–379

    Google Scholar 

  • Sugita T, Kinoshita T, Kawano T, Yuji K, Yamaguchi K, Nagata R, Shimizu A, Chen LZ, Kawasaki S, Todoroki A (2005) Rapid construction of a linkage map using high-efficiency genome scanning/AFLP and RAPD, based on an intraspecific, doubled-haploid population of Capsicum annuum. Breed Sci 55(3):287–295

    Article  CAS  Google Scholar 

  • Sugita T, Yamaguchi K, Kinoshita T, Yuji K, Sugimura Y, Nagata R, Kawasaki S, Todoroki A (2006) QTL analysis for resistance to Phytophthora blight (Phytophthora capsici Leon.) using an intraspecific doubled-haploid population of Capsicum annuum. Breed Sci 56(2):137–145

    Google Scholar 

  • Tan MYA, Hutten RCB, Celis C, Park TH, Niks RE, Visser RGF, van Eck HJ (2008) The R Pi-mcd1 locus from Solanum microdontum involved in resistance to Phytophthora infestans, causing a delay in infection, maps on potato chromosome 4 in a cluster of NBS-LRR genes. Mol Plant Microbe Interact 21(7):909–918. doi:10.1094/mpmi-21-7-0909

    Article  PubMed  CAS  Google Scholar 

  • Thabuis A, Palloix A, Pflieger S, Daubèze AM, Caranta C, Lefebvre V (2003) Comparative mapping of Phytophthora resistance loci in pepper germplasm: evidence for conserved resistance loci across Solanaceae and for a large genetic diversity. Theor Appl Genet 106(8):1473–1485

    PubMed  CAS  Google Scholar 

  • Thabuis A, Lefebvre V, Bernard G, Daubèze AM, Phaly T, Pochard E, Palloix A (2004a) Phenotypic and molecular evaluation of a recurrent selection program for a polygenic resistance to Phytophthora capsici in pepper. Theor Appl Genet 109(2):342–351

    Article  PubMed  CAS  Google Scholar 

  • Thabuis A, Palloix A, Servin B, Daubèze AM, Signoret P, Hospital F, Lefebvre V (2004b) Marker-assisted introgression of 4 Phytophthora capsici resistance QTL alleles into a bell pepper line: validation of additive and epistatic effects. Mol Breed 14(1):9–20

    Article  CAS  Google Scholar 

  • Truong HTH, Kim KT, Kim DW, Kim S, Chae Y, Park JH, Oh DG, Cho MC (2012) Identification of isolate-specific resistance QTLs to phytophthora root rot using an intraspecific recombinant inbred line population of pepper (Capsicum annuum). Plant Pathol 61(1):48–56. doi:10.1111/j.1365-3059.2011.02483.x

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Lee Tvd, Hornes M, Friters A, Pot J, Paleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23(21):4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Langston DB, Csinos AS, Gitaitis RD, Walcott RR, Ji PS (2009) Development of an improved isolation approach and simple sequence repeat markers to characterize Phytophthora capsici populations in irrigation ponds in Southern Georgia. Appl Environ Microbiol 75(17):5467–5473. doi:10.1128/aem.00620-09

    Article  PubMed  CAS  Google Scholar 

  • Wu FN, Eannetta NT, Xu YM, Durrett R, Mazourek M, Jahn MM, Tanksley SD (2009) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118(7):1279–1293. doi:10.1007/s00122-009-0980-y

    Article  PubMed  CAS  Google Scholar 

  • Yi G, Lee JM, Lee S, Choi D, Kim B-D (2006) Exploitation of pepper EST-SSRs and an SSR-based linkage map. Theor Appl Genet 114(1):113–130

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge Morgane Ardisson, Ghislaine Nemouchi, Thérèse Phaly and Anne-Marie Sage-Palloix for their assistance in the experimental parts of this study, Alain Palloix for his critical review of the manuscript, Münevver Göçmen (BATEM, Antalya, Turkey) for supplying the Phytophthora capsici isolate Pc204, referenced as TOP-1 in her collection, Jean-Paul Bouchet for his help in bio-informatics, and the staff of the INRA GAFL Experimental Unit for plant cultivation support. This work was partly supported by the Génoplante contract PhytoSol-2 that resides under the French National Agency for Research (ANR), and by the PhyCor project supported by the French Ministry of Agriculture and Fishing (MAAPRAT). In addition, it was approved by the French competitiveness cluster PEIFL (European fruits and vegetables innovative cluster). S.M. and S.E. were funded by Génoplante. M.C. was funded by the French Ministry of Higher Education and Research (MESR) through a doctoral research grant. This paper is dedicated to the memory of Babou, who is greatly missed. The experiments presented in this manuscript comply with the current laws in France.

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The authors declare that they have no conflict of interest.

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  1. Génétique et Amélioration des Fruits et Légumes (GAFL), Institut National de la Recherche Agronomique (INRA), UR 1052, CS 60094, 84143, Montfavet Cedex, France

    Stéphanie Mallard, Mélissa Cantet, Anne Massire, Alexandre Bachellez, Sophie Ewert & Véronique Lefebvre

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  1. Stéphanie Mallard
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  2. Mélissa Cantet
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Correspondence to Véronique Lefebvre.

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Mallard, S., Cantet, M., Massire, A. et al. A key QTL cluster is conserved among accessions and exhibits broad-spectrum resistance to Phytophthora capsici: a valuable locus for pepper breeding. Mol Breeding 32, 349–364 (2013). https://doi.org/10.1007/s11032-013-9875-3

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