Skip to main content

Advertisement

SpringerLink
Log in

Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The root-knot nematode (Meloidogyne spp.) is a major plant pathogen, affecting several solanaceous crops worldwide. In Capsicum annuum, resistance to this pathogen is controlled by several independent dominant genes—the Me genes. Six Me genes have previously been shown to be stable at high temperature in three highly resistant and genetically distant accessions: PI 322719, PI 201234, and CM334 (Criollo de Morelos 334). Some genes (Me4, Mech1, and Mech2) are specific to certain Meloidogyne species or populations, whereas others (Me1, Me3, and Me7) are effective against a wide range of Meloidogyne species, including M. arenaria, M. javanica, and M. incognita, the most common species in Mediterranean and tropical areas. These genes direct different response patterns in root cells depending on the pepper line and nematode species. Allelism tests and fine mapping using the BSA-AFLP approach showed these genes to be different but linked, with a recombination frequency of 0.02–0.18. Three of the PCR-based markers identified in several genetic backgrounds were common to the six Me genes. Comparative mapping with CarthaGene software indicated that these six genes clustered in a single genomic region within a 28 cM interval. Four markers were used to anchor this cluster on the P9 chromosome on an intraspecific reference map for peppers. Other disease resistance factors have earlier been mapped in the vicinity of this cluster. This genomic area is colinear to chromosome T12 of tomato and chromosome XII of potato. Four other nematode resistance genes have earlier been identified in this area, suggesting that these nematode resistance genes are located in orthologous genomic regions in Solanaceae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aravind L, Dixit V, Koonin E (1999) The domains of death: evolution of the apoptosis machinery. Trends Biol Sci 24:47–53

    Article  CAS  Google Scholar 

  • Berthou F, Palloix, Mugniery D (2003) Characterisation of virulence in populations of Meloidogyne chitwoodi and evidence for a resistance gene in pepper Capsicum annuum L. line PM 217. Nematology 5:383–390

    Article  Google Scholar 

  • Bleve-Zaccheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P (1998) The pepper resistance genes Me1 et Me3 induce differential penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection. Plant Sci 133:79–90

    Article  Google Scholar 

  • Caranta C, Lefebvre V, Palloix A (1997) Polygenic resistance of pepper to potyviruses consists of a combination of isolate-specific and broad-spectrum quantitative trait loci. Mol Plant Microbe Interact 10:872–878

    CAS  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Djian-Caporalino C (2001) New data on the specificity of the root-knot nematode resistance genes Me1 and Me3 in pepper. Plant Breed 120:429–433

    Article  CAS  Google Scholar 

  • Claverie M (2004) Stratégie de clonage du gène Ma1 conférant la résistance aux nématodes du genre Meloidogyne chez Prunus cerasifera. Thèse de Doctorat, Ecole Nationale Supérieure Agronomique de Montpellier, pp 134

  • Cook AA (1984) Florida XVR 3–25 bell pepper. Hortscience 19:375

    Google Scholar 

  • Cook AA, Guevara YG (1984) Hypersensitivity in Capsicum chacoense to race 1 of the bacterial spot pathogen of pepper. Plant Dis 68:329–330

    Google Scholar 

  • de Jong W, Forsyth A, Leister D, Gebhardt C, Baulcombe DC (1997) A potato hypersensitive resistance gene against potato virus X maps to a resistance gene cluster on chromosome 5, Theor Appl Genet 95:246–252

    Article  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Januel A, Lefebvre V, Daubeze A, Palloix A, Dalmasso A, Abad P (1999) Spectrum of resistance to root-knot nematodes and inheritance of heat-stable resistance in pepper (Capsicum annuum L.). Theor Appl Genet 99:496–502

    Article  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Fazari A, Samson M, Gaveau L, O’Byrne C, Lefebvre V, Caranta C, Palloix A, Abad P (2001) High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me3 and Me4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.). Theor Appl Genet 103:592–600

    Article  CAS  Google Scholar 

  • Dumas de Vaulx R, Chambonnet D, Pochard E (1981) Culture in vitro d’anthères de piment (Capsicum annuum) : amélioration des taux d’obtention de plantes chez différents génotypes par des traitements à +35°C. Agronomie 1(10):859–864

    Google Scholar 

  • Ernst Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schatschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F (1991) RFLP maps of potato and their alignment with the homologous tomato genome. Theor Appl Genet 83:49–57

    Article  Google Scholar 

  • Giovannoni JJ, Wing RA, Ganal MW, Tanksley SD (1991) Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. Nucleic Acids Res 19(23):6553–6558

    Article  PubMed  CAS  Google Scholar 

  • Grube RC (1999) Genetics of virus resistance in Capsicum and comparative analysis of disease resistance in the Solanaceae. PhD, Cornell University, USA, p 172

  • Grube RC, Blauth JR, Arnedo MS, Caranta C, Jahn MK (2000a). Identification and comparative mapping of a dominant potyvirus resistance gene cluster in Capsicum. Theor Appl Genet 101:852–859

    Article  CAS  Google Scholar 

  • Grube RC, Radwanski ER, Jahn MK (2000b) Comparative genetics of disease eesistance within the Solanaceae. Genetics 155:873–887

    CAS  Google Scholar 

  • Hare WW (1956) Resistance in pepper to Meloidogyne incognita acrita. Phytopathology 46:98–104

    Google Scholar 

  • Hendy H (1984) Contribution à l’étude des relations hôte-parasite chez les nématodes phytophages du genre Meloidogyne. Génétique et mécanismes de la résistance chez Capsicum spp. Thèse de Doctorat, USTL Montpellier, France, p 157

  • Hendy H, Pochard E, Dalmasso A (1985) Transmission héréditaire de la résistance aux Meloidogyne portée par deux lignées de Capsicum annuum: études de descendances d’homozygotes issues d’androgénèse. Agronomie 5:93–100

    Google Scholar 

  • Hulbert S, Pryor T, Hu G, Richter T, Drake J (1997) Genetic fine structure of resistance loci. In: Crute IR, Holub EB, Burdon JJ (eds) The gene-for-gene relationship in plant–parasite interactions. CAB International, Wallingford

  • Kim JM, Vanguri S, Boeke JD, Gabriel A, Voyta DF (1998) Transposable elements and genome organization: a comparative survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8:464–478

    PubMed  CAS  Google Scholar 

  • Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410

    Article  PubMed  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Kouassi AB, Kerlan MC, Caromel B, Dantec JP, Fouville D, Manzanares-Dauleux M, Ellissèche D, Mugniéry D (2005) A major gene mapped on chromosome XII is the main factor of a quantitatively inherited resistance to Meloidogyne fallax in Solanum sparsipilum. Theor Appl Genet, Published online, 20 December 2005

  • Kruijt M., Bas BF, de Wit PJGM (2004) Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes that mediate Avr9 responsiveness. Genetics 168:1655–1663

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre V (2004) Molecular markers for genetics and breeding: development and use in pepper (Capsicum spp.) In: Lörz H, Wenzel G (eds) Biotechnology in agriculture and forestry, vol 55. Molecular marker systems in plant breeding and crop improvement. Springer, Berlin Heidelberg New York, pp 189–214

  • Lefebvre V, Palloix A, Rives M (1993) Nuclear RFLP between pepper cultivars (Capsicum annuum L.). Euphytica 71:189–199

    Article  Google Scholar 

  • Lefebvre V, Goffinet B, Chauvet JC, Caromel B, Signoret P, Brand R, Palloix A (2001) Evaluation of genetic distances between pepper inbred lines for cultivar protection purposes : comparison of AFLP, RAPD and phenotypic data. Theor Appl Genet 102: 741–750

    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 45:839–854

    Article  PubMed  CAS  Google Scholar 

  • Leonards-Schippers C, Gieffers W, Schafer-Pregl R, Ritter E, Knapp S, Salamini F, Gebhardt C (1994) Quantitative resistance to Phytophthora infestans in potato: a case study for QTL mapping in an allogamous plant species. Genetics 137:67–77

    PubMed  CAS  Google Scholar 

  • Li X, van Eck HJ, Rouppe van der Voort JNAM, Huigen DJ, Stam P, Jacobsen E (1998) Autotetraploids and genetic mapping using common AFLP markers: the R2 allele conferring resistance to Phytophthora infestans mapped on chromosome IV. Theor Appl Genet 96:1121–1128

    Article  CAS  Google Scholar 

  • Lincoln SE, Daly MJ, Lander ES (1993) Construction of a genetic linkage map with Mapmaker/Exp v3.0: a tutorial and reference manual. Technical report, Whitehead Institute, Cambridge

  • Melcher U (2000) SSCPs. http://www.opbs.okstate.edu/∼melcher/MG/MGW1/MG11129.html

  • Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8(2):129–134

    Article  PubMed  CAS  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8(11):1113–1130

    PubMed  CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed  CAS  Google Scholar 

  • Milligan S, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    Article  PubMed  CAS  Google Scholar 

  • Mueller LA, Giovannoni JJ, van Eck J, Stack S, Tanksley SD (2005) Tomato genome sequencing direct submission. Plant breeding and genetics, Cornell University, Emerson Hall, Ithaca

  • Orita M, Suzuki Y, Sekiva T, Hayashi K (1989) Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain. Genomics 5(4):874–879

    Article  PubMed  CAS  Google Scholar 

  • Paal J, Henselewski H, Muth J, Meksem K, Menendez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1–4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297

    Article  PubMed  CAS  Google Scholar 

  • Palloix A, Depestre T, Daubèze AM, Lafortune D, Nono Wodin R, Elamin AA, Duranton C (1998) Breeding multiresistant belle pepper for intertropical cultivation conditions: The LIRA program. In: Palloix A, Daunay MC (eds) Proceedings of the Xth Eucarpia meeting on genetics and breeding of Capsicum and eggplant, Avignon (France), September 7–11, 1998. INRA Montfavet, France, pp 65–69

  • Paran I, Rouppe van der Voort J, Lefebvre V, Jahn M, Landry L, van Schriek M, Tanyolac B, Caranta C, Ben Chaim A, Livingstone K, Palloix A, Peleman J (2004) An integrated genetic linkage map of pepper (Capsicum spp.). Mol Breed 13:251–261

    Article  CAS  Google Scholar 

  • Pegard A, Brizzard G, Fazari A, Soucaze O, Abad P, Djian-Caporalino C (2005) Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum L. Phytopathology 95(2):158–165

    CAS  Google Scholar 

  • 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 42:1100–1110

    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 103:920–929

    Article  CAS  Google Scholar 

  • Robbins TP, Carpenter R, Coen ES (1989) A chromosome rearrangement suggests that donor and recipient sites are associated during Tam3 transposition in Antirrhinum majus. EMBO J 8:5–13

    PubMed  CAS  Google Scholar 

  • Roberts PA, Dalmasso A, Cap GB, Castagnone-Sereno P (1990) Resistance in Lycopersicum peruvianum to isolates of Mi gene-compatible Meloidogyne populations. J Nematol 22:585–589

    Google Scholar 

  • Rouppe van der Voort J, Wolters P, Folkertsma R, Hutten R, van Zanvoort P, Vinke H, Kanyuka K, Bendahmane A, Jacobsen E, Janssen R, Bakker J (1997) Mapping of the cyst nematode resistance locus Gpa2 in potato using a strategy based on co-migrating AFLP markers. Theor Appl Genet 95:874–880

    Article  Google Scholar 

  • Sandbrik JM, Colon LT, Wolters PJCC, Stiekema WJ (2000) Two related genotypes of Solanum microdontum carry different segregating alleles for field resistance to Phytophthora infestans. Mol Breed 6:215–225

    Article  Google Scholar 

  • Schiex T, Chabrier P, Bouchez M, Milan D (2001) boosting em for radiation hybrid and genetic mapping. WABI 2001 (Workshop on Algorithms in Bioinformatics), LNCS, vol 2149

  • Sheperd KW, Mayo GME (1972) Genes conferring specific plant disease resistance. Science 175:375–380

    Article  Google Scholar 

  • Song WY, Bureau TE, Ronald PC (1998) Identification and characterization of 14 transposon-like elements in the noncoding regions of members of the Xa21 family of disease resistance genes in rice. Mol Gen Genet 258:449–456

    Article  PubMed  CAS  Google Scholar 

  • Staskawicz B (2004) Direct submission (16-JUL-2004) plant and microbial biology, U.C. Berkeley, 111 Koshland Hall, Berkeley

  • 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 56:137–145

    Article  CAS  Google Scholar 

  • Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Gen Genet 272(6):603–615

    CAS  Google Scholar 

  • Tai T, Staskawicz BJ (1999) Construction of a yeast artificial chromosome library of pepper (Capsicum annuum L.) and identification of clones from the Bs2 resistance locus. Theor Appl Genet 100:112–117

    Article  Google Scholar 

  • Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 96(24):14153–14158

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Röder MS, Wing RA, Wu W, Young ND (1992) High-density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    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 106:1473–1485

    PubMed  CAS  Google Scholar 

  • Thabuis A, Lefebvre V, Bernard G, Daubèze AM, Phaly T, Pochard E, Palloix A (2004) 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 

  • Thomas CM, Jones DA, English JJ, Carroll BJ, Bennetzen JL, Harrison K, Burbidge A, Bishop G, Jones JDG (1994) Analysis of the chromosomal distribution of transposon-carrying T-DNAs in tomato using the inverse polymerase chain reaction. Mol Gen Genet 242:573–585

    Article  PubMed  CAS  Google Scholar 

  • Van der Biezen E, Jones J (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:226–227

    Article  Google Scholar 

  • Van der Vossen EAG, van der Rouppe Voort JNAM, Kanyuka K, Bendahmane A, Sandbrink H, Baulcombe DC, Bakker J, Stiekema WJ, Klein-Lankhorst RM (2000) Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J 23:567–576

    Article  PubMed  Google Scholar 

  • Veremis JC, van Heusden AW, Roberts PA (1999) Mapping a novel heat-stable resistance to Meloidogyne in Lycopersicon esculentum. Theor Appl Genet 98:274–280

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, VanDelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new concept for DNA fingerprinting. Nucleic Acids Res 23(21):4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Yaghoobi J, Kaloshian I, Wen Y, Williamson VM (1995) Mapping a new nematode resistance locus in Lycopersicon peruvianum. Theor Appl Genet 91:457–464

    Article  CAS  Google Scholar 

  • Zijlstra C (2000) Identification of Meloidogyne chitwoodi, M. fallax and M. hapla based on SCAR-PCR: a powerful way of enabling reliable identification of populations or individuals that share common traits. Eur J Nematol 106:283–290

    CAS  Google Scholar 

  • Zijlstra C, Donkers-Venne THM, Fargette M (2000) Identification of Meloidogyne incognita, M. javanica and M. arenaria using sequence characterised amplified region (SCAR) based PCR assays. Nematology 2(8):847–853

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by a European grant as part of the ‘DREAM’ project (2000–2004) (EU-project QLRT-1999–1462 “DREAM”, Durable resistance against the quarantine soil-borne nematodes Meloidogyne chitwoodi and M. fallax, Website: http://www.eu-dream.nl). The various Capsicum accessions were obtained from the pepper germplasm collection of GAFL, INRA-Avignon (France). The authors would like to thank Daniel Esmenjaud and Marie-Noelle Rosso for critically reading the manuscript; Janice de Almeida Engler and Julie Sappa for substantially revising English usage; Anne-Marie Sage-Palloix for the use of pepper germplasm facilities; Ghislaine Nemouchi and Thérèse Phaly for generating the plant progenies and Nathalie Marteu for maintaining the various RKN populations and helping with resistance tests.

Author information

Authors and Affiliations

  1. INRA, UMR 1064 Interactions Plantes Microorganismes et Santé Végétale, BP167, F-06903, Sophia Antipolis, France

    C. Djian-Caporalino, A. Fazari, M. J. Arguel, T. Vernie, C. VandeCasteele, I. Faure, G. Brunoud, L. Pijarowski & P. Abad

  2. INRA, UR 1052 Génétique et Amélioration des Fruits et Légumes, BP94, F-84143, Montfavet , France

    A. Palloix & V. Lefebvre

Authors
  1. C. Djian-Caporalino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Fazari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. J. Arguel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Vernie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. VandeCasteele
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. I. Faure
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Brunoud
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. L. Pijarowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. Palloix
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. V. Lefebvre
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. P. Abad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Djian-Caporalino.

Additional information

Communicated by C. Gebhardt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Djian-Caporalino, C., Fazari, A., Arguel, M.J. et al. Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 114, 473–486 (2007). https://doi.org/10.1007/s00122-006-0447-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-006-0447-3

Keywords

Search

Navigation