Skip to main content
SpringerLink
Log in

Identification of non-TIR-NBS-LRR markers linked to the Pl5/Pl8 locus for resistance to downy mildew in sunflower

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

Abstract

The resistance of sunflower, Helianthus annuus L., to downy mildew, caused by Plasmopara halstedii, is conferred by major genes denoted by Pl. Using degenerate and specific primers, 16 different resistance gene analogs (RGAs) have been cloned and sequenced. Sequence comparison and Southern-blot analysis distinguished six classes of RGA. Two of these classes correspond to TIR-NBS-LRR sequences while the remaining four classes correspond to the non-TIR-NBS-LRR type of resistance genes. The genetic mapping of these RGAs on two segregating F2 populations showed that the non-TIR-NBS-LRR RGAs are clustered and linked to the Pl5/Pl8 locus for resistance to downy mildew in sunflower. These and other results indicate that different Pl loci conferring resistance to the same pathogen races may contain different sequences.

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

  • Aarts MGM, te Lintel Hekkert B, Holub ED, Beynon JL, Stiekema WJ, Pereia A (1998) Identification of R-gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana. Mol Plant–Microbe Interact 11:251–258

    Google Scholar 

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

    PubMed  Google Scholar 

  • Bent AF (1996) Plant disease resistance gene-function meets structure. Plant Cell 8:1757–1771

    CAS  Google Scholar 

  • Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860

    CAS  PubMed  Google Scholar 

  • Bert PF, Tourvieille de Labrouhe D, Philippon J, Mouzeyar S, Jouan I, Nicolas P, Vear F (2001) Identification of a second linkage group carrying genes controlling resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 103:992–997

    Article  CAS  Google Scholar 

  • Bert PF, Jouan I, Tourvieille de Labrouhe D, Serre F, Nicolas P, Vear F (2002) Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.). 1. QTLs involved in resistance to Sclerotinia sclerotiorum and Diaporthe helianthi. Theor Appl Genet (in press)

  • Bouzidi MF, Badaoui S, Cambon F, Vear F, Tourvieille de Labrouhe D, Nicolas P, Mouzeyar S (2002) Molecular analysis of a major locus for resistance to downy mildew in sunflower with specific PCR-based markers. Theor Appl Genet 104:592–600

    Article  Google Scholar 

  • Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant–Microbe Interact 11:968–978

    Google Scholar 

  • Donald TM, Pellerone F, Adam-Blondon AF, Bouquet A, Thomas MR, Dry LB (2002) Identification of resistance gene analogs linked to the powdery mildew resistance locus in grapevine. Theor Appl Genet 104:610–618

    CAS  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    Google Scholar 

  • Feuillet C, Schachermayr G, Keller B (1997) Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. Plant J 11:45–52

    CAS  PubMed  Google Scholar 

  • Flor HH (1955) Host-parasite interaction in flax rust: its genetics and other implications. Phytopathology 45:680–685

    Google Scholar 

  • Gedil MA, Slabaugh MB, Berry S, Johnson R, Michelmore R, Miller J, Gulya T, Knapp SJ (2001a) Candidate disease resistance genes in sunflower cloned using conserved nucleotide-binding site motifs: genetic mapping and linkage to the downy mildew resistance gene Pl1. Genome 44:205–212

    Article  CAS  PubMed  Google Scholar 

  • Gedil MA, Wye C, Berry S, Segers B, Peleman J, Jones R, Leon A, Slabaugh MB, Knapp SJ (2001b) An integrated restriction fragment length polymorphism-amplified fragment length polymorphism linkage map for cultivated sunflower. Genome 44:213–221

    CAS  PubMed  Google Scholar 

  • Gentzbittel L, Mouzeyar S, Badaoui S, Mestries E, Vear F, Tourvieille de Labrouhe D, Nicolas P (1998) Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L. Theor Appl Genet 96:519–525

    CAS  Google Scholar 

  • Gentzbittel L, Mestries E, Mouzeyar S, Mazeyrat F, Badaoui S, Vear F, Tourvieille de Labrouhe D, Nicolas P (1999) A composite map of expressed sequences and phenotypic traits of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet 99:218–234

    Article  CAS  Google Scholar 

  • Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846

    CAS  PubMed  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1997) Plant disease resistance genes. Annu Rev Plant Physiol Mol Biol 48:575–607

    Google Scholar 

  • Hayes AJ, Saghai Maroof MA (2000) Targeted resistance gene mapping in soybean using modified AFLPs. Theor Appl Genet 100:1279–1283

    Article  CAS  Google Scholar 

  • Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11,746–11,750

    Article  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 1:174–181

    CAS  PubMed  Google Scholar 

  • Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7:1195–1206

    CAS  PubMed  Google Scholar 

  • Lawson WR, Goulter KC, Henry RJ, Kong GA, Kochman JK (1998) Marker-assisted selection for two rust resistance genes in sunflower. Mol Breed 4:227–234

    Article  CAS  Google Scholar 

  • Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nature Genet 14:421–429

    CAS  PubMed  Google Scholar 

  • Martin GB (1999) Functional analysis of plant disease genes and their downstream effectors. Curr Opin Plant Biol 2:273–279

    CAS  PubMed  Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Pecherer RM, Sivaramakrishnan S, Sobral B, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide binding super family. Plant J 20:317–332

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW (1995a) Isolation of disease resistance genes from crop plants. Curr Opin Biotechnol 6:145–152

    Article  CAS  Google Scholar 

  • Michelmore RW (1995b) Molecular approaches to manipulation of disease resistance genes. Annu Rev Phytopathol 15:393–727

    Article  Google Scholar 

  • Michelmore RW (2000) Genomic approaches to plant disease resistance. Curr Opin Plant Biol 3:125–131

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Miller JF, Gulya TJ (1991) Inheritance of resistance to race 4 of downy mildew derived from interspecific crosses in sunflower. Crop Sci 31:40–43

    Google Scholar 

  • Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The A. thaliana disease-resistance gene RPS2 encodes a protein containing a nucleotide binding site and leucine-rich repeats. Cell 78:1089–1099

    CAS  PubMed  Google Scholar 

  • Mouzeyar S, Tourvieille de Labrouhe D, Vear F (1993) Histopathological studies of resistance of sunflower (Helianthus annuus L.) to downy mildew (Plasmopara halstedii). J Phytopathol 139:289–297

    Google Scholar 

  • Mouzeyar S, Tourvieille de Labrouhe D, Vear F (1994) Effect of host-race combination on resistance of sunflower (Helianthus annuus L.) to downy mildew (Plasmopara halstedii). J Phytopathol 141:249–258

    Google Scholar 

  • Mouzeyar S, Roeckel-Drevet P, Gentzbittel L, Philippon J, Tourvieille de Labrouhe D, Vear F, Nicolas P (1995) RFLP and RAPD mapping of the sunflower Pl1 locus for resistance toPlasmopara halstedii race 1. Theor Appl Genet 91:733–737

    CAS  Google Scholar 

  • Nicholas KB, Nicholas HB, Deerfield, DW (1997) EMBnet News 4: 14

    Google Scholar 

  • Ohmori T, Murata M, Motoyoshi F (1998) Characterization of disease resistance gene-like sequences in near-isogenic lines of tomato. Theor Appl Genet 96:331–338

    CAS  Google Scholar 

  • Parker JE, Coleman MJ (1997) Molecular intimacy between proteins specifying plant–pathogen recognition. Trends Biochem Sci 22:291–296

    Article  CAS  PubMed  Google Scholar 

  • Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniels MJ (1996) Characterization of eds 1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8:2033–2046

    Article  CAS  PubMed  Google Scholar 

  • Parniske M, Wulff BB, Bonnema G, Thomas CM, Jones DA, Jones JD (1999) Homologues of the Cf-9 disease resistance gene (Her9s) are present at multiple loci on the short arm of tomato chromosome 1. Mol Plant Microbe Interact 12:93–102

    CAS  PubMed  Google Scholar 

  • Penuela S, Danesh D, Young ND (2002) Targeted isolation, sequence analysis, and physical mapping of non-TIR NBS-LRR genes in soybean. Theor Appl Genet 104:261–272

    Article  Google Scholar 

  • Roeckel-Drevet P, Gagne G, Mouzeyar S, Gentzbittel L, Philippon J, Nicolas P, Tourvieille de Labrouhe D, Vear F (1996) Colocation of downy mildew (Plasmopara halstedii) resistance genes in sunflower (Helianthus annuus L.). Euphytica 91:225–228

    CAS  Google Scholar 

  • Saghai Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Sci USA 81:8014–8018

    Google Scholar 

  • Shen KA, Keyers BC, Islam-Faridi MN, Chin DB, Stelly DM, Michelmore RW (1998) Resistance gene candidate identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce. Mol Plant–Microbe Interact 11:815–823

    Google Scholar 

  • Speulman E, Bouchez D, Holub ED, Beynon JL (1998) Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana. Plant J 14:467–474

    CAS  PubMed  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker Bj, Ellis JG, Jones JDG (1995) Molecular genetics of plant disease resistance. Science 268:661–667

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgens DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  PubMed  Google Scholar 

  • Vear F, Gentzbittel L, Philippon J, Mouzeyar S, Mestries E, Roeckel-Drevet P, Tourvieille de Labrouhe D, Nicolas P (1997) The genetics of resistance to five races of downy mildew (Plasmopara halstedii). Theor Appl Genet 95:584–589

    Article  Google Scholar 

  • Vear F, Philippon J, Roche S, Walser P, Tourvieille de Labrouhe D, Mouzeyar S, Nicolas P (2000) Genetical analysis of the sunflower downy mildew resistance gene Pl5. 15th Int Sunflower Conf, Toulouse-France, pp 53–66

  • Vranceanu V, Stoenescu F (1970) Immunity to sunflower downy mildew due to a single dominant gene. Probleme Agric 22:34–40

    Google Scholar 

  • Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of tobacco mosaic virus resistance gene N: similarity to Toll and interleukin-1 receptor. Cell 78:1101–1115

    CAS  PubMed  Google Scholar 

  • Yu Yg, Buss GR, Saghai Maroof MA (1996) Isolation of the super family of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc Natl Acad Sci USA 93:11,751–11,756

    Article  Google Scholar 

  • Yu JK, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring MJ, Soper J, Han F, Chu WC, Webb DM, Thompson L, Edwards KJ, Berry S, Leon A, Olungu C, Maes N, Knapp SJ (2002) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci (in press)

Download references

Acknowledgements

We thank F.Cambon, S.Roche and P.Walser for their technical assistance. The first author thanks the Egyptian Ministry of Higher Education for a Doctoral Scholarship. This study was supported by PROMOSOL. Some equipment was financed by a state-region grant "Qualité des Aliments".

Author information

Authors and Affiliations

  1. UMR 1095 INRA-UBP "Amélioration et Santé des Plantes", Université Blaise Pascal, 24, Avenue des Landais 63177 Aubiére Cedex, France

    O. Radwan, M.F. Bouzidi, P. Nicolas & S. Mouzeyar

  2. UMR 1095 INRA-UBP "Amélioration et Santé des Plantes", INRA, 234, avenue du Brézet 63039 Clermont Ferrand Cedex 02, France

    F. Vear, J. Philippon & D. Tourvieille de Labrouhe

Authors
  1. O. Radwan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M.F. Bouzidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Vear
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Philippon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. Tourvieille de Labrouhe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Nicolas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Mouzeyar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Mouzeyar.

Additional information

Communicated by C. Möllers

Rights and permissions

Reprints and permissions

About this article

Cite this article

Radwan, O., Bouzidi, M., Vear, F. et al. Identification of non-TIR-NBS-LRR markers linked to the Pl5/Pl8 locus for resistance to downy mildew in sunflower. Theor Appl Genet 106, 1438–1446 (2003). https://doi.org/10.1007/s00122-003-1196-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-003-1196-1

Keywords

Search

Navigation