Skip to main content

Advertisement

Log in

Development of PCR markers for the Pl5/Pl8 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC-NBS-LRR sequences

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

Abstract

Sunflower downy mildew, caused by Plasmopara halstedii, is one of the major diseases of this crop. Development of elite sunflower lines resistant to different races of this oomycete seems to be the most efficient method to limit downy mildew damage. At least two different gene clusters conferring resistance to different races of P. halstedii have been described. In this work we report the cloning and mapping of two full-length resistance gene analogs (RGA) belonging to the CC-NBC-LRR class of plant resistance genes. The two sequences were then used to develop 14 sequence tagged sites (STS) within the Pl5/Pl8 locus conferring resistance to a wide range of P. halstedii races. These STSs will be useful in marker-assisted selection programs.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2A, B
Fig. 3a–h

Similar content being viewed by others

References

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

  • Ballvora A, Ercolano MR, Welis J, Meksem K, Bormann CA, Oberbagemann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30:361–371

    Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Girauda 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, Tourvielle 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 

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

    Google Scholar 

  • Bittner-Eddy P, Crute IR, Holub EB, Beynon JL (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J 21:177–188

    Article  CAS  PubMed  Google Scholar 

  • Bogorad L, Gubbins EJ, Krebbers E, Larrinua IM, Mulligan BJ, Muskavitch KMT, Orr EA, Rodermel SR, Schantz R, Steinmetz AA, de Vos G, Ye YK (1983) Cloning and physical mapping of maize plastid genes. Methods Enzymol 97:524–554

    CAS  Google Scholar 

  • Bouzidi MF, Badaoui S, Cambon F, Vear F, Tourvielle 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 

  • Brunner S, Keller B, Feuillet C (2000) Molecular mapping of the Rph7.g leaf rust resistance gene in barley (Hordeum vulgare L.). Theor Appl Genet 101:783–788

    Article  CAS  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 (2001) 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 

  • Gentzbittel L, Mestries E, Mouzeyar S, Mazeyrat F, Badaui 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

    CAS  Google Scholar 

  • Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193

    Article  CAS  PubMed  Google Scholar 

  • Hehl R, Faurie E, Hesselbach J, Salamini F, Whitham S, Barker B, Gebhardt C (1999) TMV resistance gene N homologues are linked to Synchytrium endobioticum resistance in potato. Theor Appl Genet 98:379–386

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jones DA, Thomas CM, Hammond-Kosack KE, Balintkurti PJ, Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793

    CAS  PubMed  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 

  • 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

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

    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 to 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 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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 halistedii). J Phytopathol 141:249–258

    Google Scholar 

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

    Google Scholar 

  • Ori N, Eshed Y, Paran I, Presting G, Aviv D, Tanksley S, Zamir D, Fluhr R (1997) The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leuciene-rich repeat superfamily of plant resistance genes. Plant Cell 9:521–532

    CAS  PubMed  Google Scholar 

  • Pan QL, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    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

    Google Scholar 

  • Radwan O, Bouzidi MF, Vear F, Philippon J, Tourvieille de Labrouhe D, Nicolas P, Mouzeyar S (2003) Identification of non-TIR-NBS-LRR markers linked to PL5/PL8 locus for resistance to downy mildew in sunflower. Theor Appl Genet 106:1438–1446

    CAS  PubMed  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 

  • Sato S, Nakmura Y, Kaneko T, Katoh T, Asamizu E, Tabata S (2000) Structural analysis of Arabidopsis thaliana chromosome 3 1. Sequence features of the regions of 4,504,864 bp covered by 60 P1 and TAC clones. DNA Res 7:131–135

    CAS  PubMed  Google Scholar 

  • Sela-Burrlage MB, Budai-Hadrian O, Pan Q, Carmel-Goren L, Vunsch R, Zamir D, Fluhr R (2001) Genome wide dissection of Fusarium resistance in tomato reveals multiple complex loci. Mol Genet Genomics 265:1104–1111

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OF, Lavelle DO, Wroblewski T, Meyers BG, Michelmore RW (2002) Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol Plant Microbe Interact 3:251–261

    Google Scholar 

  • Song WY, Xang GL, Chen LL (1995) A receptor kinase-like protein encoded by the rice resistance gene, Xa21. Science 270:1804–1806

    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 

  • Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics 162:381–394

    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 

  • Williams CE, Wang B, Holsten TE, Scambray J, de Assis Goes da Silva F, Ronald PC (1996) Markers for selection of rice Xa21 disease resistance gene. Theor Appl Genet 93:1119–1122

    Article  CAS  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 (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387

    CAS  Google Scholar 

Download references

Acknowledgements

The first author thanks the Egyptian Ministry of Higher Education for a Doctoral Scholarship. We thank F. Vear and D. Tourvieille de Labrouhe for critical reading of the manuscript and PROMOSOL for financial support.

Author information

Authors and Affiliations

Authors

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.F., Nicolas, P. et al. Development of PCR markers for the Pl5/Pl8 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC-NBS-LRR sequences. Theor Appl Genet 109, 176–185 (2004). https://doi.org/10.1007/s00122-004-1613-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1613-0

Keywords

Navigation