Skip to main content
SpringerLink
Log in

Rdr3, a novel locus conferring black spot disease resistance in tetraploid rose: genetic analysis, LRR profiling, and SCAR marker development

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

Abstract

Black spot disease of rose, incited by the fungus Diplocarpon rosae, is found worldwide and is the most important disease of garden roses. A gene-for-gene interaction in this pathosystem is evidenced by the presence of pathogenic races of D. rosae and the previous discovery of a dominant resistance allele at the Rdr1 locus in the diploid Rosa multiflora. The objective of the present study was to genetically analyze resistances to North American black spot races 3, 8, and 9 previously reported in tetraploid roses. Resistance to North American races 3 and 8 segregated 1:1 in multiple F1 populations, indicating that both are conferred by dominant alleles at single loci and are present in simplex (Rrrr) configuration. Gene pyramiding was demonstrated by combining both resistances into single genotypes. Resistance to race 9 was partial and segregated in a quantitative fashion. Analysis of these populations with microsatellite markers previously developed for Rdr1 revealed that the gene conferring race 3 resistance resides within the same R gene cluster as Rdr1. Race 8 resistance segregated independently and is, therefore, a novel locus for black spot resistance in rose which we have named Rdr3. NBS and LRR profiling were used in a bulked segregant analysis to identify a marker 9.1 cM from Rdr3, which was converted to a SCAR marker form for marker-assisted breeding.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  • Blechert O, Debener T (2005) Morphological characterization of the interaction between Diplocarpon rosae and various rose species. Plant Pathol 54:82–90

    Article  Google Scholar 

  • Burnham CR (1962) Discussions in cytogenetics. Burgess, Minneapolis

    Google Scholar 

  • Byrne DH, Black W, Ma Y (1996) The use of amphidiploidy in the development of blackspot resistant rose germplasm. Acta Hort 424:269–272

    Google Scholar 

  • Calenge F, Van der Linden CG, Van de Weg E, Schouten HJ, Van Arkel G, Denancé C, Durel CE (2005) Resistance gene analogues identified through the NBS profiling method map close to major genes and QTL for disease resistance in apple. Theor Appl Genet 110:660–668

    Article  CAS  PubMed  Google Scholar 

  • Chen XM, Line RF, Leung H (1998) Genome scanning for resistance-gene analogs in rice, barley, and wheat by high-resolution electrophoresis. Theor Appl Genet 97:345–355

    Article  CAS  Google Scholar 

  • Crute IR, Norwood JM (1986) Gene-dosage effects on the relationship between Bremia lactucae (downy mildew) and Lactuca sativa (lettuce): the relevance to a mechanistic understanding of host-parasite specificity. Physiol Mol Plant Pathol 29:133–145

    Google Scholar 

  • De Vries DP, Dubois LAM (2001) Developments in breeding for horizontal and vertical fungus resistance in roses. Acta Hort 552:103–112

    Google Scholar 

  • Debener T, Drewes-Alvarez R, Rockstroh K (1998) Identification of five physiological races of blackspot, Diplocarpon rosae Wolf, on roses. Plant Breed 117:267–270

    Article  Google Scholar 

  • Dobbs RB (1984) Research battles blackspot in roses. Am Rose Annu 69:44–54

    Google Scholar 

  • Gudin S (2000) Rose: genetics and breeding. Plant Breed Rev 17:159–189

    CAS  Google Scholar 

  • Hattendorf A, Debener T (2007) Molecular characterization of NBS-LRR-RGAs in the rose genome. Physiol Plant 129:775–786

    Article  CAS  Google Scholar 

  • Hattendorf A, Linde M, Mattiesch L, Kaufmann H, Debener T (2004) Genetic analysis of rose resistance genes and their localization in the rose genome. Acta Hort 651:123–130

    CAS  Google Scholar 

  • Haymes KM (1996) A DNA miniprep method suitable for a plant breeding program. Plant Mol Biol Rep 14:280–284

    Article  CAS  Google Scholar 

  • Hess G, Byrne DH, Zhang HB (2007) Toward positional cloning of everblooming gene (evb) in plants: a BAC library of Rosa chinensis cv. ‘Old Blush’. Acta Hort 751:169–174

    CAS  Google Scholar 

  • Horst RK, Cloyd R (2007) Compendium of rose diseases and pests, 2nd edn. APS Press, St. Paul

    Google Scholar 

  • Junghans DT, Alfenas AC, Brommonschenkel SH, Oda S, Mello EJ, Grattapaglia D (2003) Resistance to rust (Puccinia psidii Winter) in Eucalyptus: mode of inheritance and mapping of a major gene with RAPD markers. Theor Appl Genet 108:175–180

    Article  CAS  PubMed  Google Scholar 

  • Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann H, Mattiesch L, Lörz H, Debener T (2003) Construction of a BAC library of Rosa rugosa Thunb. and assembly of a contig spanning Rdr1, a gene that confers resistance to blackspot. Mol Genet Genomics 268:666–674

    CAS  PubMed  Google Scholar 

  • Leus L (2005) Resistance breeding for powdery mildew (Podosphaera pannosa) and black spot (Diplocarpon rosae) in roses. PhD Thesis, Faculty of Bioscience Engineering, Ghent University, Belgium

  • Mantovani P, Van der Linden G, Maccaferri M, Sanguineti MC, Tuberosa R (2006) Nucleotide-binding site (NBS) profiling of genetic diversity in durum wheat. Genome 49:1473–1480

    Article  CAS  PubMed  Google Scholar 

  • Mather K (1936) Segregation and linkage in autotetraploids. J Genet 32:287–314

    Article  Google Scholar 

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

    Article  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 detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, 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 

  • Soriano JM, Vilanova S, Romero C, Llácer G, Badenes ML (2005) Characterization and mapping of NBS-LRR resistance gene analogs in apricot (Prunus armeniaca L.). Theor Appl Genet 110:980–989

    Article  CAS  PubMed  Google Scholar 

  • Svejda FJ, Bolton AT (1980) Resistance of rose hybrids to three races of Diplocarpon rosae. Can J Plant Pathol 2:23–25

    Google Scholar 

  • Syed NH, Sorensen AP, Antonise R, Van de Wiel C, Van der Linden CG, van ‘t Westende W, Hooftman D, den Nijs H, Flavell AJ (2006) A detailed linkage map of lettuce based on SSAP, AFLP, and NBS markers. Theor Appl Genet 112:517–527

    Article  CAS  PubMed  Google Scholar 

  • Terefe D, Debener T (2009) Sequence analysis of BAC contigs spanning the resistance gene Rdr1 against black spot (Diplocarpon rosae) in roses. Plant and Animal Genomes XVII Conference, San Diego, USA (mtg. abstr.)

  • Van der Linden CG, Wouters D, Mihalka V, Kochieva E, Smulders M, Vosman B (2004) Efficient targeting of plant disease resistance loci using NBS profiling. Theor Appl Genet 109:384–393

    Article  PubMed  Google Scholar 

  • Von Malek B, Debener T (1998) Genetic analysis of resistance to blackspot (Diplocarpon rosae) in tetraploid roses. Theor Appl Genet 96:228–231

    Article  Google Scholar 

  • Von Malek B, Weber WE, Debener T (2000) Identification of molecular markers linked to Rdr1, a gene conferring resistance to blackspot in roses. Theor Appl Genet 101:977–983

    Article  Google Scholar 

  • Whitaker VM, Hokanson SC (2009) Breeding roses for disease resistance. In: Janick J (ed) Plant Breed Rev 31. Wiley, New York, pp 277–324

  • Whitaker VM, Zuzek K, Hokanson SC (2007) Resistance of twelve rose genotypes to fourteen isolates of Diplocarpon rosae (rose blackspot) collected from eastern North America. Plant Breed 126:83–88

    Article  Google Scholar 

  • Whitaker VM, Debener T, Roberts AV, Hokanson SC (2009) Unified nomenclature for an international collection of Diplocarpon rosae races and a standard host differential set (submitted)

  • Xu Q, Wen X, Deng X (2005) Isolation of TIR and nonTIR NBS-LRR resistance gene analogues and identification of molecular markers linked to a powdery mildew resistance locus in chestnut rose (Rosa roxburghii Tratt). Theor Appl Genet 111:819–830

    Article  CAS  PubMed  Google Scholar 

  • Yan Z, Denneboom C, Hattendorf A, Dolstra O, Debener T, Stam P, Visser B (2005) Construction of an integrated map of rose with AFLP, SSR, PD, RGA, RFLP, SCAR, and morphological markers. Theor Appl Genet 110:766–777

    Article  CAS  PubMed  Google Scholar 

  • Yokoya K, Kandasamy KI, Walker S, Mandegaran Z, Roberts AV (2000) Resistance of roses to pathotypes of Diplocarpon rosae. Ann Appl Biol 136:15–20

    Article  Google Scholar 

  • Zhang J, Yuan Y, Niu C, Hinchliffe DJ, Lu Y, Yu S, Percy RG, Ulloa M, Cantrell RG (2007) AFLP-RGA markers in comparison with RGA and AFLP in cultivated tetraploid cotton. Crop Sci 47:180–187

    Article  CAS  Google Scholar 

  • Zlesak DC, Thill CA, Anderson NO (2005) Trifluralin-mediated polyploidization in Rosa chinensis minima (Voss) Sims seedlings. Euphytica 141:281–290

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. David Zlesak for contributing expertise in rose germplasm resources and assistance with disease ratings and Dr. Ron Phillips for lending expertise with tetraploid segregation models. Thanks also to Ann-Katrin Lühmann for preparation and shipment of D. rosae isolates, Kathy Zuzek for assistance with controlled crosses and, Brandi Miatke for assistance with inoculations. This manuscript is Scientific Journal Series No. 091210185 of the Department of Horticultural Science, University of Minnesota and has been supported by the Minnesota Agricultural Experiment Station, the University of Minnesota Graduate School, and a National Science Foundation Central European Summer Research Institute fellowship.

Author information

Authors and Affiliations

  1. Department of Horticultural Science, Gulf Coast Research and Education Center, University of Florida, 14625 CR 672, Wimauma, FL, 33598, USA

    Vance M. Whitaker

  2. Department of Plant Pathology, University of Minnesota, 495 Borlaug Hall, 1991 Upper Buford Circle, St. Paul, MN, 55108, USA

    James M. Bradeen

  3. Institute of Plant Genetics, Leibniz University, Herrenhaeuser Strasse 2, 30419, Hannover, Germany

    Thomas Debener & Anja Biber

  4. Department of Horticultural Science, University of Minnesota, 1970 Folwell Ave., St. Paul, MN, 55108, USA

    Stan C. Hokanson

Authors
  1. Vance M. Whitaker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James M. Bradeen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Debener
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anja Biber
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stan C. Hokanson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stan C. Hokanson.

Additional information

Communicated by H. Nybom.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Whitaker, V.M., Bradeen, J.M., Debener, T. et al. Rdr3, a novel locus conferring black spot disease resistance in tetraploid rose: genetic analysis, LRR profiling, and SCAR marker development. Theor Appl Genet 120, 573–585 (2010). https://doi.org/10.1007/s00122-009-1177-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1177-0

Keywords

Search

Navigation