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Mapping the black spot resistance locus Rdr3 in the shrub rose ‘George Vancouver’ allows for the development of improved diagnostic markers for DNA-informed breeding

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Abstract

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Rdr3 is a novel resistance gene of black spot in roses that maps to a chromosome 6 homolog. A new DNA test was developed and can be used to pyramid black spot resistance in roses.

Abstract

Diplocarpon rosae, the cause of rose black spot, is one of the most devastating foliar pathogens of cultivated roses (Rosa spp.). The primary method of disease control is fungicides, and they are viewed unfavorably by home gardeners due to potential environmental and health impacts. Planting rose cultivars with genetic resistance to black spot can reduce many of the fungicide applications needed in an integrated pest management system. To date, four resistance genes have been identified in roses (Rdr1, Rdr2, Rdr3, and Rdr4). Rdr3 was never mapped and is thought to be unique from Rdr1 and Rdr2. It is unknown whether it is an allele of Rdr4. To assess the novelty of Rdr3, a mapping population was created by crossing the Rdr3 containing cultivar George Vancouver with the susceptible cultivar Morden Blush. The mapping population was genotyped with the WagRhSNP 68 K Axiom array and mapped using the ‘polymapR’ package. Rdr3 was mapped to a chromosome 6 homolog confirming it is different from Rdr1 and Rdr2, found on chromosome 1, and from Rdr4, found on chromosome 5. The mapping information was used in conjunction with the Rosa chinensis genome assembly to develop new tightly linked SSRs for marker-assisted breeding. Three markers were able to predict the presence of Rdr3 in a 63-cultivar validation set. Additionally, 12 cultivars appear to have resistance genes other than Rdr3. The improved diagnostic markers will be a great asset to the rose-breeding community toward developing new black spot-resistant cultivars.

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References

  • Aliu O, Chung KC (2012) Assessing strength of evidence in diagnostic tests. Plast Reconstr Surg 129:989e–998e

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beier S, Thiel T, Münch T, Scholz U, Mascher M (2017) MISA-web: a web server for microsatellite prediction. Bioinformatics 33:2583–2585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292:2281–2285

    Article  PubMed  CAS  Google Scholar 

  • Bourke PM, Arens P, Voorrips RE, Esselink GD, Koning-Boucoiran CFS, van’t Westende WPC, Leonardo TS, Wissink P, Zheng C, van Geest G, Visser RGF, Krens FA, Smulders MJM, Maliepaard C (2017) Partial preferential chromosome pairing is genotype dependent in tetraploid rose. Plant J 90:330–343

    Article  PubMed  CAS  Google Scholar 

  • Bourke PM, van Geest G, Voorrips RE, Jansen J, Kranenburg T, Shahin A, Visser RGF, Arens P, Smulders MJM, Maliepaard C (2018) polymapR—linkage analysis and genetic map construction from F1 populations of outcrossing polyploids. Bioinformatics 34:3496–3502

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Byrne DH (2015) Advances in rose breeding and genetics in North America. Acta Hortic 1064:89–98

    Article  Google Scholar 

  • Debener T, Byrne DH (2014) Disease resistance breeding in rose: current status and potential of biotechnological tools. Plant Sci 228:107–117

    Article  PubMed  CAS  Google Scholar 

  • Dong Q, Wang X, Byrne DH, Ong K (2017) Characterization of partial resistance to black spot disease of Rosa sp. HortScience 52:49–53

    Article  Google Scholar 

  • Gachomo EW, Dehne HW, Steiner U (2006) Microscopic evidence for the hemibiotrophic nature of Diplocarpon rosae, cause of black spot disease of rose. Physiol Mol Plant Pathol 69:86–92

    Article  Google Scholar 

  • Gilmore BS, Bassil NV, Hummer KE (2011) DNA extraction protocols from dormant buds of twelve woody plant genera. J Am Pomolog Soc 65:201–206

    Google Scholar 

  • Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PMM (2003) The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 56:1129–1135

    Article  PubMed  Google Scholar 

  • Harp DA, Zlesak D, Hammond G, George S, Mackay W (2009) Earth-Kind® rose trials—identifying the world’s strongest, most beautiful landscape roses. Floric Ornam Biotechnol 3:166–175

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hibrand Saint-Oyant L, Ruttink T, Hamama L, Kirov I, Lakhwani D, Zhou NN, Bourke PM, Daccord N, Leus L, Schulz D, Vand de Geest H, Hesselink T, Van Laere K, Debray K, Balzergue S, Thouroude T, Chastellier A, Jeauffre J, Voisine L, Gaillard S, Borm TJA, Arens P, Voorrips RE, Maliepaard C, Neu E, Linde M, Le Paslier MC, Bérard A, Bounon R, Clotault J, Choisne N, Quesneville H, Kawamura K, Aubourg S, Sakr S, Smulders MJM, Schijlen E, Bucher E, Debener T, De Riek J, Foucher F (2018) A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat Plants 4:473–484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koning-Boucoiran CFS, Esselink GD, Vukosavijev M, van ‘t Westende WPC, Gitonaga VW, Krens FA, Voorrips RE, van de Weg WE, Schulz D, Debener T, Maliepaard C, Arens P, Smulders MJM (2015) Using RNA-Seq to assemble a rose transcriptome with more than 13,000 full-length expressed genes and to develop the WagRhSNP 68 k Axiom SNP array for rose (Rosa L.). Front Plant Sci 6:249

    Article  PubMed  PubMed Central  Google Scholar 

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  PubMed  CAS  Google Scholar 

  • Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Menz I, Straube J, Linde M, Debener T (2017) The TNL gene Rdr1 confers broad-spectrum resistance to Diplocarpon rosae. Mol Plant Pathol 19:1104–1113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ogilvie IS, Arnold NP (1995) ‘George Vancouver’ rose. HortScience 30:146

    Article  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:846–847

    Article  CAS  Google Scholar 

  • Preedy KF, Hackett CA (2016) A rapid marker ordering approach for high-density genetic linkage maps in experimental autotetraploid populations using multidimensional scaling. Theor Appl Genet 129:2117–2132

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Raymond O, Gouzy J, Just J, Badouin H, Verdenaud M, Lemainque A, Vergne P, Moja S, Choisne N, Pont C, Carrère S, Caissard J, Couloux A, Cottret L, Aury J, Szécsi Latrasse D, Madoui M, François L, Fu X, Yang S, Dubois A, Piola F, Larrieu A, Perez M, Labadie K, Perrier L, Govetto B, Labrousse Y, Villand P, Bardoux C, Bolz V, Lopez-Roques C, Heitzler P, Vernoux T, Vandenbussche M, Quesneville H, Boualem A, Bendahmane A, Liu C, Le Bris M, Salse J, Baudino S, Benhamed M, Wincker P, Bendahmane M (2018) The Rosa genome provides new insights into the domestication of modern roses. Nat Genet 50:772–777

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roberts AV, Gladis T, Brumme H (2009) DNA amounts of roses (Rosa L.) and their use in attributing ploidy levels. Plant Cell Rep 28:61–71

    Article  PubMed  CAS  Google Scholar 

  • Salinas NR, Zurn JD, Mathey M, Mookerjee S, Denoyes B, Perrotte J, Potier A, Finn CE, Hancock JF, Stewart P, Bassil NV (2017) Validation of molecular markers associated with perpetual flowering in octoploid Fragaria germplasm. Mol Breed 37:70

    Article  CAS  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  PubMed  CAS  Google Scholar 

  • Smulders MJM, Arens P, Koning-Boucoiran CFS, Gitonga VW, Krens FA, Atanassov A, Atanassov I, Rusanov KE, Bendahmane M, Dubois A, Raymond O, Caissard JC, Baudino S, Crespel L, Gudin S, Ricci SC, Kovatcheva N, Van Huylenbroeck J, Leus L, Wissemann V, Zimmermann H, Hensen I, Werlemark G, Nybom H (2011) Rosa. In: Kole C (ed) Wild crop relatives: genomic and breeding resources: plantation and ornamental crops. Springer, Berlin, pp 243–274

    Chapter  Google Scholar 

  • Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422

    Article  PubMed  CAS  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Voorrips RE, Gort G, Vosman B (2011) Genotype calling in tetraploid species from bi-allelic marker data using mixture models. BMC Bioinform 12:172

    Article  Google Scholar 

  • Waliczek TM, Byrne DH, Holeman DJ (2018) Opinions of landscape roses available for purchase and preferences for the future market. HortTechnology 28:807–814

    Article  Google Scholar 

  • Whitaker VM, Hokanson SC (2009) Partial resistance to black spot disease in diploid and tetraploid roses: general combining ability and implications for breeding and selection. Euphytica 169:421–429

    Article  Google Scholar 

  • Whitaker VM, Bradeen JM, Debener T, Biber A, Hokanson SC (2010a) 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

    Article  PubMed  CAS  Google Scholar 

  • Whitaker VM, Debener T, Roberts AV, Hokanson SC (2010b) A standard set of host differentials and unified nomenclature for an international collection of Diplocarpon rosae races. Plant Pathol 59:745–752

    Article  Google Scholar 

  • Xue AG, Davidson CG (1998) Components of partial resistance to black spot disease (Diplocarpon rosae Wolf) in garden roses. HortScience 33:96–99

    Article  Google Scholar 

  • Zlesak DC (2006) Rosa × hybrida L. In: Anderson NO (ed) Flower breeding and genetics: issues, challenges, and opportunities for the 21st century. Springer, Berlin, pp 695–738

    Google Scholar 

  • Zlesak DC, Whitaker VM, George S, Hokanson SC (2010) Evaluation of roses from the Earth-Kind® trials: black spot (Diplocarpon rosae Wolf) resistance and ploidy. HortScience 45:1779–1787

    Article  Google Scholar 

  • Zlesak DC, Clark A, Bradeen JM, Hokanson SC (2015) Determining the association of SCAR marker ND5E and resistance to race 8 of Diplocarpon rosae Wolf in a diverse group of landscape roses. Acta Hortic 1064:79–86

    Article  Google Scholar 

  • Zurn JD, Carter KA, Yin MH, Worthington M, Clark JR, Finn CE, Bassil N (2018a) Validating blackberry seedling pedigrees and developing an improved multiplexed microsatellite fingerprinting set. J Am Soc Hortic Sci 143:381–390

    Article  CAS  Google Scholar 

  • Zurn JD, Zlesak DC, Holen M, Bradeen JM, Hokanson SC, Bassil NV (2018b) Mapping a novel black spot resistance locus in the climbing rose Brite Eyes™ (‘RADbrite’). Front Plant Sci 9:1730

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank April Nyberg, Jaimie Green, Katie Pardee, Andy Sherwood, Sarah Kummeth, Drew Zagala, and Seth Heder for their technical support and Bailey Nurseries and Star® Roses and Plants for donating rose plants. The authors also would like to thank Mandie Driskill for technical support in testing the diagnostic markers.

Funding

This research was funded through the USDA’s National Institute of Food and Agriculture—Specialty Crop Research Initiative project, ‘RosBREED: Combining Disease Resistance and Horticultural Quality in New Rosaceous Cultivars’ (2014-51181-22378).

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Authors and Affiliations

  1. USDA-ARS National Clonal Germplasm Repository, Corvallis, OR, USA

    Jason D. Zurn & Nahla V. Bassil

  2. Department of Plant and Earth Science, University of Wisconsin-River Falls, River Falls, WI, USA

    David C. Zlesak

  3. Department of Horticulture, University of Minnesota, St. Paul, MN, USA

    Matthew Holen & Stan C. Hokanson

  4. Department of Plant Pathology, University of Minnesota, St. Paul, MN, USA

    James M. Bradeen

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  1. Jason D. Zurn
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  6. Nahla V. Bassil
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Contributions

JDZ conducted the analysis and wrote the manuscript. DCZ, MH, and SCH conceived the experiment, conducted the phenotypic assays, and maintained the plants. JMB provided laboratory space to conduct the phenotypic assays. NVB conceived the experiment and wrote the manuscript. All authors reviewed and edited the final manuscript.

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Correspondence to Nahla V. Bassil.

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Communicated by Albrecht E. Melchinger.

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Zurn, J.D., Zlesak, D.C., Holen, M. et al. Mapping the black spot resistance locus Rdr3 in the shrub rose ‘George Vancouver’ allows for the development of improved diagnostic markers for DNA-informed breeding. Theor Appl Genet 133, 2011–2020 (2020). https://doi.org/10.1007/s00122-020-03574-4

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