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Identification of SNPs linked to eight apple disease resistance loci

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Abstract

Although genetic and genomic studies have progressed to a very advanced level in apple, the application of this acquired knowledge for marker-assisted breeding (MAB) remains limited mainly to pyramiding monogenetically inherited resistances against apple scab, powdery mildew and fire blight. Crucial contributing reasons are the uncertainty in map position of some genes and the lack of tightly linked markers suitable for high-throughput analysis (HTA) that reduces the costs of MAB. Single-nucleotide polymorphism (SNP) markers have the potential to resolve these major issues. Here we present the refined map positions of the apple scab resistance genes Rvi2, Rvi4 and Rvi11, and the systematic search for SNPs associated with apple scab (Rvi2, Rvi4, Rvi6, Rvi11, Rvi15), powdery mildew (Pl2) and fire blight (FB_E and FB_MR5) resistances. With the aid of the ‘Golden Delicious’ sequence, several SNPs linked to each of the eight resistances were identified in the genomic regions around the resistance loci previously delimited by simple sequence repeat markers. The specificity of the alleles in coupling with the resistances was determined by screening eight apple genotypes, six of them being founding clones of modern apple cultivars. These SNPs can now be used to develop SNP-based HTA assays for MAB.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bassil N, Lewers K (2009) Genomics opportunities, new crops and new products. In: Folta KM, Gardiner SE (eds), Genetics and genomics of rosaceae, plant genetics and genomics: crops and models, 6:55–70

  • Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, Zhu J, Vinatzer BA, Gianfranceschi L, Gessler C, Sansavini S (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Natl Acad Sci USA 101:886–890

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Broggini GAL, Galli P, Parravicini G, Gianfranceschi L, Gessler C, Patocchi A (2009) HcrVf paralogs are present on linkage groups 1 and 6 of Malus. Genome 52:129–138

    Article  CAS  PubMed  Google Scholar 

  • Broggini GAL, Wöhner T, Fahrentrapp J, Kost TD, Flachowsky H, Peil A, Hanke V, Richter K, Patocchi A, Gessler C (2014) Engineering fire blight resistance into the apple cultivar ‘Gala’ using the FB_MR5 CC-NBS-LRR resistance gene of Malus × robusta 5. Plant Biotech J 12:728–733

  • Bus VGM, White A, Gardiner S, Weskett R, Ranatunga C, Samy A, Cook M, Rikkerink E (2002) An update on apple scab resistance breeding in New Zealand. Acta Hort 595:43–47

    Google Scholar 

  • Bus VGM, Rikkerink EHA, van de Weg WE, Rusholme RL, Gardiner SE, Basset HCM, Kodde LP, Parisi L, Laurens FND, Meulenbroek EJ, Plummer KM (2005) The Vh2 and Vh4 scab resistance genes in two differential hosts derived from Russian apple R12740-7A map to the same linkage group of apple. Mol Breed 15:103–116

    Article  CAS  Google Scholar 

  • Bus VGM, Chagné D, Bassett H, Bowatte D, Calenge F, Celton J-M, Durel C, Malone M, Patocchi A, Ranatunga A, Rikkerink E, Tustin D, Zhou J, Gardiner S (2008) Genome mapping of three major resistance genes to woolly apple aphid (Eriosoma lanigerum Hausm.). Tree Genet Genome 4:233–236

  • Bus VGM, Esmenjaud D, Buck E, Laurens F (2009) Application of genetic markers in rosaceous crop. In: Folta KM, Gardiner SE (eds), Genetics and genomics of rosaceae, plant genetics and genomics: crops and models, 6:563–599

  • Celton J-M, Tustin DS, Chagné D, Gardiner SE (2009) Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genet Genome 5:93–107

    Article  Google Scholar 

  • Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B Biol Sci 363:557–572

    Article  CAS  Google Scholar 

  • Fahrentrapp J, Broggini GAL, Kellerhals M, Peil A, Richter K, Zini E, Gessler C (2013) A candidate gene for fire blight resistance in Malus × robusta 5 is coding for a CC–NBS–LRR. Tree Genet Genome 9:237–251

    Article  Google Scholar 

  • Fernández-Fernández F, Antanaviciute L, van Dyk MM, Tobutt KR, Evans KM, Rees DJG, Dunwell JM, Sargent DJ (2012) A genetic linkage map of an apple rootstock progeny anchored to the Malus genome sequence. Tree Genet Genome 8:991–1002

    Article  Google Scholar 

  • Frey JE, Frey B, Sauer C, Kellerhals M (2004) Efficient low-cost DNA extraction and multiplex fluorescent PCR method for high-throughput marker-assisted selection (MAS) in apple breeding. Plant Breed 123:554–557

    Article  CAS  Google Scholar 

  • Galli P, Broggini GAL, Gessler C, Patocchi A (2010a) Phenotypic characterization of the Rvi15 (Vr2) apple scab resistance. J Plant Pathol 92:219–226

    Google Scholar 

  • Galli P, Broggini GAL, Kellerhals M, Gessler C, Patocchi A (2010b) High-resolution genetic map of the Rvi15 (Vr2) apple scab resistance locus. Mol Breed 26:561–572

    Article  Google Scholar 

  • Galli P, Patocchi A, Broggini GAL, Gessler C (2010c) The Rvi15 (Vr2) apple scab resistance locus contains three TIR–NBS–LRR genes. Mol Plant Microb Interact 23:608–617

    Article  CAS  Google Scholar 

  • Gardiner SE, Bus VGM, Rusholme RL, Chagne D, Rikkerink EHA (2007) Apple. In: Kole C (ed) Fruits and nuts. Berlin genome mapping and molecular breeding in plants 4. Springer, New York, pp 1–62

    Google Scholar 

  • Gardiner S, Norelli J, de Silva N, Fazio G, Peil A, Malnoy M, Horner M, Bowatte D, Carlisle C, Wiedow C, Wan Y, Bassett C, Baldo A, Celton J-M, Richter K, Aldwinckle H, Bus V (2012) Putative resistance gene markers associated with quantitative trait loci for fire blight resistance in Malus ‘robusta 5’ accessions. BMC Genet 13:25

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gianfranceschi L, Koller B, Seglias N, Kellerhals M, Gessler C (1996) Molecular selection in apple for resistance to scab caused by Venturia inaequalis. Theor Appl Genet 93:199–204

    Article  CAS  PubMed  Google Scholar 

  • Guilford P, Prakash S, Zhu JM, Rikkerink E, Gardiner S, Bassett H, Forster R (1997) Microsatellites in Malus × domestica (apple): abundance, polymorphism and cultivar identification. Theor Appl Genet 94:249–254

    Article  CAS  Google Scholar 

  • Gygax M, Gianfranceschi L, Liebhard R, Kellerhals M, Gessler C, Patocchi A (2004) Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor Appl Genet 109:1702–1709

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Zheng D, Vimolmangkang S, Khan MA, Beever JE, Korban SS (2011) Integration of physical and genetic maps in apple confirms whole-genome and segmental duplications in the apple genome. J Exp Bot 62:5117–5130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jänsch M, Frey JE, Hilber-Bodmer M, Broggini GAL, Weger J, Schnabel G, Patocchi A (2012) SSR marker analysis of Monilinia fructicola from Swiss apricots suggests introduction of the pathogen from neighboring countries and the United States. Plant Pathol 61:247–254. doi:10.1111/j.1365-3059.2011.02511.x

    Article  Google Scholar 

  • Koller B, Gianfranceschi L, Seglias N, McDermott J, Gessler C (1994) DNA markers linked to the Malus floribunda 821 scab resistance. Plant Mol Biol 26:597–602

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Chagné D, Bink MCAM, Volz RK, Whitworth C, Carlisle C (2012) Genomic selection for fruit quality traits in apple (Malus × domestica Borkh.). PLoS One 7(5):e36674. doi:10.1371/journal.pone.0036674

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laurens F, Durel C-E, Patocchi A, Peil A, Salvi S, Tartarini S, Velasco R, van der Weg E (2010) review on apple genetics and breeding programmes and presentation of a new European initiative to increase fruit breeding efficiency. J Fruit Sci 27:102–107

    Google Scholar 

  • Le Roux P-M, Flachowsky H, Hanke M-V, Gessler C, Patocchi A (2012) Use of a transgenic early flowering approach in apple (Malus × domestica Borkh.) to introgress fire blight resistance from cultivar Evereste. Mol Breed 30:857–874

    Article  Google Scholar 

  • Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterization of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 10:217–241

    Article  CAS  Google Scholar 

  • Micheletti D, Troggio M, Zharkikh A, Costa F, Malnoy M, Velasco R, Salvi S (2011) Genetic diversity of the genus Malus and implications for linkage mapping with SNPs. Tree Genet Genome 7:857–868

    Article  Google Scholar 

  • Noiton D, Shelbourne CJA (1992) Quantitative genetics in an apple breeding strategy. Euphytica 60:213–219

    Google Scholar 

  • Norelli JL, Farrell RE, Bassett CL, Baldo AM, Lalli DA, Aldwinckle HS, Wisniewski ME (2009) Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genet Genome 5:27–40

    Article  Google Scholar 

  • Parravicini G, Gessler C, Denance C, Lasserre-Zuber P, Vergne E, Brisset M-N, Patocchi A, Durel C-E, Broggini GAL (2011) Identification of serine/threonine kinase and nucleotide-binding site–leucine-rich repeat (NBS–LRR) genes in the fire blight resistance quantitative trait locus of apple cultivar ‘Evereste’. Mol Plant Pathol 12:493–505

    Article  CAS  PubMed  Google Scholar 

  • Patocchi A, Gianfranceschi L, Gessler C (1999a) Towards the map-based cloning of Vf: fine and physical mapping of the Vf region. Theor Appl Genet 99:1012–1017

    Article  CAS  Google Scholar 

  • Patocchi A, Vinatzer BA, Gianfranceschi L, Tartarini S, Zhang HB, Sansavini S, Gessler C (1999b) Construction of a 550 kb BAC contig spanning the genomic region containing the apple scab resistance gene Vf. Mol Gen Genet 262:84–891

    Article  Google Scholar 

  • Patocchi A, Frei A, Frey JE, Kellerhals M (2009) Towards improvement of marker assisted selection of apple scab resistant cultivars: Venturia inaequalis virulence surveys and standardization of molecular marker alleles associated with resistance genes. Mol Breed 24:337–347

    Article  CAS  Google Scholar 

  • Rezzonico F, Smits THM, Montesinos E, Frey JE, Duffy B (2009) Genotypic comparison of Pantoea agglomerans plant and clinical strains. BMC Microbiol 9:204–226

  • Rikkerink HA, Hilario-Andrade EM, Dare AP, Gardiner SE, Yoon M, Bus VGM (2007) Resistance gene and uses thereof. New Zealand Patent Application 563032, filed 31 Oct 2007

  • Roche P, Alston FH, Maliepaard C, Vrielink R, Dunemann F, Markussen T, Tartarini S, Brown LM, Ryder C, King GJ (1997) RFLP and RAPD markers linked to the rosy leaf curling aphid resistance gene (Sd1) in apple. Theor Appl Genet 94:528–533

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) PRIMER3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386

    Google Scholar 

  • Schouten HJ, Brinkhuis J, van der Burgh A, Schaart JG, Groenwold R, Broggini GAL, Gessler C (2014) Cloning and functional characterization of the Rvi15 (Vr2) gene for apple scab resistance. Tree Genet Genome 10:251–260

    Article  Google Scholar 

  • Silfverberg-Dilworth E, Matasci CL, Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genome 2:202–224

    Article  Google Scholar 

  • Tartarini S, Gianfranceschi L, Sansavini S, Gessler C (1999) Development of reliable PCR markers for the selection of the Vf gene conferring scab resistance in apple. Plant Breed 118:183–186

    Article  Google Scholar 

  • van Nocker S, Gardiner SE (2014) Breeding better cultivars, faster: applications of new technologies for the rapid deployment of superior horticultural tree crops Hortic Res 1, Article number: 14022 doi:10.1038/hortres.2014.22

  • van Ooijen JW (2006) JoinMap® 4.0, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839. doi:10.1038/ng.654

    Article  CAS  PubMed  Google Scholar 

  • Vinatzer BA, Patocchi A, Tartarini S, Gianfranceschi L, Sansavini S, Gessler C (2004) Isolation of two microsatellite markers from BAC clones of the Vf scab resistance region and molecular characterization of scab-resistant accessions in Malus germplasm. Plant Breed 123:321–326

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Dr. Elena Zini for the support in the development of the Rvi11 SSR markers. This work has been (partly) funded under the EU Seventh Framework Programme by the FruitBreedomics Project No. 265582: Integrated Approach for Increasing Breeding Efficiency in Fruit Tree Crop. The views expressed in this work are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission. The New Zealand component of the research was funded by the Plant and Food Research Pipfruit Core programme 1433.

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    Authors and Affiliations

    1. Agroscope, Institute for Plant Production Sciences, Phytopathology, 8820, Wädenswil, Switzerland

      Melanie Jänsch, Giovanni A. L. Broggini, Juliane Weger & Andrea Patocchi

    2. Plant Pathology Group, Swiss Federal Institute of Technology, Universitätstrasse 2, 8092, Zurich, Switzerland

      Giovanni A. L. Broggini & Juliane Weger

    3. The New Zealand Institute for Plant and Food Research Limited, Private Bag 1401, Havelock North, 4157, New Zealand

      Vincent G. M. Bus

    4. The New Zealand Institute for Plant and Food Research Limited, Private Bag 11600, Palmerston North, 4442, New Zealand

      Susan E. Gardiner & Heather Bassett

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    1. Melanie Jänsch
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    Correspondence to Andrea Patocchi.

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    Melanie Jänsch and Giovanni A. L. Broggini have equally contributed to this work.

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    11032_2015_242_MOESM3_ESM.tif

    Example of mapping of a SNP (SNP FBsnRvi2-7_Y536) associated with the resistance gene Rvi2 and verification of the level of specificity of the allele in coupling (T). The number of resistant, susceptible, and recombinants has been reduced to two for each type of progeny plant for graphical reason. TSR34T15: resistant parent; ‘Golden Delicious’: susceptible parent; ResPP: resistant progeny plant; SusPP: susceptible progeny plant; RecSusPP: susceptible recombinant progeny plant; RecResPP: resistant recombinant progeny plant; Genotypes from ‘Braeburn’ to ‘Jonathan’: founders tested to verify the specificity of the SNP allele associated with the resistance Rvi2. As ‘Cox’ Orange Pippin’ amplifies the allele in coupling with the Rvi2 resistance markers based on this SNP will not be 100% specific for this resistance gene (TIFF 261 kb)

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    Jänsch, M., Broggini, G.A.L., Weger, J. et al. Identification of SNPs linked to eight apple disease resistance loci. Mol Breeding 35, 45 (2015). https://doi.org/10.1007/s11032-015-0242-4

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