Skip to main content
Log in

Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Marker-assisted selection (MAS) offers quick and reliable prediction of the phenotypes of seedlings in large populations and thus opens new approaches for selection to breeders of apple (Malus x domestica Borkh.). The development of framework maps enables the discovery of genetic markers linked to desired traits. Although genetic maps have been reported for apple scion cultivars, none has previously been constructed for apple rootstocks. We report the construction of framework genetic maps in a cross between ‘M.9’ (‘Malling 9’) and ‘R.5’ (‘Robusta 5’) apple rootstocks. The maps comprise 224 simple sequence repeat (SSR) markers, 18 sequence-characterised amplified regions, 14 single nucleotide polymorphisms and 42 random amplified polymorphic DNAs. A new set of 47 polymorphic SSRs was developed from apple EST sequences and used for construction of this rootstock map. All 17 linkage groups have been identified and aligned to existing apple genetic maps. The maps span 1,175.7 cM (‘M.9’) and 1,086.7 cM (‘R.5’). To improve the efficiency of mapping markers to this framework map, we developed a bin mapping set. Applications of these new genetic maps include the elucidation of the genetic basis of the dwarfing effect of the apple rootstock ‘M.9’ and the analysis of disease and insect resistance traits such as fire blight (Erwinia amylovora), apple scab (Venturia inaequalis) and woolly apple aphid (Eriosoma lanigerum). Markers for traits mapped in this population will be of direct use to apple breeders for MAS and for identification of causative genes by map-based cloning.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aldwinckle HS, Beer SV (1979) Fire blight and its control. Hortic Rev 1:425–476

    Google Scholar 

  • Boudichevskaia A, Fischer C, Flachowsky H, Hanke V, Dunemann F (2004) Development of molecular markers for (Vr1, a scab resistance factor from R12740-7A apple. Acta Hort 663:171–176

    CAS  Google Scholar 

  • Bus V, 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, Chagné D, Bassett HCM, Bowatte D, Calenge F, Celton J-M, Durel CE, Malone MT, Patocchi A, Ranatunga AC, Rikkerink EHA, Tustin DS, Zhou J, Gardiner SE (2008) Genome mapping of three major resistance genes to woolly apple aphid (Eriosoma lanigerum Hausm.). Tree Genetics and Genomes 4:233–236

    Article  Google Scholar 

  • Calenge F, Faure A, Goerre M, Gebhardt C, Van de Weg E, Parisi L, Durel C-E (2004) Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379

    Article  PubMed  CAS  Google Scholar 

  • Calenge F, Drouet D, Denancé C, Van de Weg WE, Brisset M-N, Paulin J-P, Durel C-E (2005) Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135

    Article  PubMed  CAS  Google Scholar 

  • Chagné D, Carlisle CM, Blond C, Volz RK, Whitworth CJ, Oraguzie NC, Crowhurst RN, Allan AC, Espley RV, Hellens RP, Gardiner SE (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8:212

    Article  PubMed  Google Scholar 

  • Conner PJ, Brown SK, Weeden NF (1997) Randomly amplified polymorphic DNA-based genetic linkage maps of three apple cultivars. J Am Soc Hortic Sci 122:350–359

    CAS  Google Scholar 

  • Decroocq V, Favé MG, Hagen L, Bordenave L, Decroocq S (2003) Development and transferability of apricot and grape EST microsatellite markers across taxa. Theor Appl Genet 106:912–922

    PubMed  CAS  Google Scholar 

  • Dirlewanger E, Cosson P, Tavaud M, Aranzana M, Poizat C, Zanetto A, Arús P, Laigret F (2002) Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor Appl Genet 105:127–138

    Article  PubMed  CAS  Google Scholar 

  • FAO (2005) FAOSTAT database 2000. http://www.apps.fao.org/ (October 2007)

  • Fernández-Fernández F, Harvey NG, James CM (2006) Isolation and characterization of polymorphic microsatellite markers from European pear (Pyrus communis L.). Mol Ecol Notes 6:1039–1041

    Article  Google Scholar 

  • Gardiner S, Bus V, Bassett H, White A, Noiton D, Rikkerink E, Ball R, Forester R (1999) An updated genetic map around the Vf gene for resistance to apple scab and marker assisted selection for resistance. Acta Hort 484:481–485

    Google Scholar 

  • Gardiner S, Murdoch J, Meech S, Rusholme R, Bassett H, Cook M, Bus V, Rikkerink E, Gleave A, Crowhurst R, Ross G, Warrington I (2003) Candidate resistance genes from an EST database prove a rich source of markers for major genes conferring resistance to important apple pests and diseases. Acta Hort 622:141–151

    CAS  Google Scholar 

  • Gianfranceschi L, Seglias N, Tarchini R, Komjanc M, Gessler C (1998) Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96:1069–1076

    Article  CAS  Google Scholar 

  • Graham J, Smith K, MacKenzie K, Jorgenson L, Hackett C, Powell W (2004) The construction of a genetic linkage map of the red raspberry (Rubus idaeus subsp. idaeus) based on AFLPs, genomic-SSR and EST-SSR markers. Theor Appl Genet 109:740–749

    Article  PubMed  CAS  Google Scholar 

  • Guarino C, Santoro S, De Simone L, Lain O, Cipriani G, Testolin R (2006) Genetic diversity in a collection of ancient cultivars of apple (Malus x domestica Borkh.) as revealed by SSR-based fingerprinting. J Hortic Sci Biotechnol 81:39–44

    CAS  Google Scholar 

  • Guilford P, Prakash S, Zhu JM, Rikkerink E, Gardiner S, Basset H, Forster R (1997) Microsatellites in Malus x 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  PubMed  CAS  Google Scholar 

  • Hemmat M, Weeden NF, Conner PJ, Brown SK (1997) A DNA marker for columnar growth habit in apple contains a simple sequence repeat. J Am Soc Hortic Sci 122:347–349

    CAS  Google Scholar 

  • Hemmat M, Weeden NF, Brown SK (2003) Mapping and evaluation of Malus x domestica microsatellites in apple and pear. J Am Soc Hortic Sci 128:515–520

    CAS  Google Scholar 

  • Howad W, Yamamoto T, Dirlewanger E, Testolin R, Cosson P, Cipriani G, Monforte AJ, Georgi L, Abbott A, Arús P (2005) Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics 171:1305–1309

    Article  PubMed  CAS  Google Scholar 

  • Johnson E, Leonard JM, Zemetra RS, Riera-Lizarazu O (2007) Mapping the Compactum (C) locus in wheat. Plant and Animal Genome XIV Conference, San Diego, Poster 295

  • Kenis K, Keulemans J (2005) Genetic linkage maps of two apple cultivars (Malus x domestica Borkh.) based on AFLP and microsatellite markers. Mol Breed 15:205–219

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003) Creating a saturated reference map for the apple (Malus x domestica Borkh.) genome. Theor Appl Genet 106:1497–1508

    PubMed  CAS  Google Scholar 

  • Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73

    Article  CAS  Google Scholar 

  • Markussen T, Krüger J, Schmidt H, Dunemann F (1995) Identification of PCR-based markers linked to the powdery-mildew-resistance gene Pl 1 from Malus robusta in cultivated apple. Plant Breed 114:530–534

    Article  CAS  Google Scholar 

  • Monforte AJ, Arús P, Deleu W, González M, Fernández-Silva I, Moreno E, Puignomènech P, Blanca J, Nuez F, Picó B, Roig C, Garcia-MAS J (2007) Mapping melon ESTs by selective genotyping. Plant and Animal Genome XIV Conference, San Diego, Poster W96

  • Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with non repetitive DNA in plant genomes. Nat Genet 30:194–200

    Article  PubMed  CAS  Google Scholar 

  • Naik S, Hampson C, Gasic K, Bakkeren G, Korban SS (2006) Development and linkage mapping of E-STS and RGA markers for functional gene homologs in apple. Genome 49:959–968

    Article  PubMed  CAS  Google Scholar 

  • Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EHA, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, Laing WA, McArtney S, Nain B, Ross GS, Snowden KC, Souleyre EJF, Walton EF, Yauk YK (2006) Analysis of expressed sequence tags from apple. Plant Physiol 141:147–166

    Article  PubMed  Google Scholar 

  • Oddou-Muratorio S, Alignon C, Decroocq S, Plomion C, Lamant T, Mush-Demesure B (2001) Microsatellite primers for Sorbus torminalis and related species. Mol Ecol Notes 1:297–299

    Article  CAS  Google Scholar 

  • Peil A, Richter K, Garcia-Libreros T, Hanke M-V, Flachowsky H, Celton J-M, Horner M, Gardiner S, Bus V (2008) Confirmation of the fire blight QTL of Malus x robusta 5 on linkage group 3. Acta Horticulturae (in press)

  • 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, Totowa, NJ, pp 365–386

    Google Scholar 

  • Rusholme Pilcher RL, Celton J-M, Gardiner SE, Tustin DS (2008) Genetic markers linked to the dwarfing trait of apple rootstock ‘Malling 9’. J Am Soc Hortic Sci 133:100–106

    Google Scholar 

  • Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genetics and Genomes 2:202–224

    Article  Google Scholar 

  • Sosinski B, Gannavarapu M, Hager LD, Beck LE, King GJ, Ryder CD, Rajapakse S, Baird WV, Ballard RE, Abbott AG (2000) Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 101:421–428

    Article  CAS  Google Scholar 

  • Tanksley SD, Young ND, Paterson AH, Bonierbale MW (1989) RFLP mapping in plant breeding: new tools for an old science. Biotechnology 7:257–264

    Article  CAS  Google Scholar 

  • Testolin R, Marrazzo T, Cipriani G, Quarta R, Verde I, Dettori MT, Pancaldi M, Sansavini S (2000) Microsatellite DNA in peach [Prunus persica (L.) Batsch] and its use in fingerprinting and testing the genetic origin of cultivars. Genome 43:512–520

    Article  PubMed  CAS  Google Scholar 

  • Van Dyk MM, Koning G, Simayi Z, Booi S, Maharaj R, Selada MC, Rees DJG (2005) Development of microsatellite markers for marker-assisted breeding in pears (Pyrus spp.). Acta Horticulturae 671:307–313

    Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMapR 3.0: software for the calculation of genetic linkage maps. Wageningen, The Netherlands

    Google Scholar 

  • Vision TJ, Brown DG, Shmoys DB, Durrett RT, Tanksley SD (2000) Selective mapping: a strategy for optimizing the construction of high-density linkage maps. Genetics 155:407–420

    PubMed  CAS  Google Scholar 

  • Webster AD, Wertheim SJ (2003) Apple rootstocks. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CABI Publishing, CAB International

    Google Scholar 

  • Yamamoto T (2007) Marker information submitted via the DNA data bank of Japan and NCBI

  • Yamamoto T, Kimura T, Sawamura Y, Kotobuki K, Ban Y, Hayashi T, Matsuta N (2001) SSRs isolated from apple can identify polymorphism and genetic diversity in pear. Theor Appl Genet 102:865–870

    Article  CAS  Google Scholar 

  • Yamamoto T, Kimura T, Sawamura Y, Manabe T, Kotobuki K, Hayashi T, Ban Y, Matsuta N (2002a) Simple sequence repeats for genetic analysis in pear. Euphytica 124:129–137

    Article  CAS  Google Scholar 

  • Yamamoto T, Kimura T, Shoda M, Ban Y, Hayashi T, Matsuta N (2002b) Development of microsatellite markers in the Japanese pear (Pyrus pyrifolia Nakai). Mol Ecol Notes 2:14–16

    Article  CAS  Google Scholar 

  • Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002c) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18

    PubMed  CAS  Google Scholar 

  • Yamamoto T, Kimura T, Saito T, Kotobuki K, Matsuta N, Liebhard R, Gessler C, Van de Weg E, Hayashi T (2004) Genetic linkage maps of Japanese and European pears aligned to the apple consensus map. Acta Horticulturae 663:51–56

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Toshiya Yamamoto for providing Pyrus SSR primer sequences prior to deposition in the public database. This work was partially supported by the New Zealand Foundation for Research, Science and Technology, contract no. CO6X0205.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. E. Gardiner.

Additional information

Communicated by O. Savolainen

Rights and permissions

Reprints and permissions

About this article

Cite this article

Celton, JM., Tustin, D.S., Chagné, D. et al. Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genetics & Genomes 5, 93–107 (2009). https://doi.org/10.1007/s11295-008-0171-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-008-0171-z

Keywords

Navigation