Advertisement

Tree Genetics & Genomes

, Volume 4, Issue 3, pp 469–479 | Cite as

Development of an STS map of an interspecific progeny of Malus

  • F. Fernández-Fernández
  • K. M. Evans
  • J. B. Clarke
  • C. L. Govan
  • C. M. James
  • S. Marič
  • K. R. Tobutt
Original Paper

Abstract

Simple sequence repeat (SSR) markers developed from Malus, as well as Prunus, Pyrus and Sorbus, and some other sequence-tagged site (STS) loci were analysed in an interspecific F1 apple progeny from the cross ‘Fiesta’ × ‘Totem’ that segregated for several agronomic characters. A linkage map was constructed using 259 STS loci (247 SSRs, four SCARs and eight known-function genes) and five genes for agronomic traits—scab resistance (Vf), mildew resistance (Pl-2), columnar growth habit (Co), red tissues (Rt) and green flesh background colour (Gfc). Ninety SSR loci and three genes (ETR1, Rt and Gfc) were mapped for the first time in apple. The transferability of markers from other Maloideae to Malus was found to be around 44%. The loci are spread across 17 linkage groups, corresponding to the basic chromosome number of Malus and cover 1,208 cM, approximately 85% of the estimated length of the apple genome. Interestingly, we have extended the top of LG15 with eight markers covering 25 cM. The average map density is 4.7 cM per marker; however, marker density varies greatly between linkage groups, from 2.5 in LG14 to 8.9 in LG7, with some areas of the genome still in need of further STS markers for saturation.

Keywords

Apple linkage map Microsatellite transferability Red tissue Ethylene 

Notes

Acknowledgements

The authors would like to thank Dr. A. Marchese for kindly providing Prunus SSR data and Dr. D.J. Sargent for the provision of ANS, DFR and PGLM data. Pome fruit genetics research at East Malling is supported by the UK Department for Environment, Food and Rural Affairs (Defra). S. Marič acknowledges the receipt of a grant from the British Council.

Supplementary material

11295_2007_124_MOESM1_ESM.doc (764 kb)
Table S1 Locus name, amplification method, allele sizes in the parents, segregation type and ratios (expected and observed), results for χ 2 goodness-of-fit test and linkage group of the Malus progeny from the cross ‘Fiesta’ × ‘Totem’ for all SSRs tested (764 KB).

References

  1. Alston FH, Briggs JB (1968) Resistance to Sappaphis devecta (Wlk) in apple. Euphytica 17:468–472CrossRefGoogle Scholar
  2. Alston FH, Watkins R (1975) Apple breeding at East Malling. Proceedings Eucarpia Symposium on Tree Fruit Breeding 1973, Canterbury, pp. 14–29Google Scholar
  3. Alston FH, Phillips KL, Evans KM (2000) A Malus gene list. Acta Hort 538:561–570Google Scholar
  4. Bošković R, Tobutt KR (1999) Correlation of stylar ribonuclease isoenzymes with incompatibility alleles in apple. Euphytica 107:29–43CrossRefGoogle Scholar
  5. Bouvier L, Lespinasse Y, Schuster M (2000) Karyotype analysis of an haploid plant of apple (Malus domestica). Acta Hort 538:321–324Google Scholar
  6. Broothaerts W (2003) New findings in apple S-genotype analysis resolve previous confusion and request the re-numbering of some S-alleles. Theor Appl Genet 106:703–714PubMedGoogle Scholar
  7. Castiglione S, Pirola B, Sala F, Ventura M, Pancaldi M, Sansavini S (1999) Molecular studies of ACC synthase and ACC oxidase genes in apple. Acta Hort 484:305–309Google Scholar
  8. Cevik V, King GJ (2002) High-resolution genetic analysis of the Sd-1 aphid resistance locus in Malus spp. Theor Appl Genet 105:346–354PubMedCrossRefGoogle Scholar
  9. Cheng FS, Weeden NF, Brown SK, Aldwinckle HS, Gardiner SE, Bus VG (1998) Development of a DNA marker for Vm, a gene conferring resistance to apple scab. Genome 41:208–214CrossRefGoogle Scholar
  10. Chevreau E, Lespinasse Y, Gallet M (1985) Inheritance of pollen enzymes and polyploid origin of apple (Malus × domestica Borkh). Theor Appl Genet 71:268–277Google Scholar
  11. Cipriani G, Lot G, Huang WG, Marrazzo MT, Peterlunger E, Testolin R (1999) AC/GT and AG/CT microsatellite repeats in peach (Prunus persica (L.) Batsch): isolation, characterization and cross-species amplification in Prunus. Theor Appl Genet 99:65–72CrossRefGoogle Scholar
  12. Costa F, Stella S, Van de Weg WE, Guerra W, Cecchinel M, Dallavia J, Koller B, Sansavini S (2005) Role of the genes Md-ACO1 and Md-ACS1 in ethylene production and shelf life of apple (Malus domestica Borkh). Euphytica 141:181–190CrossRefGoogle Scholar
  13. Dayton DF, Williams EB (1968) Independent genes in Malus for resistance to Venturia inaequalis. Proc Am Soc Hort Sci 92:89–94Google Scholar
  14. De La Rosa R, James CM, Tobutt KR (2002) Isolation and characterisation of polymorphic microsatellites in olive (Olea europaea L.) and their transferability to other genera in the Oleaceae. Mol Ecol Notes 2:265–267CrossRefGoogle Scholar
  15. Dirlewanger E, Cosson P, Tavaud M, Aranzana MJ, Poizat C, Zanetto A, Arus 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 105:127–138PubMedCrossRefGoogle Scholar
  16. Dirlewanger E, Graziano E, Joobeur T, Garriga-Calderé F, Cosson P, Howad W, Arús P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci U S A 101:9891–9896PubMedCrossRefGoogle Scholar
  17. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  18. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427PubMedCrossRefGoogle Scholar
  19. Evans KM, James CM (2003) Identification of SCAR markers linked to Pl-w mildew resistance in apple. Theor Appl Genet 106:1178–1183PubMedGoogle Scholar
  20. Fernández-Fernández F, Harvey NG, James CM (2006) Isolation and characterization of polymorphic microsatellite markers from European pear (Pyrus communis L). Mol Ecol Notes 6:1039–1041CrossRefGoogle Scholar
  21. Gessler C, Patocchi A, Sansavini S, Tartarini S, Gianfranceschi L (2006) Venturia inaequalis resistance in apple. Crit Rev Plant Sci 25:473–503CrossRefGoogle Scholar
  22. 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 93:199–204CrossRefGoogle Scholar
  23. Gianfranceschi L, Seglias N, Tarchini R, Komjanc M, Gessler C (1998) Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96:1069–1076CrossRefGoogle Scholar
  24. 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 94:249–254CrossRefGoogle Scholar
  25. Hemmat M, Weeden NF, Manganaris AG, Lawson DM (1994) Molecular marker linkage map for apple. J Heredity 85:4–11Google Scholar
  26. 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 122:347–349Google Scholar
  27. Hemmat M, Weeden NF, Brown SK (2003) Mapping and evaluation of Malus × domestica microsatellites in apple and pear. J Am Soc Hortic Sci 128:515–520Google Scholar
  28. Hokanson SC, Szewc-McFadden AK, Lamboy WF, McFerson JK (1998) Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus × domestica Borkh. core subset collection. Theor Appl Genet 97:671–683CrossRefGoogle Scholar
  29. Inoue E, Matsuki Y, Anzai H, Evans K (2007) Isolation and characterization of microsatellite markers in Japanese pear (Pyrus pyrifolia Nakai). Mol Ecol Notes 7:445–447CrossRefGoogle Scholar
  30. Kim MY, Song KJ, Hwang JH, Shin YU, Lee HJ (2003) Development of RAPD and SCAR markers linked to the Co gene conferring columnar growth habit in apple (Malus pumila Mill). J Hort Sci Biotech 78:512–517Google Scholar
  31. King GJ, Alston FH, Batlle I, Chevreau E, Gessler C, Janse J, Lindhout P, Manganaris AG, Sansavini S, Schmidt H, Tobutt K (1991) The ‘European Apple Genome Mapping Project’—developing a strategy for mapping genes coding for agronomic characters in tree species. Euphytica 56:89–94Google Scholar
  32. King GJ, Alston FH, Brown LM, Chevreau E, Evans KM, Dunemann F, Janse J, Laurens F, Lynn JR, Maliepaard C, Manganaris AG, Roche P, Schmidt H, Tartarini S, Verhaegh J, Vrielink R (1998) Multiple field and glasshouse assessments increase the reliability of linkage mapping of the Vf source of scab resistance in apple. Theor Appl Genet 96:699–708CrossRefGoogle Scholar
  33. Kobel F, Steinegger P, Anliker J (1939) Weitere Untersuchungen über die Befruchtungsverhältnisse der Apfel und Birnsorten Landwirtschaftliches Jahrbuch der Schweiz 53:160–191Google Scholar
  34. Knight RL, Alston FH (1968) Sources of field immunity to mildew (Podosphaera leucotricha) in apple. Can J Genet Cytol 10:294–298Google Scholar
  35. Lapins KO, Watkins R (1973) Genetics of compact growth. In: Annual report of the East Malling Research Station for 1972, East Malling Research Station, UK, p 136Google Scholar
  36. Lee S, Ross G, Gardner R (1998) An apple (Malus domestica L. Borkh cv Granny Smith) homologue of the ethylene receptor gene ETR1 (Accession No. AF032448) (PGR98-125). Plant Physiol 117:1126Google Scholar
  37. Lewis D, Crane MB (1938) Genetical studies in apples II. J Genet 37:119–128CrossRefGoogle Scholar
  38. 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 × domestica Borkh). Mol Breed 10:217–241CrossRefGoogle Scholar
  39. Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003) Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet 106:1497–1508PubMedGoogle Scholar
  40. 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 97:60–73CrossRefGoogle Scholar
  41. Mnejja M, Arús P (2006) Microsatellite transportability across Rosaceae crops. Proceedings of the 3rd International Rosaceae Genomics Conference, Napier, New Zealand, March 2006 OP37Google Scholar
  42. Naik S, Hampson C, Gasic K, Bakkeren G, Korban SS (2006) Development and linkage mapping of E-STS and RGA markers for functional gene homologues in apple. Genome 49:959–968PubMedCrossRefGoogle Scholar
  43. Oddou-Muratorio S, Aligon C, Decroocq S, Plomion C, Lamant T, Mush-Demesure B (2001) Microsatellite primers for Sorbus torminalis and related species. Mol Ecol Notes 1:297–299CrossRefGoogle Scholar
  44. Oraguzie CN, Iwanami H, Soejima J, Harada T, Hall A (2004) Inheritance of the Md-ACS1 gene and its relationship to fruit softening in apple (Malus × domestica Borkh). Theor Appl Genet 108:1526–1533PubMedCrossRefGoogle Scholar
  45. Pierantoni L, Cho KH, Shin IS, Chiodini R, Tartarini S, Dondini L, Kang SJ, Sansavini S (2004) Characterisation and transferability of apple SSRs to two European pear F1 populations. Theor Appl Genet 109:1519–1524PubMedCrossRefGoogle Scholar
  46. Raspé O, Kohn JK (2002) S-allele diversity in Sorbus aucuparia and Crataegus monogyna (Rosaceae: Maloideae). Heredity 88:458–465PubMedCrossRefGoogle Scholar
  47. Roche P, Alston FH, Maliepaard C, Evans KM, 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 (Sd-1) in apple. Theor Appl Genet 94:528–533CrossRefGoogle Scholar
  48. Sargent DJ, Rys A, Nier S, Simpson DW, Tobutt KR (2007) The development and mapping of functional markers in Fragaria and their transferability and potential for mapping in other genera. Theor Appl Genet 114:373–384PubMedCrossRefGoogle Scholar
  49. 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 × domestica Borkh.) genome. Tree Genet Genom 2:202–224CrossRefGoogle Scholar
  50. 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 118:183–186CrossRefGoogle Scholar
  51. 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 43:512–520PubMedCrossRefGoogle Scholar
  52. Tobutt KR (1984) Breeding columnar apple varieties at East Malling. Sci Hort 35:72–77Google Scholar
  53. Tobutt KR, Bošković R, Roche P (2000) Incompatibility and resistance to woolly aphid in apple. Plant Breed 119:65–69CrossRefGoogle Scholar
  54. Van Ooijen JW, Voorrips RE (2001) JoinMapÒ 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, the NetherlandsGoogle Scholar
  55. 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 123:321–326CrossRefGoogle Scholar
  56. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  57. Vowden CJ, Ridout MS, Tobutt KR (1995) LINKEM: a program for genetic linkage analysis. J Hered 86:249–250Google Scholar
  58. 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 124:129–137CrossRefGoogle Scholar
  59. 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 2:14–16CrossRefGoogle Scholar
  60. 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 106:9–18PubMedGoogle Scholar
  61. Yamamoto T, Kimura T, Saito T, Kotobuki K, Matsuta N, Liebhard R, Gessler C, Van de Weg WE, Hayashi T (2004) Genetic linkage maps of Japanese and European pears aligned to the apple consensus map. Acta Hort 663:51–56Google Scholar
  62. Yamamoto T, Kimura T, Sawamura Y, Nishitani C, Ohta S, Adachi Y, Hirabayashi T, Liebhard R, Gessler C, Van de Weg WE, Hayashi T (2005) Genetic linkage maps of European and Japanese pears. I: Proceedings of the Plant and Animal Genome Conference (Abstract) San Diego, California, p 510Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • F. Fernández-Fernández
    • 1
  • K. M. Evans
    • 1
  • J. B. Clarke
    • 1
  • C. L. Govan
    • 1
  • C. M. James
    • 1
  • S. Marič
    • 1
  • K. R. Tobutt
    • 1
  1. 1.East Malling Research (EMR)KentUK

Personalised recommendations