Advertisement

Apple Structural Genomics

  • Schuyler S. Korban
  • Stefano Tartarini
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 6)

A primary focus of apple genetics is the elucidation of genes influencing diverse phenotypes of economically important horticultural traits. Most of these phenotypes are genetically complex; i.e., controlled by multiple genes occupying chromosomal positions referred to as quantitative trait loci (QTL). Mapping of QTLs has become a common first step toward understanding the molecular basis of complex genetic traits, and it has provided the impetus for developing detailed genome maps. These genome maps are built with the aid of various biochemical and molecular markers such as isozymes, restriction fragment length polymorphisms (RFLPs), random amplified polymorphic DNAs (RAPDs), amplified fragment length polymorphisms (AFLPs), and simple sequence repeats (SSRs), among others. Dominant markers, such as RAPDs, can be used for map alignment if these markers are heterozygous in both parents, but their transferability to other maps is limited. While, co-dominant markers such as SSRs are also useful in map alignment, but they are also transferable between mapping populations. More recently, single nucleotide polymorphisms (SNPs) have taken hold as SNPs can occur in both coding (gene) and noncoding regions of the genome. Those SNPs found within a coding sequence are of particular interest as they are more likely to alter the biological function of a protein. SNPs are major contributors to genetic variation, comprising approximately 80% of all know polymorphisms, and their density in plants is variable depending on the species, while in the human genome it is estimated to be on average of 1 per 1000 base pairs. Although SNPs are mostly biallelic (less informative than short tandem repeats), they are more frequent and mutationally stable, making them suitable for association studies in which linkage disequilibrium (LD) between markers and an unknown variant is used to map mutations in complex traits. SNP maps will help in identifying multiple genes associated with such complex traits influencing tree architecture, fruit quality, and disease resistance. These associations are difficult to establish with conventional gene-hunting methods because a single altered gene may only be a small contributor to such a trait.

Keywords

Quantitative Trait Locus RAPD Marker Scar Marker Apple Cultivar Scab Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alston, F.H. (1977) Practical aspects of breeding for mildew (Podosphaera leucotricha) resistance in apples. Proc. VII Eucarpia Fruit Section Symp., Top Fruit Breeding, Wageningen, 1976: 4–13Google Scholar
  2. Alston, F.H. (1983) Progress in transferring mildew (Podosphaera leucotricha) resistance from Malus species to cultivated apple. IOBC/WPRS Bull. 6: 87–95Google Scholar
  3. Alston, F.H., and J.B. Briggs (1970) Inheritance of hypersensitivity to rosy apple aphid Dysaphis plantaginea in apple. Can. J. Genet. Cytol. 12:257–258Google Scholar
  4. Alston, F.H., K.L. Phillips, K.M. Evans (2000) A Malus gene list. Acta Hortic. 538: 561–570Google Scholar
  5. Baldi, P., A. Patocchi, E. Zini, C. Toller, R. Velasco, and M. Komjanc (2004) Cloning and linkage mapping of resistance gene homologues in apple. Theor. Appl. Genet. 109:231–239PubMedCrossRefGoogle Scholar
  6. Batlle, I., and F.H. Alston (1996) Genes determining leucine aminopeptidase and mildew resistance from the ornamental apple, ‘White Angel’. Theor. Appl. Genet. 93:179–182CrossRefGoogle Scholar
  7. Belfanti, E., E. Silfverberg-Dilworth, S. Tartarini, A. Patocchi, M. Barbieri, J. Zhu, B.A. Vinatzer, L. Gianfranceschi, C. Gessler, and S. Sansavini (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. USA 101: 886–890PubMedCrossRefGoogle Scholar
  8. Bink, M.C.A.M., P. Uimari, M.J. Sillanpää, L.L.G. Janss, and R.C. Jansen (2002) Multiple QTL mapping in related plant populations via a pedigree-analysis based approach. Theor. Appl. Genet. 104: 751–762PubMedCrossRefGoogle Scholar
  9. Bink, M., R. Voorrips, E. Van de Weg, and H. Jansen (2007) Statistical tools for QTL mapping in multiple, pedigreed populations. Eucarpia XII Fruit Section Symposium, September 16–20, 2007, Zaragoza, Spain: 59Google Scholar
  10. Boudichevskaia, A., H. Flachowsky, C. Fischer, V. Hanke, and F. Dunemann (2004) Development of molecular markers for Vr1, a scab resistance factor from R12740-7A apple. Acta Hort. 663:171–176Google Scholar
  11. Boudichevskaia, A., H. Flachowsky, A. Peil, C. Fischer, and F. Dunemann (2006) Development of a multiallelic SCAR marker for the scab resistance gene Vr1/Vh4/Vx from R12740-7A apple and its utility for molecular breeding.Tree Genet. Genomes 2: 186–195Google Scholar
  12. Bournival, B.L. and S.S. Korban (1987) Electrophoretic analysis of genetic variability in the apple. Scient. Hort. 31:233–243CrossRefGoogle Scholar
  13. Bus V., C. Ranatunga, S. Gardiner, H. Bassett, and E. Rikkerink (2000) Marker assisted selection for pest and disease resistance in the New Zealand apple breeding programme. Acta Hort. 538: 541–547Google Scholar
  14. Bus, V., A. White, S. Gardiner, R. Weskett, C. Ranatunga, A. Samy, M. Cook, and E. Rikkerink (2002) An update on apple scab resistance breeding in New Zealand. Acta Hort. 595:43–47Google Scholar
  15. Bus, V.G.M., E.H.A. Rikkerink, W.E. van de Weg, R.L. Rusholme, S.E. Gardiner, H.C.M. Bassett, L.P. Kodde, L. Parisi, F.N.D. Laurens, E.J. Meulenbroek, and K.M. Plummer (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. 15:103–116CrossRefGoogle Scholar
  16. Bus, V.G.M., D. Chagné, H.C.M. Bassett, D. Bowatte, F. Calenge, J.M. Celton, C.E. Durel, M.T. Malone, A. Patocchi, A.C. Ranatunga, E.H.A. Rikkerink, D.S. Tustin, J. Zhou, and S.E. Gardiner (2007) Genome mapping of three major resistance genes to woolly apple aphid (Eriosoma lanigerum Hausm.). Tree Genet. Genomes DOI10.1007/s11295-007-0103-3Google Scholar
  17. Caffier, V. and F. Laurens (2005) Breakdown of Pl2, a major gene for resistance to apple powdery mildew, in a French experimental orchard. Plant Pathol. 54: 116–124CrossRefGoogle Scholar
  18. Calenge, F., A. Faure, M. Goerre, C. Gebhardt, W. E. Van de Weg, L. Parisi, and C.-E. Durel (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. Phytoapthology 94: 370–379CrossRefGoogle Scholar
  19. Calenge, F., C.G. van der Linden, W.E. van de Weg, H.J. Schouten, G. Van Arkel, C. Denancé, and C.E. Durel (2005a) Resistance gene analogues identified through the NBS-profiling method map close to major genes and QTL for disease resistance in apple. Theor. Appl. Genet. 110:660–668Google Scholar
  20. Calenge, F., D. Drouet, C. Denancé, W.E. Van de Weg, M.N. Brisset, J.P. Paulin, and C.E. Durel (2005b) 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. 111:128–135Google Scholar
  21. Calenge, F. and C.E. Durel (2006) Both stable and unstable QTLs for resistance to powdery mildew are delected in apple afler four years of field assessments. Molecular Breed. 17: 329–339CrossRefGoogle Scholar
  22. Cevik, V. and G.J. King (2002a) High-resolution genetic analysis of the Sd1 aphid resistance locus in Malus spp. Theor. Appl. Genet. 105: 346–354Google Scholar
  23. Cevik, V. and G.J. King (2002b) Resolving the aphid resistance locus Sd1 on a BAC contig within a sub-telomeric region of Malus linkage group 7. Genome 45: 939–945Google Scholar
  24. Chagné, D., C.M. Carlisle, C. Blond, R.K. Volz, C.J. Whitworth, N.C. Oraguzie, R.N. Crowhurst, A.C. Allan, R.V. Espley, R.P. Hellens, and S.E. Gardiner (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genomics 8: 212. doi: 10.1186/1471-2164-8-212 Chandonia, J.-M. and S.E. Brenner (2006) The impact of structural genomics: expectations and outcomes. Science 311: 347–351PubMedCrossRefGoogle Scholar
  25. Cheng F.S., N.F. Weeden, and S.K. Brown (1996) Identification of co-dominant RAPD markers tightly linked to fruit skin color in apple. Theor. Appl. Genet. 93:222–227CrossRefGoogle Scholar
  26. Cheng, F.S., N.F. Weeden, S.K. Brown, H.S. Aldwinckle, S.E. Gardiner, and V.G. Bus (1998) Development of a DNA marker for Vm, a gene conferring resistance to apple scab. Genome 41:208–214CrossRefGoogle Scholar
  27. Chevreau, E., Y. Lespinasse, and M. Gallet (1985) Inheritance of pollen enzymes and polyploidy origin of apple (Malus x domestica). Theor. Appl. Genet. 71:268–277Google Scholar
  28. Chyi, Y.S. and N.F. Weeden (1984) Relative isozyme band intensities permit the identification of the 2n gamete parent of triploid apple cultivars. HortScience 19:818–819Google Scholar
  29. Conner, P.J., S.K. Brown, and N.F. Weeden (1997) Randomly amplified polymorphic DNA-based genetic linkage maps of three apple cultivars. J. Am. Soc. Hort. Sci. 122: 350–359Google Scholar
  30. Conner, P.J., S.K. Brown, and N.F. Weeden (1998) Molecular-marker analysis of quantitative traits for growth and development in juvenile apple trees. Theor. Appl. Genet. 96:1027–1035CrossRefGoogle Scholar
  31. Costa, F., S. Stella, W.E. Van de Weg, W. Guerra, M. Cecchinel, J. Dallavia, B. Koller, and S. Sansavini (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
  32. Costes, E., P.É. Lauri, and J. L. Regnard (2006) Implications for Tree Management and Fruit Production. Horticultural Reviews, J. Janick (ed), John Wiley & Sons, 32: 1–61Google Scholar
  33. Crane, M.B., R.M. Greenslade, A.M. Massee, and H.M. Tydemans (1936) Studies on the resistance and immunity of apples to the wooly apple aphid, Eriosoma lanigerum (Hausm.). J. Pomol. Hortic. Sci. 14: 137–163Google Scholar
  34. Cummings, J.N., P.L. Forsline, and J.D. Mackenzie (1981) Woolly apple aphid colonization on Malus cultivars. J. Am. Soc. Hortic. Sci. 106: 26–30Google Scholar
  35. Dayton, D.F. (1977) Genetic immunity to apple mildew incited by Podosphaera leucotricha. HortScience 12:225–226Google Scholar
  36. Dirlewanger, E., P. Cosson, M. Tavaud, M. Aranzana, C. Poizat, A. Zanetto, P. Arús, and F. Laigret (2002) Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry. Theor. Appl. Genet. 105: 127–138PubMedCrossRefGoogle Scholar
  37. Dunemann, F., G. Bräcker, T. Markussen, and P. Roche (1999) Identification of molecular markers for the major mildew resistance gene Pl2 in apple. Acta Hort 484:411–416Google Scholar
  38. Dunemann, F., C. Fischer, B. Merkt, M. Thiermann, and A. Urbanietz (2000) Molecular approaches for breeding apple cultivars with durable powdery mildew resistance. Durable Resistance Symposium, Wageningen, SP26Google Scholar
  39. Dunemann, F., A. Urbanietz, S. Gardiner, H. Bassett, W. Legg, R. Rusholme, V. Bus, and C. Ranatunga (2004) Marker assisted selection for Pl-1 powdery mildew resistance in apple – old markers for a new resistance gene? Acta Hort. 663:757–762Google Scholar
  40. Dunemann, F., A. Peil, A. Urbanietz, and T. Garcia-Libreros (2007) Mapping of the apple powdery mildew resistance gene Pl1 and its genetic association with an NBS-LRR candidate resistance gene. Plant Breed. 126: 476–481CrossRefGoogle Scholar
  41. Durel, C.-E., L. Parisi, F. Laurens, E. van de Weg, R. Liebhard, B. Koller, and M.F. Jourjon (2003) Genetic dissection of partial resistance against two monoconidial strains of the new race 6 of Venturia inaequalis in apple. Genome 46:224–234PubMedCrossRefGoogle Scholar
  42. Durham, R.E. and S.S. Korban (1994) Evidence of gene introgression in apple using RAPD markers. Euphytica 79: 109–114CrossRefGoogle Scholar
  43. Evans, K.M. and C.M. James (2003) Identification of SCAR markers linked to Pl-w mildew resistance in apple. Theor. Appl. Genet. 106:1178–1183PubMedGoogle Scholar
  44. Evans, K.M., F. Fernández, F. Laurens, L. Feugey, and W.E. Van de Weg (2007) Harmonising fingerprinting protocols to allow comparisons between germplasm collections. Eucarpia XII Fruit Section Symposium, September 16–20, 2007, Zaragoza, Spain: 57–58Google Scholar
  45. Gallot, J.C., R.C. Lamb, and H.S. Aldwinkle (1985) Resistance to powdery mildew from some small fruited Malus cultivars. HortScience 20: 1085–1087Google Scholar
  46. Gao, Z.S., W.E. van de Weg, J.G. Schaart, I.M. van der Meer, L. Kodde, M. Laimer, H. Breiteneder, K. Hoffmann-Sommergruber, L.J.W.J. Gilissen (2005a) Linkage map positions and allelic diversity of two Mal d 3 (non-specific lipid transfer protein) genes in the cultivated apple (Malus domestica). Theor. Appl. Genet. 110: 479–491Google Scholar
  47. Gao, Z.S., W.E. van de Weg, J.G. Schaart, H.J. Schouten, D.H. Tran, L.P. Kodde, I.M. van der Meer, A.H.M. van der Geest, J. Kodde, H. Breiteneder, K. Hoffmann-Sommergruber, D. Bosch, L.J.W.J. Gilissen (2005b) Genomic cloning and linkage mapping of the Mal d 1 (PR-10) gene family in apple (Malus domestica). Theor. Appl. Genet. 111: 171–183Google Scholar
  48. Gao, Z.S., W.E. van de Weg, J.G. Schaart, G. van Arkel, H. Breiteneder, K. Hoffmann-Sommergruber, L.J.W.J. Gilissen (2005c) Genomic characterization and linkage mapping of the apple allergen genes Mal d 2 (thaumatin-like protein) and Mal d 4 (profilin). Theor. Appl. Genet. 111: 1087–1097Google Scholar
  49. Gardener, R.G., J. N. Cummins, and H.S. Aldwinckle, (1980) Inheritance of fire blight resistance in Malus in relation to rootstock breeding. J. Am. Soc. Hortic. Sci. 105: 912–916Google Scholar
  50. Gardiner, S.E., H.C.M. Bassett, D.A.M. Noiton, V.G. Bus, M.E. Hofstee, A.G. White, R.D. Ball, R.L. Forster, and E.H.A. Rikkerink (1996a) A detailed linkage map around an apple scab resistance gene demonstrates that class 3A and 3B progeny both carry the Vf gene. Theor. Appl. Genet. 93:485–493Google Scholar
  51. Gardiner, S.E., H.C.M. Bassett, C. Madie, and D.A.M. Noiton (1996b) Isoenzyme, RAPD and RFLP markers used to deduce a putative parent for the apple cv. Braeburn. J. Amer. Soc. Hort. Sci. 121:996–1001Google Scholar
  52. Gardiner, S., J. Murdoch, S. Meech, R. Rusholme, H. Bassett, M. Cook, V. Bus, E. Rikkerink, A. Gleave, R. Crowhurst, G. Ross, and I. Warrington (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: 141–151Google Scholar
  53. Gessler, C., A. Patocchi,  S. Sansavini,  S. Tartarini, and L. Gianfranceschi (2006) Venturia inaequalis Resistance in Apple. Critical Rev. Plant Sci. 25: 473–503CrossRefGoogle Scholar
  54. Gianfranceschi, L., B. Koller, N. Seglias, M. Kellerhals, and C. Gessler (1996) Molecular selection in apple for resistance to scab caused by Venturia inaequalis. Theor. Appl. Genet. 93:199–204CrossRefGoogle Scholar
  55. Gianfranceschi, L., N. Seglias, R. Tarchini, M. Komjanc, and C. Gessler (1998) Simple sequence repeats for the genetic analysis of apple. Theor. Appl. Genet. 96: 1069–1076CrossRefGoogle Scholar
  56. Gilissen, L., S. Bolhaar, C. Matos, G. Rouwendal, M. Boone, F. Krens, L. Zuidmeer, A. van Leeuwen, J. Akkerdaas, and K. Hoffmann-Sommergruber (2005) Silencing the major apple allergen Mal d 1 by using the RNA interference approach.  J. Allergy Clin Immunol 115: 364–369PubMedCrossRefGoogle Scholar
  57. Guilford, P., S. Prakash, J.M. Zhu, E. Rikkerink, S. Gardiner, H. Bassett, and R. Forster (1997) Microsatellites in Malus X domestica (apple): abundance, polymorphism and cultivar identification. Theor. Appl. Genet. 94:249–254CrossRefGoogle Scholar
  58. Gygax, M., L. Gianfranceschi, R. Liebhard, M. Kellerhals, C. Gessler, and A. Patocchi (2004) Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackii. Theor. Appl. Genet. 109: 1702–1709PubMedCrossRefGoogle Scholar
  59. Han, Y., K. Gasic, F. Sun, M.L. Xu, and S.S. Korban (2007a) A gene encoding starch branching enzyme I (SBEI) in apple (Malus × domestica Rosaceae) and its phylogenetic relationship to Sbe genes from other angiosperms. Mol. Phylogenet. Evol. 43: 852–863Google Scholar
  60. Han, Y., E. Bendik, F. Sun, K. Gasic, and S.S. Korban (2007b) Genomic isolation of genes encoding starch branching enzyme II (SBEII) in apple: Towards characterization of evolutionary disparity in SbeII genes between monocots and eudicots. Planta 226:1265–1276Google Scholar
  61. Han, Y., K. Gasic, and S.S. Korban (2007c) Multiple-copy cluster-type organization and evolution of genes encoding O-methyltransferases in apple. Genetics 176: 2625–2635Google Scholar
  62. Han, Y., K. Gasic, B. Marron, J.E. Beever, and S.S. Korban (2007d) A BAC-based physical map of the apple genome. Genomics 89: 630–637Google Scholar
  63. Han, Y. and S.S. Korban (2007) Spring: A novel family of miniature inverted-repeat transposable elements in the apple genome. Genomics 90:195–200PubMedCrossRefGoogle Scholar
  64. Harada, T., K. Matsukawa, T. Sato, R. Ishikawa, M. Niizeki, and K. Saito (1993) DNA RAPDs detect genetic variation and paternity in Malus. Euphytica 65:87–91CrossRefGoogle Scholar
  65. Hemmat, M., N.F. Weeden, A.G. Manganaris, and D.M. Lawson (1994) Molecular marker linkage map for apple. J. Hered. 85:4–11PubMedGoogle Scholar
  66. Hemmat, M., N.F. Weeden, P.J. Conner, and S.K. Brown (1997) A DNA marker for columnar growth habit in apple contains a simple sequence repeat. J. Amer. Soc. Hort. Sci. 122: 347–349Google Scholar
  67. Hemmat, M., N.F. Weeden, H.S. Aldwinckle, and S.K. Brown (1998) Molecular markers for the scab resistance (V f) region in apple. J. Amer. Soc. Hort. Sci. 123: 992–996Google Scholar
  68. Hemmat, M., S.K. Brown, and N.F. Weeden (2002) Tagging and mapping scab resistance genes from R12740-7A apple. J. Amer. Soc. Hort. Sci. 127:365–370Google Scholar
  69. Hemmat, M., S.K. Brown, H.S. Aldwinckle, and N.F. Weeden (2003) Identification and mapping of markers for resistance to apple scab from ‘Antonovka’ and ‘Hansen’s baccata #2’. Acta Hort. 622:153–161Google Scholar
  70. Hokanson S.C., A.K. Szewc-McFadden, W.F. Lamboy, and J.R. McFerson (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
  71. Hokanson S.C., W.F. Lamboy, A.K. Szewc-McFadden, and J.R. McFerson (2001) Microsatellite (SSR) variation in a collection of Malus (apple) species and hybrids. Euphytica, 118: 281–294CrossRefGoogle Scholar
  72. Howad, W., T. Yamamoto, E. Dirlewanger, R. Testolin, P. Cosson, G. Cipriani, A.J. Monforte, L. Georgi, A.G. Abbott,and P. Arús (2005) Mapping With a Few Plants: Using Selective Mapping for Microsatellite Saturation of the Prunus Reference. Genetics 171: 1305–1309PubMedCrossRefGoogle Scholar
  73. Huaracha, E.M., M.L. Xu, K. Gasic, E. Pauwels, A. Van den Putte, J.W. Keulemans, and S.S. Korban (2004) Phenotypic reaction and genetic analysis using AFLP-derived SCARs for resistance to apple scab. J. Phytopathol. 152: 260–266CrossRefGoogle Scholar
  74. Ishikawa, S., S. Kato, S. Imakawa, T. Mikami, and Y. Shimamoto (1992) Organelle DNA polymorphism in apple cultivars and rootstocks. Theor. Appl. Genet. 83: 963–967CrossRefGoogle Scholar
  75. James, C.M., J.B. Clarke, and K.M. Evans (2004) Identification of molecular markers linked to the mildew resistance gene Pl-d in apple. Theor. Appl. Genet. 110:175–181PubMedCrossRefGoogle Scholar
  76. Janick, J., J.N. Cummins, S.K. Brown, and M. Hemmat (1996) Apples. In: Janick, J. and J.N. Moore (eds) Fruit Breeding: Tree and Tropical Fruits. Vol I. John Wiley, New York, USA, pp 1–77Google Scholar
  77. Kellerhals, M., E. Dolega, B. Koller, and C. Gessler (2000a) Advances in marker-assisted apple breeding. Acta Hort. 538: 535–540Google Scholar
  78. Kellerhals, M., L. Gianfranceschi, N. Seglias, and C. Gessler (2000b) Marker-assisted selection in apple breeding. Acta Hort. 521:255–265Google Scholar
  79. Kenis K., and J. Keulemans (2004) QTL analysis of growth characteristics in apple. Acta Hortic. 663: 369–374Google Scholar
  80. Kenis, K., and J. Keulemans (2005) Genetic linkage maps of two apple cultivars (Malus x domestica Borkh.) based on AFLP and microsatellite markers. Mol. Breed. 15:205–219CrossRefGoogle Scholar
  81. Kenis, K., and J. Keulemans (2007) Study of tree architecture of apple (Malus × domestica Borkh.) by QTL analysis of growth traits. Mol. Breed. 19: 193–208CrossRefGoogle Scholar
  82. Khan, M.A., B. Duffy, C. Gessler. and A. Patocchi (2006) QTL mapping of fire blight resistance in apple. Mol. Breed. 17: 299–306CrossRefGoogle Scholar
  83. Khan, M.A., C.E. Durel, B. Duffy, D. Drouet, M. Kellerhals, C. Gessler, and A. Patocchi, (2007) Development of molecular markers linked to the ‘Fiesta’ linkage group 7 major QTL for fire blight resistance and their application for marker-assisted selection. Genome 50: 568–577PubMedCrossRefGoogle Scholar
  84. Knight, R.L. and F.H. Alston (1968) Sources of field immunity to mildew (Podosphaera leucotricha) in apple. Can. J. Genet. Cytol. 10:294–298Google Scholar
  85. Knight, R.L., J.B. Briggs, A.M. Massee. and H.M. Tydeman (1962) The inheritance of resistance to woolly aphid, Eriosoma lanigerum (Hsmnn.), in the apple. J. Hort. Sci. 37:207–218Google Scholar
  86. Koller, B., A. Lehmann, J.M. McDermott, and C. Gessler (1993) Identification of apple cultivars using RAPD markers. Theor. Appl. Genet. 85: 901–904CrossRefGoogle Scholar
  87. Koller, B., L. Gianfranceschi, N. Seglias, J. McDermott, and C. Gessler (1994) DNA markers linked to Malus floribunda 821 scab resistance. Plant Mol. Biol. 26:597–602PubMedCrossRefGoogle Scholar
  88. Korban, S.S. and D.F. Dayton (1983) Evaluation of Malus germplasm for resistance to powdery mildew. HortScience 18:219–220Google Scholar
  89. Lawson, D.M., M. Hemmat, and N. Weeden (1995) The use of molecular markers to analyze the inheritance of morphological and developmental traits in apple. J. Am. Soc. Hort. Sci. 120: 532–537Google Scholar
  90. Lesemann, S., A. Urbanietz. and F. Dunemann (2004) Determining population variation of apple powdery mildew at the molecular level. Acta Hort. 663: 199–203Google Scholar
  91. Lespinasse, Y. (1983) Amélioration du pommier pur la résistance à l’oïdium (Podosphaera leucotricha): premiers résultats concernant la virulence du champignon. IOBC/WPRS Bull. 6: 96–110Google Scholar
  92. Lespinasse, Y. (1989) Breeding pome fruits with stable resistance to disease. Genes, resistance mechanisms, present work and prospects. IOBC Bullettin 2: 100–115Google Scholar
  93. Lespinasse, Y., J.M. Olivier, J.M. Lespinasse, and M. Le Lezec (1985) ‘Florina- Quérina’®: la résistance du pommier à la tavelure. Arboriculture fruitière 378: 43–47Google Scholar
  94. Liebhard, R., L. Gianfranceschi, B. Koller, C.D. Ryder, R. Tarchini, E. Van De Weg, and C. Gessler (2002) Development and characterization of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol. Breed. 10:217–241CrossRefGoogle Scholar
  95. Liebhard, R., B. Koller, A. Patocchi, M. Kellerhals, W. Pfammatter, M. Jermini, and C. Gessler (2003a) Mapping quantitative field resistance against apple scab in a Fiesta’ x ‘Discovery’ progeny. Phytopathology 93: 493–501Google Scholar
  96. Liebhard, R., M. Kellerhals, W. Pfammatter, M. Jermini, and C. Gessler (2003b) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol. Biol. 52: 511–526Google Scholar
  97. Magein, H., and D. Leurquin (2000) Changes in amylose, amylopectin and total starch content in Jonagold apple fruit during growth and maturation. Acta Hortic. 517: 487–494Google Scholar
  98. Maliepaard, C., F.H. Alston, G. Van Arkel, L.M. Brown, E. Chevreau, F. Dunemann, K.M. Evans, S. Gardiner, P. Guilford, A.W. van Heusden, J. Janse, F. Laurens, J.R. Lynn, A.G. Manganaris, A.P.M. den Nijs, N. Periam, E. Rikkerink, P. Roche, C. Ryder, S. Sansavini, H. Schmnidt, S. Tartarini, J.J. Verhaegh, M. Vrielink-van Ginkel, and G.J. King (1998) Aligning male and female linkage maps of apple (Malus pumila Mil.) using multi-allelic markers. Theor. Appl. Genet. 97: 60–73CrossRefGoogle Scholar
  99. Malnoy, M., M.L. Xu, E. Borejsza-Wysocka, S.S. Korban, and H.S. Aldwinckle. 2008. Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol. Plant-Microbe Inter. (in press)Google Scholar
  100. Manganaris, A.G. (1989) Isoenzymes as genetic markers in apple breeding. PhD thesis, University of London, London, UKGoogle Scholar
  101. Markussen, T., J. Kruger, H. Schmidt. and F. Dunemann (1995) Identification of PCR-based markers linked to the powdery-mildew-resistance gene Pl1 from Malus robusta in cultivated apple. Plant Breed. 114:530–534CrossRefGoogle Scholar
  102. Menendez, R.A., F.E. Larsen, and R. Fritts Jr. (1986) Protein and isozyme electrophoresis and isoelectric focusing for the characterization of apple clones. Scient. Hort. 29: 211–220CrossRefGoogle Scholar
  103. Minarro, M., and E. Dapena (2004) Inheritance of tolerance to the rosy apple aphid of the cv. ‘Florina’. Acta Hort. 663:261–264Google Scholar
  104. Mulcahy, D.L., M. Cresti, S. Sansavini, G.C. Douglas, H.F. Liskens, G. Bergamini Mulcahy, R. Vignani and M. Pancaldi (1993) The use of random amplified polymorphic DNAs to fingerprint apple genotypes. Scient. Hort. 54: 89–96CrossRefGoogle Scholar
  105. Naik, S., C. Hampson, K. Gasic, G. Bakkeren, and S.S. Korban. 2006. Development and linkage mapping of E-STS and RGAs for functional gene homologues in apple. Genome 49: 959–968PubMedCrossRefGoogle Scholar
  106. Nosarzewski, M. and D.D. Archbold (2007) Tissue-specific expression of SORBITOL DEHYDROGENASE in apple fruit during early development . J. Exp. Bot. 174: 43–78Google Scholar
  107. Nybom, H. (1990a) DNA fingerprints in sports of ‘Red Delicious’ apples. HortSci. 25: 1641–1642Google Scholar
  108. Nybom, H. (1990b) Genetic variation in ornamental apple trees and their seedlings (Malus, Rosaceae) revealed by DNA ‘fingerprinting’ with the M13 repeat probe. Hereditas 113: 17–28Google Scholar
  109. Nybom, H. and B.A. Schaal (1990) DNA ‘fingerprints’ applied to paternity analysis in apples (Malus x domestica). Theor. Appl. Genet. 79:763–768Google Scholar
  110. Nybom, H., S. Gardiner, and C.J. Simon (1992) RFLPs obtained from an rDNA probe and detected with enhanced chemiluminescence in apples. HortScience 27: 355–356Google Scholar
  111. Patocchi A., B. Bigler, B. Koller, M. Kellerhals, and C. Gessler (2004) Vr2: a new apple scab resistance gene. Theor. Appl. Genet. 109: 1087–1092PubMedCrossRefGoogle Scholar
  112. Patocchi A., M. Walser, S. Tartarini, G.A.L. Broggini, F. Gennari, S. Sansavini, and C. Gessler (2005) Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene Vm. Genome 48:630–636PubMedCrossRefGoogle Scholar
  113. Peil, A., T. Garcia-Libreros, K. Richter, F.C. Trognitz, B. Trognitz, M.V. Hanke, and H. Flachowsky (2007) Strong evidence for fire blight resistance gene of Malus robusta located on linkage group 3. Plant Breed. 126: 470–475CrossRefGoogle Scholar
  114. Pierantoni, L., K-H. Cho, I-S. Shin, R. Chiodini, S. Tartarini, L. Dondini, S-J. Kang, and S. Sansavini (2004) Characterisation and transferability of apple SSRs to two European pear F1 populations. Theor. Appl. Genet. 109:1519–1524PubMedCrossRefGoogle Scholar
  115. Qubbaj, T., A. Reineke, and C.P.W. Zebitz (2005) Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica. Entomol. Experiment. Applicata 115: 145–152CrossRefGoogle Scholar
  116. Regnard, J.L., V. Segura, N. Merveille, C.E. Durel, and E. Costes (2007) QTL analysis for leaf gas exchange in an apple progeny grown under atmospheric constraints. Eucarpia XII Fruit Section Symposium, September 16–20, 2007, Zaragoza, Spain: 36Google Scholar
  117. Roche, P., F.H. Alston, C. Maliepaard, K.M. Evans, R. Vrielink, F. Dunemann, T. Markussen, S. Tartarini, L.M. Brown, C. Ryder, and G.J. King (1997a) RFLP and RAPD markers linked to the rosy leaf curling aphid resistance gene (Sd1) in apple. Theor. Appl. Genet. 94:528–533Google Scholar
  118. Roche, P., G. van Arkel, and A.W. van Heusden (1997b) A specific PCR assay for resistance to biotypes 1 and 2 of the rosy leaf curling aphid in apple based on an RFLP marker closely linked to the Sd1 gene. Plant Breed. 116: 567–572Google Scholar
  119. Rushlomé-Pilcher, R.L., J-M. Celton, S.E. Gardiner, D.S. Tustin (2008) Genetic markers linked to the dwarfing trait of apple rootstock ‘Malling 9’. J. Amer. Soc. Hort. Sci. (in press)Google Scholar
  120. Sandanayaka, W.R.M., V.G.M. Bus, P. Connolly, and R. Newcomb (2003) Characteristics associated with woolly apple aphid, Eriosoma lanigerum, resistance of three apple rootstocks. Entomol. Exp. Appl. 109: 63–72CrossRefGoogle Scholar
  121. Seglias, N.P., and C. Gessler (1997) Genetics of apple powdery mildew resistance from Malus zumi (Pl2). IOBC/WPRS Bull 20:195–208Google Scholar
  122. Segura, V., C. Cilas, F. Laurens, and E. Costes (2006)Phenotyping progenies for complex architectural traits: a strategy for 1-year-old apple trees (Malus x domestica Borkh.) Tree Genet. Genomes 2: 140–151CrossRefGoogle Scholar
  123. Segura, V., C. Denancé, C.-E. Durel, and E. Costes (2007) Wide range QTL analysis for complex architectural traits in a 1-year-old apple progeny. Genome, 50: 159–171PubMedCrossRefGoogle Scholar
  124. Service, R.F. (2002) Tapping DNA for structures produces a trickle. Science 298: 948–950PubMedCrossRefGoogle Scholar
  125. Silfverberg-Dilworth, E., C.L. Matasci, W.E. Van de Weg, M.P.W. Van Kaauwen, M. Walser, L.P. Kodde, V. Soglio, L. Gianfranceschi, C.E. Durel, F. Costa, T. Yamamoto, B. Koller, C. Gessler, and A. Patocchi (2006) Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genet. Genomes 2:202–224CrossRefGoogle Scholar
  126. Stankiewicz, M., E. Pitera, and S.W. Gawronski (2001) Genetic analysis of a polish apple selection U211 as a new source of high resistance to apple powdery mildew. Acta Hort. 546: 641–644Google Scholar
  127. Stankiewicz-Kosyl, M., E. Pitera, and S.W. Gawronski (2005) Mapping QTL involved in powdery mildew resistance of the apple clone U 211. Plant Breed. 124:63–66CrossRefGoogle Scholar
  128. Stankiewicz-Kosyl, M., A. Novicka, P. Krajewski, K.Tomala, Soska A., F. Laurens, C. Govan, M. Lateur, F. Costa, S. Tartarini, W. Guerra, M. Lewandowski, K. Rutkowski, E. Zurawicz, L. Gianfranceschi, C.E. Durel, F. Mathis, E. Barbaro, D. Mott, A. Patocchi, D. Gobbin, F. Fernandez, K. Evans, F. Dunemann, A. Boudichevskaja, J. Jansen, and E. van de Weg (2007) QTL analysis of acidity in apple using pedigree-based approach. Eucarpia XII Fruit Section Symposium, September 16–20, 2007, Zaragoza, Spain: 60–61Google Scholar
  129. Tartarini, S. (1996) RAPD markers linked to the Vf gene for scab resistance in apple. Theor. Appl. Genet. 92: 803–810CrossRefGoogle Scholar
  130. Tartarini, S., L. Gianfranceschi, S. Sansavini, C. Gessler (1999) Development of reliable PCR markers for the selection of the Vf gene conferring scab resistance in apple. Plant Breed. 118: 183–186CrossRefGoogle Scholar
  131. Tartarini, S., S. Sansavini, B. Vinatzer, F. Gennari, and C. Domizi (2000) Efficiency of marker assisted selection (MAS) for the Vf scab resistance gene. Acta Hort. 538: 549–552Google Scholar
  132. Tian, Y.-K., C.-H. Wang, J.-S. Zhang, C. James, and H.-Y. Dai (2005) Mapping Co, a gene controlling the columnar phenotype of apple, with molecular markers. Euphytica 145: 181–188CrossRefGoogle Scholar
  133. Tobutt, K.R., R. Boskovic, and P. Roche (2000) Incompatibility and resistance to woolly apple aphid in apple. Plant Breed. 119: 65–69CrossRefGoogle Scholar
  134. Urbanietz, A., and F. Dunemann (2005) Isolation, identification and molecular characterization of physiological races of apple powdery mildew (Podosphaera leucothrica). Plant Pathol. 54: 125–133CrossRefGoogle Scholar
  135. Van der Linden, C.G., D.C.A.E. Wouters, V. Mihalka, E.Z. Kochieva, M.J.M. Smulders, and B. Vosman (2004) Efficient targeting of plant disease resistance loci using NBS profiling. Theor. Appl. Genet. 109:384–393PubMedCrossRefGoogle Scholar
  136. Van de Weg, W.E., R.E. Voorrips, R. Finkers, L.P. Kodde, J. Jansen, and M.C.A.M. Bink (2004) Pedigree genotyping: a new pedigree-based approach of QTL identification and allele mining. Acta Hortic. 663: 45–50Google Scholar
  137. Van de Weg, E., H. Jansen, M. Bink, R.E. Voorrips, C.E. Durel, F. Laurens, F. Dunemann, K. Evans, A. Patocchi, W. Guerra, M. Komjanc, M. Lateur, M. Kellerhals, C. Ryder, S. Sansavini, K.Tomala, E. Zurawicz, and L. Gianfranceschi (2007) QTL mapping in multiple, pedigreed populations: the concept and the framework of the statistical procedures. Eucarpia XII Fruit Section Symposium, September 16–20, 2007, Zaragoza, Spain: 57–58Google Scholar
  138. Van Dyk, M.M., J. Baison, P. Hove, C. Marondedze, A. Klein, K. Soeker, and D.J.G. Rees (2007) BIN mapping of EST-SSRs and EST-SNPs in apple (Malus x domestica Borkh.). Eucarpia XII Fruit Section Symposium, September 16–20, 2007, Zaragoza, Spain: 57–58Google Scholar
  139. Venisse, J.S., M. Malnoy, M. Faize, J.P. Paulin, and M.N. Brisset (2002) Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. MPMI 15: 1204–1212PubMedCrossRefGoogle Scholar
  140. Venturi, S., L. Dondini, P. Donini, and S. Sansavini (2006) Retrotransposon characterisation and fingerprinting of apple clones by S-SAP markers. Theor. Appl. Genet. 112: 440–444PubMedCrossRefGoogle Scholar
  141. Visser, T., and J.J. Verhaegh (1976) Review of tree fruit breeding carried out at the Institute for Horticultural Plant Breeding at Wageningen from 1951–1976. Proc. Eucarpia Meeting of Tree Fruit Breeding, Wageningen, The Netherlands, pp 113–132Google Scholar
  142. Vinatzer, B.A., H.B. Zhang, and S. Sansavini (1998) Construction and characterization of a bacterial artificial chromosome library of apple. Theor. Appl. Genet. 97: 1183–1190CrossRefGoogle Scholar
  143. Vinatzer B.A., A. Patocchi, L. Gianfranceschi, S. Tartarini, H. Zhang, C. Gessler, and S. Sansavini (2001) Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol. Plant-Microbe Inter. 14:508–515CrossRefGoogle Scholar
  144. Vinatzer, B.A., A. Patocchi, S. Tartarini, L. Gianfranceschi, S. Sansavini, and C. Gessler (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
  145. Watillon, B., P. Druart, P. Du Jardin, R. Kettmann, P. Boxus, and A. Burny (1991) Use of random cDNA probes to detect restriction fragment length polymorphisms among apple clones. Scient. Hort. 46: 235–243CrossRefGoogle Scholar
  146. Weeden, N.F. and R.C. Lamb (1985) Identification of apple cultivars by isoenzyme phenotypes. J. Amer. Soc. Hort. Sci. 110:509–515Google Scholar
  147. Xu, M.L. and S.S. Korban (2000) Saturation mapping of the apple scab resistance gene V f using AFLP markers. Theor. Appl. Genet. 101: 844–851CrossRefGoogle Scholar
  148. Xu M.L., and Korban S.S (2002) A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics 162: 1995–2006PubMedGoogle Scholar
  149. Xu, M., S.S. Korban, J. Song, and J. Jiang (2002) Constructing a bacterial artificial chromosome library of the apple cultivar GoldRush. Acta Hort. 595: 103–112Google Scholar
  150. Xu, M., J. Song, Z. Cheng, J. Jiang, S.S. Korban (2001) A bacterial artificial chromosome (BAC) library of Malus floribunda 821 and contig construction for positional cloning of the apple scab resistance gene Vf. Genome 44:1104–1113PubMedCrossRefGoogle Scholar
  151. Yamamoto, T., T. Kimura, Y. Sawamura, K. Kotobuki, Y. Ban, T. Hayashi and N. Matsuta (2001) SSRs isolated from apple can identify polymorphism and genetic diversity in pear. Theor. Appl. Genet. 102:865–870CrossRefGoogle Scholar
  152. Yamamoto, T., T. Kimura, M. Shoda, T. Imai, T. Saito, Y. Sawamura, K. Kotobuki, T. Hayashi and N. Matsuta (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor. Appl. Genet. 106: 9–18PubMedGoogle Scholar
  153. Yamamoto, T., T. Kimura, J. Soejima, T. Sanada, Y. Ban, and T. Hayashi (2004) Identification of quince varieties using SSR markers developed from pear and apple. Breed. Sci. 54: 239–244CrossRefGoogle Scholar
  154. Yao, Y.-X., M. Li , Z. Liu , Y.-J. Hao , H. Zha (2007) A novel gene, screened by cDNA-AFLP approach, contributes to lowering the acidity of fruit in apple. Plant Physiol. Biochem. 173: 44–54Google Scholar
  155. Yang, H. and S.S. Korban (1996) Screening apples for OPD20/600 using sequence-specific primers. Theor. Appl. Genet. 92:263–266CrossRefGoogle Scholar
  156. Yang, H.Y., S.S. Korban, J. Krüger, and H. Schmidt (1997a) The use of a modified bulk segregant analysis to identify a molecular marker linked to a scab resistance gene in apple. Euphytica 94: 175–182Google Scholar
  157. Yang, H.Y., S.S. Korban, J. Krüger, and H. Schmidt (1997b) A randomly amplified polymorphic DNA (RAPD) marker tightly linked to the scab resistance gene V f in apple. J. Amer. Soc. Hort. Sci. 122: 47–52Google Scholar
  158. Yang, H.Y. and J. Krüger (1994) Identification of an RAPD markers linked to the V f gene for scab resistance in apples. Plant Breed. 112:323–329CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Natural Resources and Environmental SciencesUniversity of IllinoisUrbanaUSA 61801
  2. 2.Department of Fruit and Woody Plant SciencesAlma Mater Studiorum – Bologna University40127 BolognaItaly

Personalised recommendations