Apple Transformation and Translational Genomics

  • Mickael Malnoy
  • Herb Aldwinckle
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 6)

The apple genome sequencing, currently in progress at the Istituto Agrario San Michele all Adige Italy and Washington State University USA, in combination of various computational and empirical approaches to sequence annotation, will made possible the identification of more than thousand genes. At the time of completion of the apple genome sequence, few of these genes will have an experimental assigned function. Indeed, in Arabidopsis thalinia only 10% of the 25,500 unique genes that were initially predicted had an experimental assigned function (Arabidopsis Genome Initiative, 2000).


Apple Cultivar Fire Blight Apple Scab Apple Genome Apple Gene 
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.


  1. Arabidopsis Genome Initiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.CrossRefGoogle Scholar
  2. Astwood, J.D., Leach, J.N. and Fuchs, R.L. (1996) Stability of food allergens to digestion in vitro. Nature Biotechnology 14:1269–1273.CrossRefPubMedGoogle Scholar
  3. Atkinson, R.G., Schroder, R., Hallett, I.C., Cohen, D. and MacRae, E.A. (2002) Overexpression of polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involved in cell adhesion. Plant Physiology 129:122–133.CrossRefPubMedGoogle Scholar
  4. Awad, M.A. and de Jager, A. (2003) Influences of air and controlled atmosphere storage on the concentration of potentially healthful phenolics in apples and other fruits. PostharVest Biology and Technology 27: 53–58.CrossRefGoogle Scholar
  5. Barbieri, C. and Morini, S. (1987) In vitro regeneration from somatic tissues and seed explants of apple. Advances in Horticultural Science 1:8–10.Google Scholar
  6. Barbieri, M., Belfanti, E., Tartarini, S., Vinatzer, B., Sansavini, S., Silfverberg-Dilworth, E., Gianfranceschi, L., Hermann, D., Patocchi, A. and Gessler, C. (2003). Progress of map-based cloning of the Vf resistance gene and functional verification: Preliminary results from expression studies in transformed apple. HortScience 38:329–331.Google Scholar
  7. Baldwin, E., Fruit flavor, volatile metabolism and consumer perceptions. (2002) In Fruit Quality and its Biological Basis; M. Knee (Ed), CRC Press, Boca Raton, FL, 89–106.Google Scholar
  8. Belfanti, E., Silfverberg-Dilworth, E., Tartarini, S., Patocchi, A., Barbieri, M., Zhu, J., Vinatzer, B.A., Gianfranceschi, L., Gessler, C. and Sansavini, S. (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proceedings of the National Academy of Sciences USA 101:886–890.CrossRefGoogle Scholar
  9. Bolar, J.P., Norelli, J.L., Wong, K-W., Hayes, C.K., Harman, G.E. and Aldwinckle, H.S. (2000) Expression of endichitinase from Trichoderma harzianum in transgenic apple increases resistance to apple scab and reduces vigor. Phytopathology 90:72–77.CrossRefPubMedGoogle Scholar
  10. Bolar, J.P., Norelli, J.L., Harman, G.E., Brown, S.K. and Aldwinckle, H.S. (2001) Symergistic activity of endochitinase and exochitinase from Trichoderma atroviride (T. harzianum) against the pathogenic fungus (Venturia inaequalis) in transgenic apple plants. Transgenic Research 10:533–543.CrossRefPubMedGoogle Scholar
  11. Borejsza-Wysocka, E.E., Malnoy, M., Meng, X., Bonasera, J.M., Nissinen, R.M., Kim, J.F., Beer, S.V. and Aldwinckle, H.S. (2006) The fire blight resistance of apple clones in which DspE-interacting proteins are silenced. Acta Horticulturae 704:509–513.Google Scholar
  12. Broothaerts, W., Janssens, G.A., Proost, P., Broekaert, W.F. (1995) cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Molecular Biology 27:499–511.CrossRefPubMedGoogle Scholar
  13. Broothaerts, W., Keulemans, J. and Van Nerum, I. (2004) Self-fertile apple resulting from S-Rnase gene silencing. Plant Cell Reports 22:497–501.CrossRefPubMedGoogle Scholar
  14. Bulley, S.M., Wilson, F.M., Hedden, P., Phillips, A.L., Croker, S. and James, D. (2005) Modification of gibberellin biosynthesis in the grafted apple scion allows control of tree height independent of the rootstock. Plant Biotechnology Journal 3:215–223.CrossRefPubMedGoogle Scholar
  15. Cao, H., Bowling, S.A., Gordon, S.A. and Dong, X. (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592.CrossRefPubMedGoogle Scholar
  16. Cao, H., Gladzebrook, J., Clark,e J.D., Volko, S. and Dong, X. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63.CrossRefPubMedGoogle Scholar
  17. Cheng, L., Zhou, R., Reidel, E.J., Sharkey, T.D. and Dandekar, A.M. (2005) Antisenses inhibition of sorbitol synthesis leads to up regulation of starch synthesis without altering CO2 assimilation in apple leaves. Planta 220:767–776.CrossRefPubMedGoogle Scholar
  18. Conner, A.J., Barrell, P.J.,. Baldwin, S.J., Lokerse, A.S., Cooper, P.A, Erasmuson, A.K, Nap, J.P. and Jacobs, J.M.E. (2007) Intragenic vectors for gene transfer without foreign DNA Euphytica 154:341–353.CrossRefGoogle Scholar
  19. Dandekar, A.M., Teo, G., Defilippi, B.G., Uratsu, S.L., Passey, A.J., Kader, A.A., Stow, J.R., Colgan, R.J. and James, D.J. (2004) Effect of down regulation of ethylene biosynthesis on fruit flavor complex in apple fruit. Transgenic Research 13:373–384.CrossRefGoogle Scholar
  20. Defilippi, B., Dandekar, A.M. and Kader, A.A. (2004). Impact of suppression of ethylene action or biosynthesis on flavor metabolites in apple (Malus X domestica Borkh.) fruit. Journal of Agricultural and Food Chemistry 52: 5694–5701.CrossRefPubMedGoogle Scholar
  21. Defilippi, B., Dandekar, A.M. and Kader, A.A. (2005a) Relationship of ethylene biosynthesis to volatile production, related enzymes, and precursor availability in apple peel and flesh tissues. Journal of Agricultural and Food Chemistry 53:3133–3141.Google Scholar
  22. Defilippi, B., Dandekar, A.M. and Kader, A.A. (2005b) Apple aroma: alcohol acyltransferase, a rate limiting step for ester biosynthesis, is regulated by ethylene. Plant Science 168:199–1210.Google Scholar
  23. Ebner C., Hirschwehr R., Bauer L., Breiteneder H., Valenta R., Ebner H., et al. (1995) Identification of allergens in fruits and vegetables: IgE crossreactivities with the important birch pollen allergens Bet v 1 and Bet v 2 (birch profilin). Journal of Allergy and Clinical Immunology 95(5):962–969.CrossRefPubMedGoogle Scholar
  24. Espley, R.V., Hellens, R.P., Putterill, J., Stevenson, D.E., Kutty-Amma1, S. and Allan, A.C. (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. The Plant Journal 49: 414–427.Google Scholar
  25. Faize, M., Malnoy, M., Dupuis, F., Chevalier, M., Parisi, L. and Chevreau E. (2003) Chitinases of Trichoderma atroviridae induce scab resistance and some metabolic changes in two cultivars of apple. Phytopathology 93:1496–1504.CrossRefPubMedGoogle Scholar
  26. Faize, M., Sourice, S., Dupuis, F., Parisi, L., Gautier, M.F. and Chevreau E. (2004) Expression of wheat puroindoline b reduces scab susceptibility in transgenic apple (Malus X domestica Borkh.). Plant Science 167:347–354.CrossRefGoogle Scholar
  27. Fasolo, F, Zimmermann, R.H. and Fordham, I. (1989) Adventitious shoot formation on excised leaves of in vitro grown shoots of apple cultivars. Plant Cell, Tissue and Organ Culture 16: 75–87.CrossRefGoogle Scholar
  28. Fernandez-Rivas, M., Bolhaar, S., Gonzalez-Mancebo, E., Asero, R., van Leeuwen, A., Bohle, B., Ma, Y., Ebner, C., Rigby, N., Sancho, A.I., Miles, S., Zuidmeer, L., Knulst, A., Breiteneder, H., Mills, C., Hoffmann-Sommergruber, K. and van Ree, R. (2006) Apple allergy across Europe: How allergen sensitization profiles determine the clinical expression of allergies to plant foods. Journal of Allergy and Clinical Immunology 118:481–488.CrossRefPubMedGoogle Scholar
  29. Flachowsky, H., Peil, A., Sopanen, T., Elo, A. and Hanke, V. (2007) Overexpression of BpMADS4 from silver birch (Betula pendula Roth.) induces early-flowering in apple (Malus domestica Borkh.). Plant Breeding 126:137–145.CrossRefGoogle Scholar
  30. Flores, F., Ben Amor, M., Jones, B., Pech, J.C., Bouzayen, M., Latché, A. and Romojaro, F. (2001) The use of ethylene-suppressed lines to assess differential sensitivity to ethylene of the various ripening pathways in cantaloupe melons. Physiologia Plantarum 113:128–133.CrossRefGoogle Scholar
  31. Gilissen, L.J.W.J., Bolhaar, S.T.H.P., Matos, C.I., Rouwendal, G.J.A., Boone, M.J., Krens, F.A., Zuidmeer, L., Van Leeuwen, A., Akkerdaas, J., Hoffmann-Sommergruber, K., Knulst, A.C., Bosch, D., Van de Weg, W.E. and Van Ree, R. (2004) Silencing the major apple allergen Mal d1 by using the RNA interference approach. Journal of Allergy and Clinical Immunology 115:364–369.CrossRefGoogle Scholar
  32. Golding, J.B., McGlasson, W.B., Wyllie, S.G., Leach, D.N. (2001) Fate of apple peel phenolics during cool storage. Journal of Agricultural and Food Chemistry 49:2283–2289.Google Scholar
  33. Gray, J., Picton, S., Shabbeer, J., Schuch, W. and Grierson, D. (1992) Molecular biology of fruit ripening and its manipulation with antisense genes. Plant Molecular Biology 19: 69–87.CrossRefPubMedGoogle Scholar
  34. Holefors, A., Xue, Z.T. and Welander, M. (1998) Transformation of the apple rootstock M26 with rolA gene and its influence on growth. Plant Science 136:69–78.CrossRefGoogle Scholar
  35. Holefors, A., Xue, Z.T., Zhu, L.H. and Welander, M. (2000) The Arabidopsis phytochrome B gene influences growth of the apple rootstock M26. Plant Cell Reports 19, 1049–1056.CrossRefGoogle Scholar
  36. Hrazdina, G., Kiss, E., Galli, Z., Rosenfield, C., Norelli, J.L. and Aldwinckle, H.S. (2003) Down regulation of ethylene production in Royal Gala apples. Acta Horticulturae 628:239–251.Google Scholar
  37. Igarashi, M., Ogasawara, H., Hatsuyama, Y., Saito, A. and Suzuki, M. (2002) Introduction of rolc into Marubakaidou (Malus prunifolia Borkh. Var. ringo Asami Mo 84-A) apple rootsock via Agrobacterium tumefaciens. Plant Science 163:463–473.CrossRefGoogle Scholar
  38. James, D.J., Passey, A.J., Barbara, D.J. and Bevan, M.V. (1989) Genetic transformation of apple (Malus pumila Mill.) using disarmed Ti-binary vector. Plant Cell Reports 7: 658–666.Google Scholar
  39. James, D.J., Passey, A.J., Webster, A.D., Barbara, D.J., Viss, P., Dandekar, A.M. and Uratsu, S. (1993) Transgenic apples and strawberries: Advances in transformation, introduction of genes for insect resistance and field studies of tissue cultured plants. Acta Horticulturae 336:179–184.Google Scholar
  40. James, D.J., Passey, A.J. and Baker, S.A. (1994) Stable gene expression in transgenic apple tree tissues and segregation of transgenes in the progeny – preliminary evidence. Euphytica 77: 119–121.CrossRefGoogle Scholar
  41. James, D.J., Passey, A.J. and Baker, S.A. (1995) Transgenic apples display stable gene expression in the fruit and medelian segregation of the transgenes in the R1 progeny. Euphytica 85: 109–112.CrossRefGoogle Scholar
  42. James, D.J., Passey, A.J., Baker, S.A. and Wilson, F.M., (1996) Transgenes display stable patterns of expression in apple fruit and Mendelian segregation in the progeny. Bio/Technology 14, 56–60.CrossRefGoogle Scholar
  43. Jones, A.L. and Schnabel, E.L. (2000) The development of streptomycin-resistant strains of Erwinia amylovora. p 235–251 In: J. Vanneste(Ed), Fire blight, CAB Int., New York.Google Scholar
  44. Kanamaru, N., Ito, Y., Komori, S., Saito, M., Kato, H., Takahashi, S., Omura, M., Soejima, J., Shiratake, K., Yamada, K. and Yamaki, S. (2004) Transgenic apple transformed by sorbitol-6-phosphate dehydrogenase switch between sorbitol and sucrose supply due to its gene expression. Plant Science 167:55–61.CrossRefGoogle Scholar
  45. Knee, M. (1993) Pome fruits. In Biochemistry of Fruit Ripening; G.B. Seymour, J.E. Taylor, and G.A. Tucker (Eds), Chapman and Hall, New York, 325–346.Google Scholar
  46. Kotoda, N. and Wada, M. (2005) MdTFL1, a TFL1 like gene of apple, retards the transition from the vegetative to production phase in transgenic Arabidopsis. Plant Science 168: 95–104.CrossRefGoogle Scholar
  47. Kotoda, N., Iwanami, H., Takahashi, S. and Abe, K. (2006) Antisense expression of MdTFL1, a TFL1 like gene, reduces the juvenile phase in apple. Journal of the American Society of Horticultural Science 131:74–81.Google Scholar
  48. Korban, S.S., O’Connor, P.A. and Elobeidy, A. (1992) Effects of thidiazuron, naphthaleneacetic acid, dark incubation and genotype on shoot organogenesis from Malus leaves. Journal of the American Society of Horticultural Science 67: 341–349.Google Scholar
  49. Liu, J.R., Sink, K.C. and Dennis, F.G. Jr. (1983a) Adventive embryogenesis from leaf explants of apple seedling. HortScience 18:871–873.Google Scholar
  50. Liu, J.R., Sink, K.C. and Dennis, F.G. Jr. (1983b) Plant regeneration from apple seedling explants of apple and callus cultures. Plant Cell, Tissue and Organ Culture 2, 293–304.Google Scholar
  51. Malnoy, M. and Aldwinckle, H.S. (2007), Development of fire blight resistance by recombinant DNA technology. Plant Breeding Reviews 29:315–344.CrossRefGoogle Scholar
  52. Malnoy M., Jin Q., Borejsza-Wysocka E.E., He S.Y. and Aldwinckle, H.S. (2007a) Over-Expression of the Apple Gene MpNPR1 confers Increased Disease Resistance in Malus x Domestica MPMI. 20:1568–1580.Google Scholar
  53. Malnoy, M., Borejsza-Wysocka, E.E., Abbott, P., Lewis, S., Norelli, J.L., Flaishman, M.A., Gidoni, D. and Aldwinckle, H.S. (2007b) Genetic transformation of apple without use of a selectable marker. Acta Horticulturae 663:319–322.Google Scholar
  54. Malnoy, M., Korban, S.S., Borejsza-Wysocka E.E. and Aldwinckle H.S. Genetic Engineering of Malus. In Transgenic Series: Volume 5: Temperate Fruits & Nuts. Editors: C. Kole, Ralph Scorza and Timothy C. Hall. In press.Google Scholar
  55. Malnoy, M., Xu, M., Borejsza-Wysocka, E.E., Korban, S.S. and Aldwinckle, H.S. (2008) Two receptor like genes, Vfa1 and Vfa2 confer resistance to the fungal pathogen venturia inaequalis inciting apple scab disease. MPMI 21:448–458.CrossRefPubMedGoogle Scholar
  56. Murata, M., Haruta, M., Murai, N., Tanikawa, N., Nishimura, M., Homma, S. and Itoh, Y. (2000) Transgenic apple (Malus X domestica) shoot showing low browning potentail. Journal of Agricultural and Food Chemistry 48:5243–5248.CrossRefPubMedGoogle Scholar
  57. Murata, M., Nishimura, M., Murai, N., Haruta, M., Homma, S. and Itoh, Y. (2001) A transgenic apple callus showing reduced polyphenol oxidase activity and lower browning potential. Bioscience, Biotechnology and Biochemistry 65:383–388.CrossRefGoogle Scholar
  58. Ortolani, C., Ispano, M., Pastorello, E., Bigi, A. and Ansaloni, R. (1988) The oral allergy syndrome. Annals Allergy 61, 47–52.Google Scholar
  59. Puhringer, H., Moll, D., Hoffmann-Sommergruber, K., Watillon, B., Katinger, H. and Machado, M.L.D. (2000) The promoter of an apple Ypr10 gene, encoding the major allergen Mal d 1, is stress- and pathogen-inducible. Plant Science 152, 35–50.CrossRefGoogle Scholar
  60. Radchuck, V.V. and Korkhovoy, V.I. (2005) The rolB gene promotes rooting in vitro and increases fresh root weight in vivo of transformed apple scion cultivar ‘Florina’. Plant Cell, Tissue and Organ Culture 81, 203–212.CrossRefGoogle Scholar
  61. Rommens, C.M., Humara, J.M., Ye, J., Yan, H., Richael, C., Zhang, L., Perry, R. and Swords, K. (2004) Crop improvement through modification of the plant’s own genome. Plant Physiology 135: 421–431.CrossRefPubMedGoogle Scholar
  62. Schaffer, R.J., Friel, E.N., Souleyre, E.J.F., Bolitho, K., Thodey, K., Ledger, S., Bowen, J.H., Ma J.-H., Nain, B., Cohen, D., Gleave, A.P., Crowhurst, R.N., Janssen, B.J., Yao, J.L. and Newcomb, R.D. (2007) A genomics approach reveals that aroma production in apple is controlled by ethylene predominantly at the final step in each biosynthetic pathway. Plant Physiology 144:1899–1912.CrossRefPubMedGoogle Scholar
  63. Schmidt, H. and van de Weg, W.E. (2005) Breeding. In J. Tromp, A.D. Webster, and S.J. Wertheim (Eds) Fundamentals of Temperate Zone Tree Fruit Production. Backhuys, Leiden, The Netherlands, 136–155.Google Scholar
  64. Silfverberg-Dilworth, E., Patacchi, A., Belfanti, E., Tartarini, S., Sansavini, S. and Gessler, C. (2005) Hcrvf2 introduced into Gala confers race-specific apple scab resistance. In: Plant & Animal Genome XIII Conference, January 15–19, 2005, San Diego, CA, USA.Google Scholar
  65. Snyder, M. and Gerstein, M. (2003) vGenomics. Defining genes in the genomics era. Science 300:258–260.CrossRefPubMedGoogle Scholar
  66. Sriskandarajah, S., Skirvin, R.M., Abu Qaoud, H. and Korban, S.S. (1990) Factors involved in elongation and growth of adventitious shoots from tree apple scion cultivars in vitro. Journal Horticultural Science 65:113–121.Google Scholar
  67. Teo, G., Suzuki, Y., Uratsu, S.L., Lampinen, B., Ormonde, N., Hu, W.K., Dejong, T.M. and Dandekar, A.M. (2006) Silencing leaf sorbitol synthesis alters long-distance partitioning and apple fruit quality. Proccedings of the National Academy of Sciences USA 103:18842–18847.CrossRefGoogle Scholar
  68. Vanek-Krebitz, M., Hoffmann-Sommergruber, K., Machado, M.L.D., Susani, M., Ebner, C., Kraft, D., Scheiner, O. and Breiteneder, H. (1995) Cloning and Sequencing of Mal d 1, the Major Allergen from Apple (Malus domestica), and Its Immunological Relationship to Bet v 1, the Major Birch Pollen Allergen. Biochemical and Biophysical Research Communications 214:538–551.CrossRefPubMedGoogle Scholar
  69. Vinatzer, B.A., Patocchi, A., Gianfranceschi, L., Tartarini, S., Zhang, H.B., Gessler, C., Sansavini, S. (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. Molecular Plant Microbe Interactions 14:508–514.CrossRefPubMedGoogle Scholar
  70. 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 162:1995–2006.PubMedGoogle Scholar
  71. Webb, K.L. and Burley, J.W.A. (1962) Sorbitol translocation in apple. Science 137:766.CrossRefPubMedGoogle Scholar
  72. Welander, M. (1988) Plant regeneration from leaf and stem segments of shoots raised in vitro from mature apple trees. Journal of Plant Physiology 132:738–744.Google Scholar
  73. Welander, M., Pawlicki, N., Holefors, A. and Wilson, F. (1998) Genetic transformation of apple rootstock M26 with rolB gene and its influence on rooting. Journal of Plant Physiology 53: 371–380.Google Scholar
  74. Zhou, Z.Q. and Li, Y.N. (2000) The RAPD evidence for the phylogenetic relationship of the closely related species of the cultivated apple. Genetic Resources and Crop Evolution 47:353–357.CrossRefGoogle Scholar
  75. Zhu, L.H. and Welander, M. (2000) Growth characteristics of apple cultivar Gravenstein plants grafted onto the transformed rootstock M.26 with rolA and rolB under non-limiting nutrient conditions. Plant Science 147:75–80.CrossRefGoogle Scholar
  76. Zhu, L.H., Ahlman, A., Li, X.Y. and Welander, M. (2001a) Intergration of the rolA gene into the genome of the vigorous apple rootstock A2 reduced plant height and shortened internodes. Journal of Horticultural Science and Biotechnology 76:758–763.Google Scholar
  77. Zhu, L.H., Holefors, A., Ahlman, A., Xue, Z.T. and Welander, M. (2001b) Transformation of the apple rootstock M.9/29 with the rolB gene and its influence on rooting and growth. Plant Science 160:433–439.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Mickael Malnoy
    • 1
  • Herb Aldwinckle
    • 2
  1. 1.Istituto Agrario San Michele all’AdigeItaly
  2. 2.Department of Plant Pathology, Cornell UniversityGenevaUSA

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