Transformation of Malus

Published Date
Volume 66 of the series Forestry Sciences pp 281-303

Author 
F. A. Hammerschlag

Abstract

In their book chapter on Malus, Way et al. (1991) included a quote by prize winning apple artist Roseanne Sanders (Sanders, 1988) who wrote ‘From the garden of Eden to the Big Apple, from William Tell to Johnny Appleseed, to Paris of Troy who gave the troublesome golden apple to Aphrodite which started the Trojan War, the apple has occupied a very special place in our affections both as a symbol and as one of the simplest and most delicious of Nature’s gifts’. In this chapter, I will discuss briefly the history of apple, problems of commercial apple cultivars, conventional breeding solutions to apple problems, and then will focus on apple transformation, with an emphasis on strategies to improve the efficiency of Agrobacterium-mediated transformation.

References

1. Agrawal, S. (1992) Antisense oligonucleotides as antiviral agents. Trends in Bio Technol. 10, 152–158.
2. Akama, K., Shiraishi, K., Ohta, S., Nakamura, K., Okada, K., and Shimura, Y. (1992) Efficient transformation of Arabidopsis thaliana: comparison of the efficiencies with various organs, plant ecotypes andAgrobacterium strains. Plant Cell Rep. 12, 7–11.
3. Alston, F.H. (1981) Breeding high quality high yielding apples. in P.W. Goodenough and R.K. Aitkin (eds.), Quality in Stored and Processed Vegetables and Fruit, Academic Press, London, pp. 93–102.
4. Alt-Morbe, J., Kuhlmann, H., and Schroder, J. (1989) Differences in induction of Ti plasmid virulence genes virG and virD, and continued control of virD expression by four external factors. Mol. Plant-Microbe Inter, 301–308.
5. Ankenbauer, R.G. and Nester, E.W. (1990) Sugar-mediated induction of Agrobacterium tumefaciens
6. virulence genes: structural specificity and activities of monosaccharides. J. Bacteriol.172, 6442–6446.
7. Ballard, J.K., Proebsting, E.L., Tukey, R.B., and Mills, H. (1971) Critical temperatures for blossom buds. Wash. StateAgr. Ext. Circ. 369–374.
8. Barrett, C. and Cassells, A.C. (1994) An evaluation of antibiotics for the elimination of Xanthomonas campestris pv. pelargonii (Brown) limn Pelargonium x domesticum cv. Grand Slam explants in vitro. Plant Cell Tissue Organ Cult. 36, 169–175.
9. Beachy, R.N., Loesch-Fries, S., and Turner, N.E. (1990) Coat protein-mediated resistance against virus infection. Annu. Rev. Phytopathol. 28, 451–474.
10. Belaizi, M., Paul, H., Sangwan, R.S., and Sangwan-Norreel, B.S. (1991) Direct organogenesis from intemodal segments of in vitro grown shoots of apple cv. Golden Delicious. Plant Cell Rep. 9, 471–474.
11. Sidney, D., Scelonge, Ch., Martich, J., Burrus, M., Sims, L, and Huffman, G. (1992) Microprojectile bombardment of plant tissues increases transformation frequency by Agrobacterium tumefaciens.Plant Mol. Biot. 18, 301–313.
12. Bolar, J.P., Brown, S.K., Norelli, J.L., and Aldwinckle, H.S. (1999a) Factors affecting the transformation of ‘Marshall McIntosh’ apple by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult. 54, (In press)
13. Bolar, J.P., Norelli, J.L., Harman, G.E., Brown, S.K., and Aldwinckle, H.S. (1999b) Expression of fungal chitinolytic enzymes in transgenic apples confers high levels of resistance to scab, in A. Altman, S. Izhar, and M. Ziv (eds.), Plant Biotechnology and In Vitro Biology in the 21’ t Century, Kluwer Academic Publishers, Dordrecht. ( In press )
14. Bolton, G.W., Nester, E.W., and Gordon, M.P. (1986) Plant phenolic compounds induce expression of Agrobacterium tumefaciens loci needed for virulence. Science 232, 983–985.PubMed
15. Briggs, J.B. and Alston, F.H. (1969) Sources of pest resistance in apple cultivars. Rep. E. Mailing Res. Stn. for1968: 159–162.
16. Broglie, K., Chet, I., Holliday, M., Cressman, R., Biddle, P., Knowlton, S., Mauvais, C.J., and Broglie, R. (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctoma solani. Science 254, 1194–1197.
17. Brown, A.G. (1975) Apples, in J. Janick and J.N. Moore (eds.), Advances in Fruit Breeding, Purdue Univ. Press, West Lafayette, IN, pp. 3–37.
18. Brown, S.K. (1992) Genetics of apple. Plant Breed. Rev. 9, 333–366.
19. Carmona, J.J., Molina, A., Fernandez, J.A., Lopez-Fando, J.J., and Garcia-Olmedo, F. (1993) Expression of the a-thionin gene from barley in tobacco confers enhanced resistance to bacterial pathogens. Plant J. 3, 457–462.PubMed
20. Cheng, F.S., Weeden, N.F., and Brown, S.K. (1996) Identification of co-dominant RAPD markers tightly linked to fruit skin colar. Theor. Appl. Genet. 93, 222–227.
21. Cheng, F.S., Weeden, N.F., Brown, S.K., Aldwinckle, H.S., Gardiner, S.E., and Bus, V.G. (1998) Development of a DNA marker for V, a gene conferring resistance to apple scab. Genome 41, 208–214.
22. Chyi, Y-S. And Phillips, G.C. (1987) High efficiency Agrobacterium-mediated transformation of Lycopersicon based on conditions favorable for regeneration. Plant Cell Rep. 6, 105–108.
23. Connor, P.J., Brown, S.K., and Weeden, N.F. (1997) Randomly amplified polymorphic DNA-based genetic linkage maps of three apple cultivars. J. Amer. Soc. Hort. Sci. 122, 350–359.
24. Crane, M.B. (1953) The genetics and breeding of tree fruits. Rep. Intl. Hort. Cong., Int. Soc. Hort., London, pp. 687–695.
25. Dandekar, A. (1992) Transformation, in F.A. Hammerschlag and R.E. Litz (eds.), Biotechnology of Perennial Fruit Crops, CAB International, Wallinford, pp. 141–168.
26. Dandekar, A., Uratsu, S.L., and Matsuta, N. (1990) Factors influencing virulence in Agrobacteriummediated transformation of apple. Acta Hort. 280, 483–494.
27. Dandekar, A., McGranahan, G.H., and James, D.J. (1993) Transgenic woody plants. in Transgenic Plants, Vol. 2, Academic Press, London, pp. 129–151.
28. Dayton, D.F. (1959) Red color distribution in apple skin. Proc. Amer. Soc. Hort. Sci. 74, 72–81.
29. De Bondt, A., Eggermont, K., Druart, P., De Vil, M., Goderis, I., Vanderleyden, J., and Broekaert, W.F. (1994)Agrobacterium-mediated transformation of apple (Malus x domestica Borkh.): an assessment of factors affecting gene transfer efficiency during early transformation steps. Plant Cell Rep. 13, 587–593.
30. De Bondt, A., Eggermont, K., Penninckx, I., Goderis, I., and Broekaert, W.F. (1996) Agrobacteriummediated transformation of apple (Malus x domestica Borkh.): an assessment of factors affecting regeneration of transgenic plants. Plant Cell Rep. 15, 549–554.
31. Doerr, B.I., Glomot, R., Kief, H., Kramer, M., and Sakaguchi, T. (1980) Toxicology of cefotaxime in comparison to other cephalosporins. J. Antimicrob. Chemother. 6, 79–82.PubMed
32. Donson, J., Keamey, C.M., Turpen, T.H., Khan, I.A., Kurath, G., Turpen, A.M., Jones, G.E., Dawson, W.O., and Lewandowski, D.J. (1993) Broad resistance to tobamoviruses is mediated by a modified tobacco mosaic virus replicase transgene. Mol. Plant-Microbe Interactions 6, 635–642.
33. During, K., Porsch, P., Fladung, M., and Lorz, H. (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Erwinia amylovora. Plant J. 3, 587–598..
34. Food and Agriculture Organization of the United Nations (1998) Production Yearbook for 1997. FAO, Rome. Fasolo, F., Zimmerman, R.H., and Fordham I (1989) Adventitious shoot formation on excised leaves of in vitro grown shoots of apple cultivars. Plant Cell Tissue Organ Cult. 16, 75–87.
35. Forsline, P.L. (1983) Winter hardiness of common New York apple varieties. Proc. N.Y. State Hort. Soc. 128, 20–42.
36. Gallagher, S.R. (ed.) (1992) GUS Protocol: Using the GUS Gene as a Reporter of Gene Expression, Academic Press, New York.
37. Gebhardt, S.E., Cutrufelli, R., and Matthews. R.H. (1982) Composition of foods…Fruits and fruit juices. U.S. Dept. Agr., Agr. Handbook 8–9 (rev), Washington, DC.
38. Gercheva, P., Zimmerman, R.H., Owens, L.D., Berry, C., and Hammerschlag, F.A. (1994) Particle bombardment of apple leaf explants influences adventitious shoot formation. HortScience 29, 1536–1538.
39. Gmitter, F.G. Grosser, J.W., and Moore, G.A. (1992) Citrus, in F.A. Hammerschlag and R.E. Litz (eds.), Biotechnology ofPerennial Fruit Crops, CAB Intl., Wallinford, pp. 335–369.
40. Golemboski, D.B., Lomonossoff, G.P., and Zaitlin, M. (1990) Plants transformed with a tobacco mosaic virus non-structural gene sequence are resistant to the virus. Proc. Natl. Acad. Sci. USA 87, 6311–6315.PubMed
41. Gray, J., Picton, S., Shabbeer, J., Schuch, W., and Grierson, D. (1992) Molecular biology of fruit ripening and its manipulation with antisense genes. Plant Mol Biol. 19, 69–87.PubMed
42. Hammerschlag, F.A. and Smigocki, A.C. (1998) Growth and in vitro propagation of peach plants transformed with the shooty mutant strain ofAgrobacterium tumefaciens. HortScience 33, 897–899.
43. Hammerschlag, F.A., Zimmerman, R.H., Yadava, U.L., Hunsucker, S., and Gercheva, P. (1997) Effect of antibiotics and exposure to an acidified medium on the elimination of Agrobacterium tumefaciens from apple leaf explants and on shoot regeneration. J. Amer. Soc. Hort. Sci. 122, 758–763.
44. Haseloff, J., and Amos, B. (1995) GFP in plants. Trends Genet. 11, 328–329.PubMed
45. Haseloff, Jl, Siemering, K.R., Prasher, D.C., and Hodge, S. (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. USA 94, 2122–2127.PubMed
46. Hassan, M., Sinden, S.S., Kobayashi, R.S., Nordeen, R.O., and Owens, L.D. (1993) Transformation of potato (Solanum tuberosum) with a gene for an anti-bacterial protein, cecropin. Acta Hort. 336, 127–131.
47. Hemmat, M., Weeden, N.F., and Brown, S.K. (1995) Molecular markers for the scab resistance (Vf) region in apple. HortScience 30, 850.
48. Hemmat, M., Weeden, N.F., Aldwinckle, H.S., and Brown, S.K. (1998) Molecular markers for the scab resistance (V1) region in apple. HortScience 123, 992–996.
49. Hemmat, M., Weeden, N.F., Conner, P.J., and Brown, S.K. (1997) A DNA marker for columnar growth habit in apple contains a simple sequence repeat. J. Amer. Soc. flort. Sci. 122. 347–349.
50. Hightower, R., Baden, C., Penzes, E., Lund, P., and Dunsmuir, P. (1991) Expression of antifreeze proteins in transgenic plants. Plant Mol. Biol. 17, 1013–1021.PubMed
51. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J., and Schilperoort, R.A. (1983) A binary plant vector strategy based on separation of vir-and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303, 179–180.
52. Hokanson, S.C., McFerson, J.R., Forsline, P.L., Lamboy, W.F., Luby, J.J., Djangaliev, A.D., and Aldwinckle, H.S. (1997) Collecting and managing wild Malus gennplasm in its center of diversity. HortScience 32, 173–176.
53. Holefors, A., Zhongtian, X., and Welander, M. (1998) Transformation of the apple rootstock M26 with the rolA gene and its influence on growth. Plant Sci. 136, 69–78.
54. Hood, E.E., Helmer, G.C., Fraley, R.T., and Chilton, M.D. (1986) The hypovirulence ofAgrobacterium tumefaciensA281 is encoded in the region of pTiBo542 outside the T-DNA. J. Bacteriol. 168, 1291–1301.PubMed
55. Howe, G.H. and Robinson, W.B. (1946) Ascorbic acid content of apple varieties and seedlings at Geneva, N.Y., in 1944–1945. Proc. Amer. Soc. Hort. Sci. 48, 133–136.
56. Hu, E.-Y., Chee, P.P., Chesney, R.H., Zhou, J.H., Miller, P.D., and O’Brien, W.T. (1990) GUS-like activities in seed plants. Plant Cell Rep. 9, 1–5.
57. Hu, W. and Cheng, C: L. (1995) Expression ofAeguorea green fluorescent protein in plants cells. FEBS Lett. 369, 331–334.
58. Huang, Y., Nordeen, R.O., Di, M., Owens, L.D., and McBeath, J.H. (1997) Expression of an engineered cecropin gene cassette in transgenic tobacco plants confers disease resistance to Pseudomonas syringae pv. tabaci. Mol. Plant PathoL 87, 494–499.
59. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., and Thomashow, M.F. (1998) Arabidopsis CBFIoverexpression induces COR genes and enhances freezing tolerance. Science 280, 104–106.PubMed
60. James, D.J. (1991) Agrobacterium-mediated transformation of apple (Malus pumila Mill.), in M.R. Abuja, (ed.), Woody Plant Biotechnology, Plenum Press, New York, pp. 213–226.
61. James, D.J. and Dandekar, AM. (1991) Regeneration and transformation of apple (Malus pumila Mill.), in K. Lindsey (ed.), Plant Tissue Culture Manual: Fundamentals and Application. Vol. B Kluwer Academic Publishers, Dordrecht, pp. 1–18.
62. James, D.J., Passey, A.J. and Barbara, D.J. (1990) Regeneration and transformation of apple and strawberry using disarmed Ti-binary vectors. Acta Hort. 280, 495–502.
63. James, D.J., Passey, A.J., and Malhotra, S.B. (1984) Organogenesis in callus derived from stem and leaf tissues of apple and cherry rootstocks. Plant Cell Tissue Organ Cult. 3, 333–341.
64. James, D.J., Passey, A.J., and Rugini, E. (1988a) Factors affecting high frequency plant regeneration from apple leaf tissues cultured in vitro. J. PlantPhysiol. 132, 148–154.
65. 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.
66. James, D.J., Passey, Ai., Barbara, D.J. and Bevan, M. (1989). Genetic transformation of apple (Malus pumila Mill.) using a disarmed Ti-binary vector. Plant Cell Rep. 7, 658–661.
67. James, D.J., Passey, A.J., Predieri, S., and Rugini, E. (1988b) Regeneration and transformation of apple plants using wild-type and engineered plasmids in Agrobacterium spp., in M.R. Ahuja (ed.), Somatic Cell Genetics of Woody Plants, Kluwer Academic Publishers, The Hague, pp. 65–71.
68. James, D.J., Uratsu, S., Cheng, J., Negri, P., Viss, P., and Dandekar, AM. (1993) Acetosyringone and osmoprotectants like betaine or proline synergistically enhance Agrobacterium-mediated transformation of apple. Plant Cell Rep. 12, 559–563.
69. Janick,J., Emerson, F.H., Pecknold, P.C., Korban, S.S., and Dayton, D.F. (1988) ‘Williams Pride’ apple. HortScience23, 928–930.
70. Jaynes, J.M., Nagpala, P., Destefano-Beltran, L., Hong Huang, J., Kin, J. Denny, T. and Cetiner, S. (1993) Expression of a cecropin B lytic peptide analog in transgenic tobacco confers enhanced resistance to bacterial wilt caused by Pseudomonas solanacearum. Plant Sci. 89, 43–53.
71. Jefferson, RA, Kavanagh, T.A., and Bevan, M.W. (1987) GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907.PubMed
72. Jin, S., Komari, T., Gordon, M.P., and Nester, E.W. (1987) Genes responsible for the supervirulence phenotype ofAgrobacterium tumefaciens A281. J. Bacteriol. 169, 4417–4425.PubMed
73. Jones, AL. and Aldwinckle, H.S. (1990) Compendium of Apple and Pear Diseases. American Phytopathological Society, St. Paul, MN.
74. Jones, J.D.G., Dean, C. Gidoni, D., Gilbert, D., Bond-Nutter, D., Lee, Bedbrook, J., and Dunsmuir, P. (1988) Expression of bacterial chitinase protein in tobacco leaves using two photosynthetic gene promoters. Mol. Gen. Genet. 212, 536–542.
75. Kitts, P., Adams, M., Kondepudi, A, Gallagher, C., and Kain, S. (1995) Green fluorescent protein (GFP): a novel reporter for monitoring gene expression in living cells and organisms. Clontechniques 10, 1–3.
76. Ko, K., Brown, S.K., Norelli, J.L., and Aldwinckle, H.S. (1998a) Alterations in nptIl and gus expression
77. following micropropagation of transgenic M.7 apple rootstock lines. J. Amer. Soc. Hort. Sci. 123, 11–18.
78. Ko, K., Grethel, A, Timur Momol, M., Norelli, J.L., and Aldwinckle, H.S. (1998b) Enhanced resistance to fire blight (Erwinia amylovora) of Gala apple lines transgenic for lytic protein genes. Abstr. Intl. Cong. Plant Cell Tissue Culture9, 127.
79. Korban, S.S. (1986) Interspecific hybridization in Malus. HortScience 21, 41–48.
80. Korban, S.S. and Chen, H. (1992) Apple, in F.A. Hammerschlag and R.E. Litz (eds.), Biotechnology of Perennial Fruit Crops, CAB, Wallingford, pp. 203–227.
81. Korban, S.S. and O’Connor, P.A. (1990) Disease resistant apple cultivars developed from the apple breeding program at the University of Illinois. Illinois Agri. Exper. Stat. Bull, no. 790.
82. Korban, S.S. and Skirvin, R.M. (1984) Nomenclature of the cultivated apple. HortScience 19, 177–180.
83. 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. J. Hort. Sci. 67, 341–349.
84. Kosugi, S., Ohashi, Y., Nakajima, K., and Arai, Y. (1990) An improved assay for p-glucuronidase in transformed cells: Methanol almost completely suppresses a putative endogenous ß-glucuronidase activity. Plant Sci. 70, 133–140.
85. Lamb, R.C. (1974) Future gennplasm resources of pome fruits. Fruit Var. J. 28, 75–79.
86. Lambert, C. and Tepfer, D. (1991) Use ofAgrobacterium rhizogenes to create chimeric apple trees through genetic grafting. Bio/Technology 9, 80–83.
87. Lambert, C. and Tepfer, D. (1992) Use ofAgrobacterium rhizogenes to create transgenic apple trees having an altered organogenic response to hormones. Theor. Appl. Genet. 85, 105–109.
88. Lapins, K. (1969) Separation of compact growth types in certain apple seedlings progenies. Can. J. Plant Sci. 49, 765–768.
89. Liu, D., Raghothama, K.G., Hasegawa, P.M., and Bressan, R.A. (1994) Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad. Sci. USA 91, 1888–1892.PubMed
90. Liu, Q., Salih, S., and Hammerschlag, F. (1998) Etiolation of ‘Royal Gala’ apple (Malus x domestica Borkh.) shoots promotes high-frequency shoot organogenesis and enhanced ß-glucuronidase expression from stem intemodes. Plant Cell Rep. 17. (In press)
91. Liu, Q., and Hammerschlag, F.A. (1998) Exogenous application of auxin enhances Agrobacteriummediated transformation efficiency of etiolated intemodes from ‘Royal Gala’ apple. In Vitro Cell. Dev. Biol. 34, 75A.
92. Lodge, J.K., Kaniewski, W.K., and Turner, N.E. (1993) Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein. Proc. Natl. Acad. Sci USA 90, 7089–7093.PubMed
93. Logemann, J., Jach, G. Tommerup, H., Mundy, J., and Schell, J. (1992) Expression of a ribosome-inactivating protein leads to increased fungal protection in transgenic tobacco plants. Bio/Technology 10, 305–308.
94. Lorito, M., Peterbauer, C., Hayes, C.K., and Harman, G.E. (1994) Synergistic interaction between fungal cell wall degrading enzymes and different antifungal compounds enhances inhibition of spore germination. Microbiol. 140, 623–629.
95. Maheswaran, G., Welander, M., Hutchinson, J.F., Graham, M.W., and Richards, D. (1992) Transformation of apple rootstock M26 with Agrobacterium tumefaciens. J. Plant Physiol. 39, 560–568.
96. Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D., and Tanksley, S.D. (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science262, 1432–1436.PubMed
97. Martin, G.C., Miller, A.N., Castle, L.A., Morris, J.W., Morris, R.O., and Dandekar, A.M. (1990) Feasibility studies using (i-glucuronidase as a gene fusion marker in apple, peach, and radish. J. Amer. Soc. Hort. Sci. 115, 689–691.
98. Martin, T., WBhner, R, Hummel, S., Willmitzer, L, and Frommer, W.B. (1992) The GUS reporter system as a tool to study plant gene expression, in S.R. Gallagher (ed.), GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression, Academic Press, New York, pp. 23–43.
99. Mathias, R.J. and Mukasa. (1987) The effects of cefotaxime on the growth and regeneration of callus from four varieties of barley (Hordeum vulgare L.) Plant Cell Rep. 6, 454–457.
100. Matzk, A., Mantell, S., and Shiemann, J. (1996) Localization of persisting agrobacteria in transgenic tobacco plants. Mol. Plant Microbe Interact. 9, 373–381.
101. Maximova, S.N., Dandekar, A.M., and Guiltinan, M.J. (1998) Investigation ofAgrobacterium-mediatedtransformation of apple using green fluorescent protein: high transient expression and low stable transformation suggest that factors other than T-DNA transfer are rate limiting. Plant Mol. Biol. 37, 549–559.PubMed
102. Mills, D., Hammerschlag, F.A., Nordeen, RO., and Owens, L.D. (1994) Evidence for the breakdown of cecropin B by proteinases in the intercellular fluid of peach leaves. Plant Sci. 104, 17–22.
103. Niedz, R., Sussman, M., and Satterlee, J. (1995) Green fluorescent protein: an in vivo reporter of plant gene expression. Plant Cell Rep. 14, 403–407.
104. Norelli, J.L and Aldwinckle, H.S. (1993) The role of aminoglycoside antibiotics in the regeneration and selection of neomycin phosphotransferase-transgenic apple tissue. J. Amer. Soc. Hort. Sci. 118, 311–316.
105. Norelli, J.L., Aldwinckle, H.S., Destefano-Beltran, L., and Jaynes, J.M. (1994) Transgenic ‘Mailing 26’ apple expressing the attacin E gene has increased resistance to Erwinia amylovora. Euphytica 77, 123–128.
106. Norelli, J.L., Aldwinckle, H.S., Destefano-Beltran, L., and Jaynes, J.M. (1994) Transgenic ‘Mailing 26’ apple expressing the attacin E gene has increased resistance to Erwinia amylovora. Euphytica 77, 123–128.
107. Norelli, J.L., Ko, K., Bolar, J.P., Hannan, G.E., Hrazdina, G.E., and Aldwinckle, H.S. (1997) Genetic engineering of apple for improved disease resistance and horticultural quality. Korean Soc. Hort. Sci. 15, 7–11.
108. Norelli, J.L., Mills, J., and Aldwinckle, H.S. (1996) Leaf wounding increases efficiency ofAgrobacteriummediated transformation of apple. HortScience 3, 1026–1027.
109. Norelli, J.L., Mills, J.Z., Jensen, L.A., Momol, M.T., and Aldwinckle, H.S. (1998) Genetic engineering of apple for increased resistance to fire blight. Acta Hort. (In press)
110. Oppenheimer, C. and Slor, E. (1968) Breeding of apples for a sub-tropical climate. Theor. Appl. Genet. 38, 97–102.
111. Owens, L.D. (1995) Overview of gene availability, identification, and regulation. HortScience 30, 957–961.
112. Owens, L.D. and Heutte, T. (1997) A single amino acid substitution in the antimicrobial defense protein cecropin B is associated with diminished degradation by leaf intercellular fluid. Mol. Plant Microbe Interactions 10, 525–528.
113. Penarrubia, L, Kim, R., Giovannoni, J., Kim, S.-H., and Fischer, R.L. (1992) Production of the sweet protein monellin in transgenic plants. Bio/Technology 10, 561–564.
114. Perlak, F.J., Fuchs, R.L, Dean, D.A, McPherson, S.L., and Fischhoff, D.A. (1991) Modification of the coding sequence enhances plant expression of insect control protein genes. Proc. Natl. Acad. Sci. USA 88, 3324–3328.PubMed
115. Pollack, K., Barfield, D.G., and Shields, R. (1983) The toxicity of antibiotics to plant cell cultures. Plant Cell Rep. 2, 36–39.
116. Ponomarenko, V.V. (1986) Review of the species in the genus Malus Mill. Bull. Appl. Bot. Genet. Breed. 106, 3–27.
117. Predieri, S. and Malavasi, F.F. (1989) High-frequency shoot regeneration from leaves of the apple rootstock M26 (Malus pumila Mill.) Plant Cell Tissue Organ Cult. 17, 133–142.
118. Puite, K.J. and Schaart, J.G. (1996) Genetic modification of the commercial apple cultivars Gala, Golden Delicious and Elstar via an Agrobacterium tumefaciens-mediated transformation method. Plant Sci. 119, 125–133.
119. Ragan, W.H. 1926. Nomenclature of the apple: a catalogue index of the known varieties referred to in American publications from 1804 to 1904. USDA Bur. Plant Ind. Bull. 56, Washington, DC. Rehder, A. (1940)Manual ofCultivated Trees and Shrubs. Arnold Arboretum of Harvard University, Jamaica Plain.
120. Rouwendal, G.J., Mendes, O., Wolbert, E.M., and Douwe de Boer, A. (1997) Enhanced expression in tobacco of the gene encoding green fluorescent protein by modification of its codon usage. Plant Mol. Biol. 33, 989–999.PubMed
121. Sanders, R. (1988) The Apple Book, Philosophical Library, New York.
122. Sangwan, R.S., Bourgeois, Y., and Sangwan-Norreel, B.S. (1991) Genetic transformation ofArabidopsis thalianazygotic embryos and identification of critical parameters influencing transformation efficiency. MoLGen.Genet. 230, 475–485.
123. Schaart, J.G., Puite, K.J., Kolova, L., and Pogrebnyak, N. (1995) Some methodological aspects of apple transformation by Agrobacterium. Euphytica 85, 131–134.
124. Singh, Z. and Sansavini, S. (1998) Genetic transformation and fruit crop improvement. Plant Breeding Rev. 16, 87–134.
125. Smigocki, AC. (1991) Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene. Plant Mol. Biol. 16, 105–115.PubMed
126. Smigocki, A., Neal., J.W., McCanna, I, and Douglass, L. (1993) Cytokinin-mediated insect resistance in Nicotianaplants transformed with the ipt gene. Plant Mol. Biot. 23, 325–335.
127. Sriskandarajah, S. and Goodwin, P.B. (1998) Conditioning promotes regeneration and transformation in apple leaf explants. Plant Cell Tissue Organ Cult. 53, 1–11.
128. Sriskandarajah, S., Goodwin, P.B., and Speirs, J. (1994) Genetic transformation of apple scion cultivar ‘Delicious’ via Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult. 36, 317–329.
129. Sriskandarajah, S., Skirvin, R.M., Abu-Qaoud, H., and Korban, S.S. (1990) Factors involved in shoot elongation and growth of adventitious and axillary shoots of three apple scion cultivars in vitro. J. Hort. Sci. 65, 113–121.
130. Strang, J.C. and Stushnoff, C. (1975) A classification of hardy North American apple cultivars based on hardiness zones. Fruit Var. J. 29, 78–108.
131. Swartz, H.J., Bors, R., Mohamed, F., and Naess, S.K. (1990) The effect of in vitro pretreatments on subsequent shoot organogenesis from excised Rubus and Malus leaves. Plant Cell Tissue Organ Cult. 21, 179–184.
132. Tarczynski, M.C. Jensen, R.G., and Bohnert, H.J. (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508–510.
133. Tydeman, H.M. (1964) The relation between time of leaf break and of flowering in apple seedlings. Rep. E. Mailing Res. Stn. For 1963, 70–72.
134. USDA (1960) Index of plant diseases in the United States. Agr. Handbook 165, 384–389.
135. Van Camp, W., Willekens, H., Bowler, C., Van Montagu, M., Inze, D., Reupold-Popp, P., Sandermann, H., and Langebartels, C., (1994) Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. Bio/Technology 12, 165–168.
136. Vancanneyt, G., Schmidt, R., O’Connor-Sanchez, A., Willmitzer, L., and Rocha-Sosa, M. (1990) Construction of an intron-containing marker gene:Splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation. Mol. Gen. Genet. 220, 245–250.PubMed
137. Vemade, D., Herrera-Estrella, A., Wang, K., and Van Montagu, M. (1988) Glycine betaine allows enhanced induction of the Agrobacterium tumefaciens vir genes by acetosyringone at low pH. J. Bacteriol. 170, 5822–5829.
138. Watkins, R. (1976) Apple and pear, in N.E. Simmonds (ed.), Evolution of Crop Plants, Longman, New York, pp. 247–250.
139. Watkins, R. and Spangelo, L.P. (1970) Components of genetic variance for plant survival and vigour of apple trees. Theor. Appl. Genet. 40, 195–203.
140. Way, R.D., Aldwinckle, H.S., Lamb, R.C., Rejman, A., Sansavini, S., Shen,T.,Watkins, R., Westwood, M.N., and Yoshida, Y. (1991) Apples (Malus), in J.N. Moore and J.R. Ballington (eds.), Genetic Resources of Temperate Fruit and nut Crops, Intl. Soc. Hort. Sci. Wageningen, pp. 1–62 (Acta Hort. 290 ).
141. Welander, M. (1988) Plant regeneration from leaf and stem segments of shoots raised in vitro from mature apple trees. J. Plant Physiol. 32, 738–744.
142. Welander, M. and Maheswaran, G. (1991) Regeneration and transformation in apple, in M.R. Ahuja (ed.), Woody Plant Biotechnology, Plenum Press, New York, pp. 237–246.
143. Welander, M. and Maheswaran, G. (1992) Shoot regeneration from leaf explants of dwarfing apple rootstocks. J. Plant Physiol. 140, 223–228.
144. Westwood, M.N. (1978) Temperate-Zone Pomology, Freeman, San Francisco.
145. Wilcox, A.N. (1962) The apple, in H. Kappert and W. Rudorf (eds.), Handbuch der Planzenzuchtung, 2nd ed. Vol. 6, Parey, Berlin, pp. 637–645.
146. Wilcox, W.F., Riedl, H., and Stiles, W.C. (1986) Tree-Fruit Production Recommendations, N.Y. State College of Agric. and Life Sciences, Cornell Univ., Ithaca, NY.
147. Wilson, K.J., Hughes, S.G., and Jefferson, R.A. (1992) The Escherichia coli gus Operon: Induction and expression of the gus operon in E. coli and the occurrence and use of GUS in other bacteria, in S. R. Gallagher (ed.), GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression, Academic Press, New York, pp. 7–22.
148. Wise, R., Rollason, T., Logan, M., Andrews, J.M., and Bedford, K.A. (1978) HR 756, a highly active cephalosporin: Comparison with cefazolin and carbenicillin. Antimicrob. Agents Chemother. 14, 807–811.PubMed
149. Yao, J., Cohen, D., Atkinson, R., Richardson, K., and Morris, B. (1995) Regeneration of transgenic plants from the commercial apple cultivar Royal Gala. Plant Cell Rep. 14, 407–412.
150. Yepes, L. and Aldwinckle, H.S. (1994) Factors that affect leaf regeneration efficiency in apple, and effect of antibiotics in morphogenesis. Plant Cell Tissue Organ Cult. 37, 257–269.
151. Yoshida, Y. (1986) Quality improvement in apple breeding in Japan. Proc. Plant Breed. Symp., Dept. Sci. Indust. Res., Agron. Soc. New Zealand Spec. Pub. 5, 255–257.
152. Yoshikura, H. (1989) Suppression of focus formation by bovine papillomavirus-transformed cells by contact with non-transformed cells: Involvement of sugar(s) and phosphorylation. Intl. J. Cancer 44, 885–891.
153. Zhu, B., Chen, T.H.H., and Li, P.H. (1996) Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198, 70–77.PubMed
154. Zhu, Q., Mahler, E.A., Masoud, S., Dixon, R., and Lamb, C.J. (1994) Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Bio/Technol. 12, 807–812.

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