Plant Molecular Biology

, Volume 26, Issue 3, pp 781–790

Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase

  • Xin Good
  • Jill A. Kellogg
  • Wendy Wagoner
  • Dan Langhoff
  • Wendy Matsumura
  • Richard K. Bestwick
Research Articles

Abstract

We have utilized a gene from bacteriophage T3 that encodes the enzyme S-adenosylmethionine hydrolase (SAMase) to generate transgenic tomato plants that produce fruit with a reduced capacity to synthesize ethylene. S-adenosylmethionine (SAM) is the metabolic precursor of 1-aminocyclopropane-1-carboxylic acid, the proximal precursor to ethylene. SAMase catalyzes the conversion of SAM to methylthioadenosine and homoserine. To restrict the presence of SAMase to ripening fruit, the promoter from the tomato E8 gene was used to regulate SAMase gene expression. Transgenic tomato plants containing the 1.1 kb E8 promoter bore fruit that expressed SAMase during the breaker and orange stage of fruit ripening and stopped expression after the fruit fully ripened. Plants containing the 2.3 kb E8 promoter expressed SAMase at higher levels during the post-breaker phases of fruit ripening and had a substantially reduced capacity to synthesize ethylene.

Key words

Ethylene ripening S-adenosylmethionine hydrolase SAMase tomato transgenic 

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References

  1. 1.
    Adams, DO, Yang, SF: Methionine metabolism in apple tissue: implication of S-adenosylmethionine as an intermediate in the conversion of methionine to ethylene. Plant Physiol 70: 117–123 (1977).Google Scholar
  2. 2.
    An, G, Ebert, P, Mitra, A, Ha, SB: Binary vectors. In: Plant Molecular Biology Manual A3: 1–19 Kluwer Academic Publishers, Dordrecht (1988).Google Scholar
  3. 3.
    An, G, Watson, BD, Stachel, S, Gordon, MP, Nester, EW: New cloning vehicles for transformation of higher plants. EMBO J 4: 277–284 (1985).Google Scholar
  4. 4.
    Benfey, PN, Chua, NH: The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250: 959–966 (1990).Google Scholar
  5. 5.
    Deikman, J, Fischer, RL: Ihteraction of a DNA binding factor with the 5′-flanking region of an ethylene-responsive fruit ripening gene from tomato. EMBO J 7: 3315–3320 (1988).PubMedGoogle Scholar
  6. 6.
    Deikman, J, Kline, R, Fischer, R: Organization of ripening and ethylene regulatory regions in a fruit-specific promoter from tomato (Lycopersicon esculentum). Plant Physiol 100: 2013–2017 (1992).Google Scholar
  7. 7.
    Fillatti, JJ, Kiser, J, Rose, R, Comai, L: Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Bitechnology 5: 726–730 (1987).Google Scholar
  8. 8.
    Sambrook, J, Fritsch, EF, Maniatis, T: Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 1989.Google Scholar
  9. 9.
    Gallie, DR: Posttranscriptional regulation of gene expression in plants. Ann Rev Plant Physiol Plant Mol Biol 44: 77–105 (1993).CrossRefGoogle Scholar
  10. 10.
    Giovannoni, JJ, DellaPenna, D, Bennett, AB, Fischer, RL: Expression of a chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell 1: 53–63 (1989).CrossRefPubMedGoogle Scholar
  11. 11.
    Good X, Matsumura W, Langhoff D, Kellogg J, Clough G, Bestwick RK: Delayed and modified ripening by tomatoes expressing S-adenosylmethionine hydrolase. Manuscript submitted (1994).Google Scholar
  12. 12.
    Guy, M, Kende, H: Conversion of 1-aminocyclopropane-1carboxylic acid to ethylene by isolated vacuoles of the Pisum sativum L. Planta 160: 281–287 (1984).CrossRefGoogle Scholar
  13. 13.
    Guy, M, Kende, H: Ethylene formation in Pisum sativum and Vicia faba protoplasts. Planta 160: 276–280 (1984).CrossRefGoogle Scholar
  14. 14.
    Hamilton, AJ, Lycett, GW, Grierson, D: Antisense gene that inhibits the synthesis of the hormone ethylene in transgenic plants. Nature 346: 284–287 (1990).CrossRefGoogle Scholar
  15. 15.
    Hausmann, R.: The T7 Group. In: Calender, R (ed) The Bacteriophages. Plenum Press, New York (1988).Google Scholar
  16. 16.
    Hood, E, Helmer, GL, Fraley, RT, Chilton, MD: The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J Bact 168: 1291–1301 (1986).PubMedGoogle Scholar
  17. 17.
    Hughes, JA, Brown, LR, Ferro, AJ: Expression of cloned coliphage T3 S-adenosylmethionine hydrolase gene inhibits DNA methylation and polyamine biosynthesis in E. coli. J Bact 169: 3625–3632 (1987).PubMedGoogle Scholar
  18. 18.
    Hughes, JA, Brown, LR, Ferro, AJ: Nucleotide sequence analysis of the coliphage T3 S-adenosylmethionine hydrolase gene and its surrounding ribonuclease III processing sites. Nucl Acid Res 15: 717–729 (1987).Google Scholar
  19. 19.
    Imaseki H: The biochemistry of ethylene biosynthesis. In: Matoo AK, Suttle JC (eds) The Plant Hormone Ethylene, pp. 1–20. CRC Press (1991).Google Scholar
  20. 20.
    Joshi, CP: An Inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl Acid Res 16: 6643–6653 (1987).Google Scholar
  21. 21.
    Kende, H: Enzymes of ethylene biosynthesis. Plant Physiol 91: 1–4 (1989).Google Scholar
  22. 22.
    Kende, H: Ethylene biosynthesis. Ann Rev Plant Physiol Plant Mol Biol 44: 283–307 (1993).CrossRefGoogle Scholar
  23. 23.
    Klee, HJ, Hayford, MB, Kretzmer, KA, Barry, GF, Kishore, GM: Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell 3: 1187–1193 (1991).PubMedGoogle Scholar
  24. 24.
    Kozak, M: Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol Cell Biol 9: 5073–5080 (1989).PubMedGoogle Scholar
  25. 25.
    Kushad, MM, Richardson, DG, Ferro, AJ: Intermediates in the recycling of 5-methylthioribose to methionine in fruits. Plant Physiol 73: 257–261 (1983).Google Scholar
  26. 26.
    Lincoln, JE, Cordes, S, Read, E, Fischer, RL: Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. Proc Natl Acad Sci USA 84: 2793–2797 (1987).PubMedGoogle Scholar
  27. 27.
    Lutcke, HA, Chow, KC, Mickel, FS, Moss, KA, Kern, HF Scheele, GA: Selection of AUG initiation codons differs in plants and animals. EMBO J 6: 43–48 (1987).PubMedGoogle Scholar
  28. 28.
    Nagel, R, Elliot, A, Masel, A, Birch, RG, Manners, JM: Electroporation of binary Ti plasmid vector into Agrobacterium tumefaciens and Agrobacterium rhizogenes. FEMS Microbiol Lett 67: 325–327 (1990).CrossRefGoogle Scholar
  29. 29.
    Oeller, PW, Lu, MW, Taylor, LP, Pike, DA, Theologis, A: Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254: 437–439 (1991).PubMedGoogle Scholar
  30. 30.
    Picton, S, Barton, SL, Bouzayen, M, Hamilton, AJ, Grierson, D: altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J 3: 469–481 (1993).Google Scholar
  31. 31.
    Spoeler, N, Herrlich, P: Colivirus-T3-coded S-adeno-sylmethionine hydrolase. Eur J Biochem 95: 227–233 (1979).PubMedGoogle Scholar
  32. 32.
    Studier, FW, Movva, NR: SAMase gene of bacteriophage T3 is responsible for overcoming host restriction. J Virol 19: 136–145 (1976).PubMedGoogle Scholar
  33. 33.
    Theologis, A: One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell 70: 181–184 (1992).CrossRefPubMedGoogle Scholar
  34. 34.
    Usdin, E, Borchardt, RT, Creveling, CR: Transmethylation. Elsevier/North Holland Publishing Co., New York (1979).Google Scholar
  35. 35.
    Ward, TM, Wright, M, Roberts, JA, Self, R, Osborne, DJ: Analytical procedures for the assay and identification of ethylene. In: Hillman, J (ed) Isolation of Plant Growth Substances, pp. 135–151. Cambridge University Press, Cambridge (1978).Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Xin Good
    • 1
  • Jill A. Kellogg
    • 1
  • Wendy Wagoner
    • 1
  • Dan Langhoff
    • 1
  • Wendy Matsumura
    • 1
  • Richard K. Bestwick
    • 1
  1. 1.Agritope, Inc.BeavertonUSA

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