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.
Similar content being viewed by others
References
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).
An, G, Ebert, P, Mitra, A, Ha, SB: Binary vectors. In: Plant Molecular Biology Manual A3: 1–19 Kluwer Academic Publishers, Dordrecht (1988).
An, G, Watson, BD, Stachel, S, Gordon, MP, Nester, EW: New cloning vehicles for transformation of higher plants. EMBO J 4: 277–284 (1985).
Benfey, PN, Chua, NH: The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250: 959–966 (1990).
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).
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).
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).
Sambrook, J, Fritsch, EF, Maniatis, T: Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 1989.
Gallie, DR: Posttranscriptional regulation of gene expression in plants. Ann Rev Plant Physiol Plant Mol Biol 44: 77–105 (1993).
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).
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).
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).
Guy, M, Kende, H: Ethylene formation in Pisum sativum and Vicia faba protoplasts. Planta 160: 276–280 (1984).
Hamilton, AJ, Lycett, GW, Grierson, D: Antisense gene that inhibits the synthesis of the hormone ethylene in transgenic plants. Nature 346: 284–287 (1990).
Hausmann, R.: The T7 Group. In: Calender, R (ed) The Bacteriophages. Plenum Press, New York (1988).
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).
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).
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).
Imaseki H: The biochemistry of ethylene biosynthesis. In: Matoo AK, Suttle JC (eds) The Plant Hormone Ethylene, pp. 1–20. CRC Press (1991).
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).
Kende, H: Enzymes of ethylene biosynthesis. Plant Physiol 91: 1–4 (1989).
Kende, H: Ethylene biosynthesis. Ann Rev Plant Physiol Plant Mol Biol 44: 283–307 (1993).
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).
Kozak, M: Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol Cell Biol 9: 5073–5080 (1989).
Kushad, MM, Richardson, DG, Ferro, AJ: Intermediates in the recycling of 5-methylthioribose to methionine in fruits. Plant Physiol 73: 257–261 (1983).
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).
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).
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).
Oeller, PW, Lu, MW, Taylor, LP, Pike, DA, Theologis, A: Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254: 437–439 (1991).
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).
Spoeler, N, Herrlich, P: Colivirus-T3-coded S-adeno-sylmethionine hydrolase. Eur J Biochem 95: 227–233 (1979).
Studier, FW, Movva, NR: SAMase gene of bacteriophage T3 is responsible for overcoming host restriction. J Virol 19: 136–145 (1976).
Theologis, A: One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell 70: 181–184 (1992).
Usdin, E, Borchardt, RT, Creveling, CR: Transmethylation. Elsevier/North Holland Publishing Co., New York (1979).
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).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Good, X., Kellogg, J.A., Wagoner, W. et al. Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase. Plant Mol Biol 26, 781–790 (1994). https://doi.org/10.1007/BF00028848
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00028848