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Accumulation of wound-inducible ACC synthase transcript in tomato fruit is inhibited by salicylic acid and polyamines

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Abstract

Regulation of wound-inducible 1-aminocyclopropane-1-carboxylic acid (ACC) synthase expression was studied in tomato fruit (Lycopersicon esculentum cv. Pik-Red). A 70 base oligonucleotide probe homologous to published ACC synthase cDNA sequences was successfully used to identify and analyze regulation of a wound-inducible transcript. The 1.8 kb ACC synthase transcript increased upon wounding the fruit as well as during fruit ripening. Salicylic acid, an inhibitor of wound-responsive genes in tomato, inhibited the wound-induced accumulation of the ACC synthase transcript. Further, polyamines (putrescine, spermidine and spermine) that have anti-senescence properties and have been shown to inhibit the development of ACC synthase activity, inhibited the accumulation of the wound-inducible ACC synthase transcript. The inhibition by spermine was greater than that caused by putrescine or spermidine. The transcript level of a wound-repressible glycine-rich protein gene and that of the constitutively expressed rRNA were not affected as markedly by either salicylic acid or polyamines. These data suggest that salicylic acid and polyamines may specifically regulate ethylene biosynthesis at the level of ACC synthase transcript accumulation.

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References

  1. Adams DO, Yang SF: Ethylene biosynthesis: Identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci USA 76: 170–174 (1979).

    Google Scholar 

  2. Apelbaum A, Burg SP: Effect of ethylene on cell division and deoxyribonucleic acid synthesis in Pisum sativum. Plant Physiol 50: 117–124 (1972).

    Google Scholar 

  3. Apelbaum A, Burgoon AC, Anderson JD, Lieberman M, Ben-Arie R, Mattoo AK: Polyamines inhibit biosynthesis of ethylene in higher plant tissue and protoplasts. Plant Physiol 68: 453–456 (1981).

    Google Scholar 

  4. Apelbaum A, Goldlust A, Icekson I: Control by ethylene of arginine decarboxylase activity in pea seedlings and its implication for hormonal regulation of plant growth. Plant Physiol 79: 635–640 (1985).

    Google Scholar 

  5. Ben-Arie R, Lurie S, Mattoo AK: Temperature dependent inhibitory effects of calcium and spermine on ethylene biosynthesis in apple discs correlate with changes in microsomal membrane viscosity. Plant Sci Lett 24: 239–247 (1982).

    Google Scholar 

  6. Boller T, Herner RC, Kende H: Assay for and enzymatic formation of an ethylene precursor, 1-aminocyclopropane-1-carboxylic acid. Planta 145: 293–304 (1979).

    Google Scholar 

  7. Boller T: Ethylene in pathogenesis and disease resistance. In: Mattoo AK, Suttle JC (eds) The Plant Hormone Ethylene, pp. 293–314. CRC Press, Boca Raton, FL (1991).

    Google Scholar 

  8. Brady CJ: Fruit ripening. Annu Rev Plant Physiol 38: 155–178 (1987).

    Google Scholar 

  9. Burg SP, Burg EA: The interaction between auxin and ethylene and its role in plant growth. Proc Natl Acad Sci USA 55: 262–269 (1966).

    Google Scholar 

  10. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ: Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299 (1979).

    Google Scholar 

  11. Dibble ARG, Davies PJ, Mutschller MA: Polyamine content of long-keeping Alcobaca tomato fruit. Plant Physiol 86: 338–340 (1988).

    Google Scholar 

  12. Doherty HM, Selvendram RR, Bowles DJ: The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol Mol Plant Pathol 33: 377–384 (1988).

    Google Scholar 

  13. Evans PT, Malmberg RL: Do polyamines have roles in plant development? Annu Rev Plant Physiol Plant Mol Biol 40: 235–269 (1989).

    Google Scholar 

  14. Even-Chen Z, Mattoo AK, Goren R: Inhibition of ethylene biosynthesis by aminoethoxyvinylglycine and by polyamines shunts label from [3,4-14C] methionine into sperimidine in aged orange peel discs. Plant Physiol 69: 385–388 (1982).

    Google Scholar 

  15. Flores HE, Arteca RN, Shannon JC: Polyamines and Ethylene: Biochemistry, Physiology, and Interactions. American Society of Plant Physiologists, Washington, DC (1990).

    Google Scholar 

  16. Fuhrer J: Ethylene biosynthesis and cadmium toxicity in leaf tissue of beans (Phaseolus vulgaris L). Plant Physiol 70: 162–167 (1982).

    Google Scholar 

  17. Grierson D: Gene expression in ripening tomato fruit. CRC Crit Rev Plant Sci 3: 113–132 (1985).

    Google Scholar 

  18. Hyodo H: Stress/wound ethylene. In: Mattoo AK, Suttle JC (eds) The Plant Hormone Ethylene, pp. 43–63. CRC Press, Boca Raton, FL (1991).

    Google Scholar 

  19. Kende H, Boller T: Wound ethylene and 1-aminocyclopropane-1-carboxylate synthase in ripening tomato fruit. Planta 151: 476–481 (1981).

    Google Scholar 

  20. Lawyer FC, Stoffel S, Saiki RK, Mayambo KB, Drummond R, Gelfand DH: Isolation, characterization, and expression in E. coli of the DNA polymerase gene from the extreme thermophile, Thermus aquaticus. J Biol Chem 264: 6427–6437 (1989).

    Google Scholar 

  21. Leslie CA, Romani RJ: Salicylic acid: A new inhibitor of ethylene biosynthesis. Plant Cell Rep 5: 144–146 (1986).

    Google Scholar 

  22. Lieberman M: Biosynthesis and action of ethylene. Annu Rev Plant Physiol 30: 533–591 (1979).

    Google Scholar 

  23. 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).

    Google Scholar 

  24. Malamy J, Carr JP, Klessig DF, Raskin I: Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002–1004 (1990).

    Google Scholar 

  25. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  26. Mattoo AK, Adams DO, Patterson GW, Lieberman M: Inhibition of 1-aminocyclopropane-1-carboxylic acid synthase by phenothiazines. Plant Sci Lett 28: 173–179 (1982).

    Google Scholar 

  27. Mattoo AK, Aharoni N: Ethylene and plant senescence. In: Nooden L, Leopold AC (eds) Senescence and Aging in Plants, pp. 241–280. Academic Press, London (1988).

    Google Scholar 

  28. Mattoo AK, Anderson JD: Wound-induced increase in 1-aminocylcopropane-1-carboxylate synthase activity: Regulatory aspects and membrane association of the enzyme. In: Fuchs Y, Chalutz E (eds) Ethylene: Biochemistry, Physiological and Applied aspects, pp. 139–147. Martinus Nijhoff/Dr W. Junk Publishers, Amsterdam (1984).

    Google Scholar 

  29. Mattoo AK, Suttle JC: The Plant Hormone Ethylene. CRC Press, Boca Raton, FL (1991).

    Google Scholar 

  30. Mattoo AK, White B: Regulation of ethylene biosynthesis. In: Mattoo AK, Suttle JC (eds) The Plant Hormone Ethylene, pp. 21–42. CRC Press, Boca Raton, FL, (1991).

    Google Scholar 

  31. Mehta AM, Jordan RL, Anderson JD, Mattoo AK: Identification of a unique isoform of 1-aminocyclopropane-1-carboxylic acid synthase by monoclonal antibody. Proc Natl Acad Sci USA 85: 8810–8814 (1988).

    Google Scholar 

  32. Metraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B: Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006 (1990).

    Google Scholar 

  33. Minocha SC, Papa NS, Khan AJ, Samuelsen AI: Polyamines and somatic embryogenesis in carrot. III. Effects of methylglyoxal bis(guanylhydrazone). Plant Cell Physiol 32: 395–402 (1991).

    Google Scholar 

  34. Nakajima N, Mori H, Yamazaki K, Imaseki H: Molecular cloning and sequence of a complementary DNA encoding 1-aminocyclopropane-1-carboxylate synthase induced by tissue wounding. Plant Cell Physiol 31: 1021–1029 (1990).

    Google Scholar 

  35. Olson DC, White JA, Edelman L, Harkins RN, Kende H: Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. Proc Natl Acad Sci USA 88: 5340–5344 (1991).

    Google Scholar 

  36. Parsons BL, Mattoo AK: Wound regulated accumulation of specific transcripts in tomato fruit: interactions with fruit development, ethylene and light. Plant Mol Biol 17: 453–464 (1991).

    Google Scholar 

  37. Pech JC, Latche A, Larrigaudiere C, Reid MS: Control of early ethylene synthesis in pollinated petunia flowers. Plant Physiol Biochem 25: 431–437 (1987).

    Google Scholar 

  38. Roberts DR, Walker MA, Thompson JE, Dumbroff EB: The effects of inhibitors of polyamine and ethylene biosynthesis on senescence, ethylene production and polyamine levels in cut carnation flowers. Plant Cell Physiol 25: 315–322 (1984).

    Google Scholar 

  39. Sacher JA: Senescence and postharvest physiology. Annu Rev Plant Physiol 24: 197–224 (1973).

    Google Scholar 

  40. Sato T, Oeller PW, Theologis A: The 1-aminocyclopropane-1-carboxylate synthase of Cucurbita. Purification, properties, expression in Escherichia coli, and primary structure determination by DNA sequence analysis. J Biol Chem 266: 3752–3759 (1991).

    Google Scholar 

  41. Sato T, Theologis A: Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plant. Proc Natl Acad Sci USA 86: 6621–6625 (1989).

    Google Scholar 

  42. Saftner RA, Baldi BG: Polyamine levels and tomato fruit development: possible interaction with ethylene. Plant Physiol 92: 547–550 (1990).

    Google Scholar 

  43. Scalet M, Federico R, Angelini R: Time course of diamine oxidase and peroxidase activities, and polyamine changes after mechanical injury of chick-pea seedlings. J Plant Physiol 137: 571–575 (1991).

    Google Scholar 

  44. Sexton R, Roberts JA: Cell biology of abscission. Annu Rev Plant Physiol 33: 133–162 (1982).

    Google Scholar 

  45. Smith TA: Polyamines. Annu Rev Plant Physiol 36: 117–143 (1985).

    Google Scholar 

  46. Smith TA, Marshall JHA: The di- and polyamine oxidases of plants. In: Zappia V, Pegg AE (eds) Progress in Polyamine Research, pp. 573–587. Plenum Press, New York (1988).

    Google Scholar 

  47. Southern EM: Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517 (1975).

    Google Scholar 

  48. Suttle JC: Effect of polyamines on ethylene production. Phytochemistry 20: 1477–1480 (1981).

    Google Scholar 

  49. Taylorson RB, Hendricks SB: Dormancy in seeds. Annu Rev Plant Physiol 28: 331–354 (1977).

    Google Scholar 

  50. Vanden Driessche TH, Kevers C, Collet M, Gaspar TH: Acetabularia mediterranea and ethylene: production in relation with development, circadian rhythms in emission, and response to external application. J Plant Physiol 133: 635–639 (1988).

    Google Scholar 

  51. Van Der Straeten D, Van Wiemeersch L, Goodman HM, Van Montagu M: Cloning and sequence of two different cDNAs encoding 1-aminocyclopropane-1-carboxylate synthase in tomato. Proc Natl Acad Sci USA 87: 4859–4863 (1990).

    Google Scholar 

  52. Watson JC, Thompson WF: Purification and restriction endonuclease analysis of plant nuclear DNA. In: Weissbach A, Weissbach H (eds) Methods for Plant Molecular Biology, pp. 57–75. Academic Press, New York (1988).

    Google Scholar 

  53. Yang SF, Hoffman NE: Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35: 155–189 (1984).

    Google Scholar 

  54. Yip WK, Dong JG, Kenny JW, Thompson GA, Yang SF: Characterization and sequencing of active site of 1-aminocyclopropane-1-carboxylate synthase. Proc Natl Acad Sci USA 87: 7930–7934 (1990).

    Google Scholar 

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Authors and Affiliations

  1. Plant Molecular Biology Laboratory, USDA/ARS, Beltsville Agricultural Research Center (West), Building 006, 20705, Beltsville, MD, USA

    Ning Li, Barbara L. Parsons, Derong Liu & Autar K. Mattoo

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  1. Ning Li
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  2. Barbara L. Parsons
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  3. Derong Liu
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  4. Autar K. Mattoo
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Li, N., Parsons, B.L., Liu, D. et al. Accumulation of wound-inducible ACC synthase transcript in tomato fruit is inhibited by salicylic acid and polyamines. Plant Mol Biol 18, 477–487 (1992). https://doi.org/10.1007/BF00040664

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  • DOI: https://doi.org/10.1007/BF00040664

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