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Plant Molecular Biology

, Volume 13, Issue 3, pp 303–311 | Cite as

Control and manipulation of gene expression during tomato fruit ripening

  • Wolfgang Schuch
  • Colin R. Bird
  • John Ray
  • Christopher J. S. Smith
  • Colin F. Watson
  • Peter C. Morris
  • Julie E. Gray
  • Christine Arnold
  • Graham B. Seymour
  • Gregory A. Tucker
  • Donald Grierson
Article

Abstract

Ripening is a complex developmental process involving changes in the biochemistry, physiology and gene expression of the fruit. It is an active process characterised by changes in all cellular compartments. cDNA cloning has been used as an approach to analyse changes in gene expression during fruit ripening. This has revealed that several genes are switched on specifically during fruit ripening, including one encoding polygalacturonase (PG), a major cell wall protein. These cDNA clones have been used to study the expression of the genes in normal and ripening mutant fruits, and under environmental stress conditions.

The PG gene has been isolated and it has been demonstrated that 1450 bases 5′ of the coding region are sufficient for the tissue- and development-specific expression of a bacterial marker gene in transgenic tomatoes. Antisense RNA techniques have been developed to generate novel mutant tomatoes in which the biochemical function of this enzyme and its involvement in fruit softening has been tested.

Key words

fruit ripening tomatoes polygalacturonase antisense 

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References

  1. 1.
    Acaster MA, Kende H: Properties and partial purification of 1-aminocyclopropane-1-carboxylate synthase. Plant Physiol 72: 139–145 (1983).Google Scholar
  2. 2.
    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
  3. 3.
    Biggs MS, Harriman RW, Handa AK: Changes in gene expression during tomato fruit ripening. Plant Physiol 81: 395–403 (1986).Google Scholar
  4. 4.
    Biggs MS, Handa AK: Temporal regulation of polygalacturonase expression in fruits from normal mutant and heterozygous tomato genotypes. Plant Physiol 89: 117–125 (1989).Google Scholar
  5. 5.
    Bird CR, Smith CJS, Ray JA, Moureau P, Bevan MW, Bird AS, Hughes S, Morris PC, Grierson D, Schuch W: The tomato polygalacturonase gene and ripening-specific expression in transgenic tomato plants. Plant Mol Biol 11: 651–662 (1988).Google Scholar
  6. 6.
    Bleecker AB, Kenyon WH, Somerville SC, Kende H: Use of monoclonal antibodies in the purification and characterisation of 1-aminocyclopropane-1-carboxylate synthase, an enzyme in ethylene synthesis. Proc Natl Acad Sci USA 83: 7755–7759 (1986).Google Scholar
  7. 7.
    Bleecker AB, Robinson G, Kende H: Studies on the regulation of 1-aminocyclopropane-1-carboxylate synthase in tomato using monoclonal antibodies. Planta 173: 385–390 (1988).CrossRefGoogle Scholar
  8. 8.
    Brady C, MacAlpine G, McGlasson WB, Ueda Y: Polygalacturonase in tomato fruit and the induction of ripening. Aust J Plant Physiol 9: 171–178 (1982).Google Scholar
  9. 9.
    Crookes PR, Grierson D: Ultrastructure of tomato fruit ripening and the role of polygalacturonase isoenzymes in cell wall degradation. Plant Physiol 72: 1088–1093 (1983).Google Scholar
  10. 10.
    Davies KM, Hobson GE, Grierson D: Silver ions inhibit the ethylene stimulated production of ripening-related mRNAs in tomato. Plant Cell Envir 11: 729–738 (1988).Google Scholar
  11. 11.
    DellaPenna D, Alexander DC, Bennett AB: Molecular cloning of tomato fruit polygalacturonase: Analysis of polygalacturonase mRNA levels during ripening. Proc Natl Acad Sci USA 83: 6420–6424 (1986).Google Scholar
  12. 12.
    DellaPenna D, Kates DS, Bennett AB: Polygalacturonase gene expression in Rutgers, rin, nor, and Nr tomato fruits. Plant Physiol 85: 502–507 (1987).Google Scholar
  13. 13.
    DellaPenna D, Bennett AB: In vitro synthesis and processing of tomato fruit polygalacturonase. Plant Physiol 86: 1057–1063 (1988).Google Scholar
  14. 14.
    Diekman J, Fischer RL: Interaction 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
  15. 15.
    Giovannoni JJ, DellaPenna D, Bennett AB, Fischer RL: Expression of a chimeric polygalacturonase gene in transgenic rin tomato fruits results in polyuronide degradation but not fruit softening. Plant Cell 1: 53–63 (1989).CrossRefPubMedGoogle Scholar
  16. 16.
    Grierson D, Tucker GA: Timing of ethylene and polygalacturonase synthesis in relation to the control of tomato ripening. Planta 157: 174–179 (1983).Google Scholar
  17. 17.
    Grierson D, Slater A, Spiers J, Tucker GA: The appearance of polygalacturonase mRNA in tomatoes: one of a series of changes in gene espression during development and ripening. Planta 163: 263–271 (1985).Google Scholar
  18. 18.
    Grierson D, Slater A, Maunders M, Crookes P, Tucker G, Schuch W, Edwards K: Regulation of the expression of tomato fruit ripening genes: the involvement of ethylene. In: Roberts JA, Tucker GA (eds) Ethylene and Plant Development, pp. 147–161. Butterworths, London (1985).Google Scholar
  19. 19.
    Grierson D, Maunders MJ, Slater A, Ray J, Bird CR, Schuch W, Holdsworth MJ, Tucker GA, Knapp JE: Gene expression during tomato ripening. Phil Trans R Soc Lond B 314: 399–410 (1986).Google Scholar
  20. 20.
    Grierson D, Tucker GA, Keen J, Ray J, Bird CR, Schuch W: Sequencing and identification of a cDNA clone for tomato polygalacturonase. Nucleic Acids Res 14: 8595–8603 (1986).PubMedGoogle Scholar
  21. 21.
    Grierson D, Purton ME, Knapp JE, Bathgate B: Tomato ripening mutants. In: Thomas H, Grierson D (eds), Development of Mutants in Higher Plants, pp. 73–94 Cambridge University Press, Cambridge (1987).Google Scholar
  22. 22.
    Gross CK, Wallner SJ: Degradation of cell wall polysaccharides in ripening tomato fruit. Plant Physiol 63: 117–120 (1979).Google Scholar
  23. 23.
    Gross CK, Sams CE: Changes in neutral sugar composition during fruit ripening: a species survey. Phytochemistry 23: 2457–2461 (1984).CrossRefGoogle Scholar
  24. 24.
    Hobson GE: Polygalacturonase in normal and abnormal tomato fruit. Biochem J 92: 324–332 (1964).PubMedGoogle Scholar
  25. 25.
    Hobson GE, Nichols R, Davies JN, Atkey PT: The inhibition of tomato fruit ripening by silver. J Plant Physiol 116: 21–29 (1984).Google Scholar
  26. 26.
    Hobson GE: The firmness of tomato fruit in relation to polygalacturonase activity. J Hort Sci 40: 66–72 (1965).Google Scholar
  27. 27.
    Hobson GE: Cellulase activity during the maturation and ripening of tomato fruit. J Food Sci 33: 588–592 (1968).Google Scholar
  28. 28.
    Hoffman NE, Yang SF: Changes of 1-aminocyclopropane-1 carboxylic acid content in ripening fruits in relation to their ethylene production rates. J Am Soc Hort Sci 105: 492–495 (1980).Google Scholar
  29. 29.
    Holdsworth MJ, Bird CR, Ray J, Schuch W, Grierson D: Structure and expression of an ethylene related mRNA from tomato. Nucleic Acids Res 15: 731–739 (1987).PubMedGoogle Scholar
  30. 30.
    Holdsworth MJ, Schuch W, Grierson D: Organisation and expression of a wound/ripening related small multigene family from tomato. Plant Mol Biol 11: 81–88 (1988).Google Scholar
  31. 31.
    Huber DJ: The role of cell wall hydrolases in fruit softening. Hort Rev 5: 169–219 (1983).Google Scholar
  32. 32.
    Huber DJ: Polyuronide degradation and hemicellulose modifications in riping tomato fruit. J Am Soc Hort Sci 108: 405–409 (1983).Google Scholar
  33. 33.
    Knapp JE, Moureau P, Schuch W, Grierson D: Organisation and expression of polygalacturonase and other ripening-related genes in Ailsa Craig ‘Neverripe’ and ‘Ripening inhibitor’ tomato mutants. Plant Mol Biol 12: 105–116 (1989).CrossRefGoogle Scholar
  34. 34.
    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
  35. 35.
    Lincoln JE, Fisher RL: Regulation of gene expression by ethylene in wild-type and rin tomato (Lycopersicon esculentum) fruit. Plant Physiol 88: 370–374 (1988).Google Scholar
  36. 36.
    Mansson PE, Hsu D, Stalker D: Characterisation of fruit specific cDNAs from tomato. Mol Gen Genet 200: 356–361 (1985).Google Scholar
  37. 37.
    Maunders MJ, Holdsworth MJ, Slater A, Knapp JE, Bird CR, Schuch W, Grierson D: Ethylene stimulates the accomodation of ripening-related mRNAs in tomatoes. Plant Cell Envir 10: 177–184 (1987).Google Scholar
  38. 38.
    Mitcham EJ, Gross CK, Ng TJ: Tomato fruit cell wall synthesis during development and senescence. Plant Physiol 89: 477–481 (1989).Google Scholar
  39. 39.
    Mutschler M, Guttieri M, Kinzer S, Grierson D, Tucker GA: Changes in ripening related processes in tomatoes conditioned by the alc mutant. Theor Appl Genet 76: 285–292 (1989).Google Scholar
  40. 40.
    Picton S, Grierson D: Inhibition of expression of tomato ripening genes at high temperature. Plant Cell Envir 11: 265–272 (1988).Google Scholar
  41. 41.
    Pressey R, Avants JK: Two forms of polygalacturonase in tomatoes. Biochim Biophys Acta 309: 363–369 (1979).Google Scholar
  42. 42.
    Rattanapanone N, Speirs J, Grierson D: Evidence for changes in messenger RNA content related to tomato fruit ripening. Phytochemistry 17: 1485–1486 (1978).CrossRefGoogle Scholar
  43. 43.
    Ray J, Bird C, Maunders M, Grierson D, Schuch W: Sequence of pTOM5, a ripening related cDNA from tomato. Nucleic Acids Res 15: 10587 (1987).PubMedGoogle Scholar
  44. 44.
    Ray J, Knapp JE, Grierson D, Bird C, Schuch W: Identification and sequence determination of a cDNA clone for tomato pectin esterase. Eur J Biochem 174: 119–124 (1988).PubMedGoogle Scholar
  45. 45.
    Sato T, Kusaba S, Nakagawa H, Ogura N: Cell free synthesis of a putative precursor of polygalacturonase in tomato fruits. Plant Cell Physiol 25: 1069–1071 (1984).Google Scholar
  46. 46.
    Sato T, Kusaba S, Nakagawa H, Ogura N: Polygalacturonase mRNA of tomato: Size and content in ripe fruits. Plant Cell Physiol 26: 211–214 (1985).Google Scholar
  47. 47.
    Seymour GB, Harding SE, Taylor AJ, Hobson GE, Tucker GA: Polyuronide solubilisation during ripening of normal and mutant tomato fruit. Phytochemistry 26 1871–1875 (1987).CrossRefGoogle Scholar
  48. 48.
    Sheehy RE, Kramer MK, Hiatt WR: Reduction of polygalacturonase activity in tomato fruit by antisense RNA. Proc Natl Acad Sci USA 85: 8805–8809 (1988).Google Scholar
  49. 49.
    Sheehy RE, Pearson J, Brady CJ, Hiatt WR: Molecular characterisation of tomato fruit polygalacturonase. Mol Gen Genet 208: 30–36 (1987).CrossRefGoogle Scholar
  50. 50.
    Slater A, Maunders MJ, Edwards K, Schuch W, Grierson D. Isolation and characterisation of cDNA clones for tomato polygalacturonase and other ripening related proteins. Plant Mol Biol 5: 137–147 (1985).Google Scholar
  51. 51.
    Smith CJS, Watson CF, Ray J, Bird CR, Morris PC, Schuch W, Grierson D: Antisense RNA inhibition of polygalacturonase gene expression in transgenic tomatoes. Nature 334: 724–726 (1988).CrossRefGoogle Scholar
  52. 52.
    Smith CJS, Watson CF, Morris PC, Bird CR, Seymour GB, Gray JE, Arnold C, Tucker GA, Schuch W, Grierson D: Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes. Plant Mol Biol, submitted.Google Scholar
  53. 53.
    Themmem APN, Tucker GA, Grierson D: Degradation of isolated tomato cell walls by purified polygalacturonase in vitro. Plant Physiol 69: 122–124 (1982).Google Scholar
  54. 54.
    Tieman DM, Handa AK: Immunocytolocalisation of polygalacturonase in ripening tomato fruit. Plant Physiol 90: 17–20 (1989).Google Scholar
  55. 55.
    Tigchelaar EC, McGlasson WB, Buesher RW: Genetic regulation of tomato fruit ripening. Hort Sci 13: 508–513 (1978).Google Scholar
  56. 56.
    Tucker GA, Grierson D: Synthesis of polygalacturonase during tomato fruit ripening. Planta 155: 64–67 (1982).CrossRefGoogle Scholar
  57. 57.
    Tucker GA, Robertson NG, Grierson D: Changes in polygalacturonase isoenzymes during the ‘ripening’ of normal and mutant tomato fruit. Eur J Biochem 112: 119–124 (1980).PubMedGoogle Scholar
  58. 58.
    Tucker GA, Robertson NG, Grierson D: The conversion of tomato-fruit polygacturonase isoenzyme 2 into soenzyme 1 in in vitro. Eur J Biochem 115: 87–90 (1981).PubMedGoogle Scholar
  59. 59.
    Wallner SJ, Walker JE: Glycosidases in cell wall degrading extracts of ripening tomato fruits. Plant Physiol 55: 94–98 (1975).Google Scholar
  60. 60.
    Yang SF, Hoffman NE: Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol 35: 155–189 (1984).Google Scholar
  61. 61.
    Zainon MA, Brady CJ: Purification and characterization of polygalacturonases of tomato fruits. Aust J Plant Physiol 9: 155–169 (1982).Google Scholar

Copyright information

© Kluwer Academic Publishers 1989

Authors and Affiliations

  • Wolfgang Schuch
    • 1
  • Colin R. Bird
    • 1
  • John Ray
    • 1
  • Christopher J. S. Smith
    • 2
  • Colin F. Watson
    • 2
  • Peter C. Morris
    • 2
  • Julie E. Gray
    • 2
  • Christine Arnold
    • 2
  • Graham B. Seymour
    • 2
  • Gregory A. Tucker
    • 3
  • Donald Grierson
    • 2
  1. 1.ICI Seeds Plant Biotechnology SectionJealott's Hill Research StationBracknell, BerkshireUK
  2. 2.Department of Physiology and Environmental ScienceUniversity of Nottingham, Faculty of agricultural ScienceLoughboroughUK
  3. 3.Department of Applied Biochemistry and Food ScienceUniversity of Nottingham, Faculty of Agricultural ScienceLoughboroughUK

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