Abstract
Carotenoids, gibberellins (GAs), sterols, abscisic acid and β-amyrins were analysed in tomato (Lycopersicon esculentum Mill.) pericarp during fruit development and ripening. The contents of these isoprenoids in wild-type (cv. Ailsa Craig) fruit were compared with those in fruit of the carotenoid-deficient R-mutant and a transgenic plant containing antisense RNA to a phytoene synthase gene. In both carotenoid-deficient genotypes, a 14-fold reduction in carotene and twofold decrease in xanthophyll content, compared to the wild type, was found in ripe fruit. Immature green fruit from wild type and R-mutant plants contained similar amounts of the C19-GAs, GA1, and GA20, and their C20 precursor, GA19. Immature fruit from the transgenic plants contained three- to fivefold higher contents of these GAs. In wild-type fruit at the mature green stage the contents of these GAs had decreased to < 10% of the levels in immature fruit. A similar decrease in GA19 content occurred in the other genotypes. However, the contents of GA1 and GA20 in fruit from phytoene synthase antisense plants decreased only to 30% between the immature and mature green stages and did not decrease at all in R-mutant fruit. At the breaker and ripe stages, the contents of each GA were much reduced for all genotypes. The amount of abscisic acid was the same in immature fruit from all three genotypes, but, on ripening, the levels of this hormone in antisense and R-mutant fruit were ca. 50% of those in the wild type. Quantitative differences in the amounts of the triterpenoid β-amyrins, total sterols, as well as individual sterols, such as campesterol, stigmasterol and sitosterol, were apparent between all three genotypes during development. Amounts of free sterols of wild type and antisense fruit were greatest during development and decreased during ripening, whereas the opposite was found in the R-mutant. This genotype also possessed less free sterol and more bound sterol in comparison to the other varieties. These data provide experimental evidence to support the concept of an integrated metabolic relationship amongst the isoprenoids.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABA:
-
abscisic acid
- dpb:
-
days post breaker
- FDP:
-
farnesyl diphosphate
- GA:
-
gibberellin
- GGDP:
-
geranyl-geranyl diphosphate
References
Addicott, F.T. (1983) Abscisic Acid. Praeger, New York
Aspinall, D., Paleg, L.G., Addicott, F.T. (1967) Abscisin II and some hormone-related plant responses. Aus. J. Biol. Sci. 20, 869–882
Banthorpe, D.V. (1991) Classification of terpenoids and general procedures for their characterisation. In: Methods in plant biochemistry, vol. 7, pp. 1–41, Charlwood, B.V., Banthorpe, D.V., eds. Academic Press, London
Bartley, G.E., Scolnik, P.A. (1994) cDNA cloning, expression during development, genome mapping of PSY2, a second tomato gene encoding phytoene synthase. J Biol. Chem. 268, 25718–25721
Benveniste, P. (1986) Sterol biosynthesis. Annu. Rev. Plant Physiol. 37, 275–308
Bird, C.R., Ray, J.A., Fletcher, J.D., Boniwell, J.M., Bird, A.S., Teulieres, C., Blain, I., Bramley, P.M., Schuch, W. (1991) Using antisense RNA to study gene function: inhibition of carotenoid biosynthesis in transgenic tomatoes. Biotechnology 9, 635–639
Bligh, E.C., Dyer, W.J. (1959) A rapid method of lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917
Bohner, J., Hedden, P., Bora-Haber, E., Bangerth, F. (1988) Identification and quantitation of gibberellins in fruits of Lycopersicon esculentum, and their relationship to fruit size in L. esculentum and L. pimpinellifolium. Physiol. Plant. 73, 348–353
Bramley, P.M. (1993) Carotenoid biosynthesis. In: Methods in plant biochemistry, vol. 9, pp. 281–298, Lea, P., ed. Academic Press, London
Bramley, P.M., Teulieres, C., Blain, I., Bird, C., Schuch, W. (1992) Biochemical characterisation of transgenic tomato plants in which carotenoid synthesis has been inhibited through expression of antisense RNA to pTOM5. The Plant J. 2, 343–349
Burden, R.S., Clark, T., Holloway, P.J. (1987) Effects of sterol biosynthesis inhibiting fungicides and plant growth regulators on the sterol composition of barley plants. Pestic. Biochem. Physiol. 27, 289–300
Croker, S.J., Hedden, P., Lenton, J.R., Stoddart, J.L. (1990) Comparison of gibberellins in normal and slender barley seedlings. Plant Physiol. 94, 194–200
Crozier, A. (ed.) (1983) The Biochemistry and physiology of gibberellins, vol. 2, Praeger Publishers, New York
Davies, B.H. (1976) Carotenoids. In: Chemistry and biochemistry of plant pigments, vol. 2, pp. 38–185, Goodwin, T.W., ed., Academic Press, London
Dostal, H.C., Leopold, A.C. (1967) Gibberellin delays ripening of tomatoes. Science 158, 1579–1580
Epstein, W.W., Rilling, H.C. (1970) Studies on the mechanism of squalene biosynthesis. The structure of presqualene pyrophosphate. J. Biol. Chem. 245, 4597–4601
Fraser, P.D., Truesdale, M., Bird, C.R., Schuch, W., Bramley, P.M. (1994) Carotenoid biosynthesis during tomato fruit development. Evidence for tissue-specific gene expression. Plant Physiol. 105, 405–413
Fray, R., Grierson, D. (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol. Biol. 22, 589–602
Graebe, J.E. (1987) Gibberellin biosynthesis and control. Annu. Rev. Plant Physiol. 38, 419–465
Gray, J.C. (1987) Control of isoprenoid biosynthesis in higher plants. Adv. Bot. Res. 14, 25–91
Hedden, P. (1987) Gibberellins. In: The principles and practice of plant hormone analysis, vol. 1, pp. 9–110, Rivier, L., Crozier, A., eds. Academic Press, London
Hedden, P., Lewis, M.J. (1990) Quantitative analysis of abscisic acid by combined gas chromatography-mass spectrometry. In: Molecular aspects of hormonal regulation of plant development, pp. 55–62, Kutacek, M., Elliott, M.C., Machackova, I., eds., SPB Academic, The Hague
Parry, A.D., Blonstein, A.D., Babiano, M.J., King, P.J., Horgan, R. (1991) Abscisic acid metabolism in a wilty mutant of Nicotiana plumbaginifolia. Planta 183, 237–243
Ray, J., Moureau, P., Bird, C., Grierson, D., Maunders, M., Truesdale, M., Bramley, P.M., Schuch, W. (1992) Cloning and characterisation of a gene involved in phytoene synthesis from tomato. Plant Mol. Biol. 19, 401–404
Sandmann, G. (1991) Biosynthesis of cyclic carotenoids: Biochemistry and molecular genetics of the reaction sequence. Physiol. Plant. 83, 186–193
Whitaker, B.D. (1988) Changes in the steryl lipid content and composition of tomato fruit during ripening. Phytochemistry 27, 3411–3416
Zeevart, J.A.D., Creelman, R.A. (1988) Metabolism and physiology of abscisic acid. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 439–473
Author information
Authors and Affiliations
Additional information
We thank Mr. Paul Gaskin (Long Ashton Research Station) for the qualitative GC-MS of triterpenoids and Dr. R. Horgan (University of Wales, Aberystwyth) for a gift of [6-3H2]ABA. The work was supported by a research grant (No. PG111/617) to P.M.B. from the Agricultural and Food Research Council to whom we express our thanks.
Rights and permissions
About this article
Cite this article
Fraser, P.D., Hedden, P., Cooke, D.T. et al. The effect of reduced activity of phytoene synthase on isoprenoid levels in tomato pericarp during fruit development and ripening. Planta 196, 321–326 (1995). https://doi.org/10.1007/BF00201391
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00201391