Abstract
Two genes encoding enzymes in the abscisic acid (ABA) biosynthesis pathway, zeaxanthin epoxidase (ZEP) and 9-cis-epoxycarotenoid dioxygenase (NCED), have previously been cloned by transposon tagging in Nicotiana plumbaginifolia and maize respectively. We demonstrate that antisense down-regulation of the tomato gene LeZEP1 causes accumulation of zeaxanthin in leaves, suggesting that this gene also encodes ZEP. LeNCED1 is known to encode NCED from characterization of a null mutation (notabilis) in tomato. We have used LeZEP1 and LeNCED1 as probes to study gene expression in leaves and roots of whole plants given drought treatments, during light/dark cycles, and during dehydration of detached leaves. During drought stress, NCED mRNA increased in both leaves and roots, whereas ZEP mRNA increased in roots but not leaves. When detached leaves were dehydrated, NCED mRNA responded rapidly to small reductions in water content. Using a detached leaf system with ABA-deficient mutants and ABA feeding, we investigated the possibility that NCED mRNA is regulated by the end product of the pathway, ABA, but found no evidence that this is the case. We also describe strong diurnal expression patterns for both ZEP and NCED, with the two genes displaying distinctly different patterns. ZEP mRNA oscillated with a phase very similar to light-harvesting complex II (LHCII) mRNA, and oscillations continued in a 48 h dark period. NCED mRNA oscillated with a different phase and remained low during a 48 h dark period. Implications for regulation of water stress-induced ABA biosynthesis are discussed.
Similar content being viewed by others
References
Addicott, F.T. and Carns, H.R. 1983. History and introduction. In: F.T. Addicott (Ed.), Abscisic Acid, Praeger, New York, pp. 1–21.
Audran, C., Borel, C., Frey, A., Sotta, B., Meyer, C., Simonneau, T. and Marion-Poll, A. 1998. Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol. 118: 1021–1028.
Beator, J. and Kloppstech, K. 1996. Significance of circadian gene expression in higher plants. Chronobiol. Int. 13: 319–339.
Bird, C.R., Smith, C.J.S., Ray, J.A., Moureau, P., Bevan, M.W., Bird, A.S., Hughes, S., Morris, P.C., Grierson, D. and Schuch, W. 1988. The tomato polygalacturonase gene and ripeningspecific expression in transgenic plants. Plant Mol. Biol. 11: 651–662.
Burbidge, A., Grieve, T.M., Woodman, K.J. and Taylor, I.B. 1995. Strategies for targeted transposon tagging of ABA biosynthetic mutants in tomato. Theor. Appl. Genet. 91: 1022–1231.
Burbidge, A., Grieve, T.M., Terry, C., Corlett, J.E., Thompson, A.J. and Taylor, I.B. 1997a. Structure and expression of a cDNA encoding zeaxanthin epoxidase, isolated from a wiltrelated tomato (Lycopersicon esculentum Mill.) library. J. Exp. Bot. 48: 1749–1750.
Burbidge, A., Grieve, T.M., Jackson, A.C., Thompson, A.J. and Taylor, I.B. 1997b. Structure and expression of a cDNA encoding a putative neoxanthin cleavage enzyme (NCE), isolated from a wilt-related tomato (Lycopersicon esculentum Mill.) library. J. Exp. Bot. 48: 2111–2112.
Burbidge, A., Grieve, T.M., Jackson, A.C., Thompson, A.J., McCarty, D.R. and Taylor, I.B. 1999. Characterisation of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J. 17: 427–431.
Cohen, A. and Bray, E.A. 1990. Characterisation of three mRNAs that accumulate in wilted tomato leaves in response to elevated levels of endogenous abscisic acid. Planta 182: 27–33.
Corlett, J.E., Wilkinson, S. and Thompson, A.J. 1998. Diurnal control of the drought-inducible putative histone H1 gene in tomato (Lycopersicon esculentum Mill. L.). J. Exp. Bot. 49: 945–952.
Creelman, R.A. and Zeevaart, J.A.D. 1984. Incorporation of oxygen into abscisic acid and phaseic acid from molecular oxygen. Plant Physiol. 75: 166–169.
Creelman, R.A. and Zeevaart, J.A.D. 1985. Abscisic acid accumulation in spinach leaf slices in the presence of penetrating and non-penetrating solutes. Plant Physiol. 77: 25–28.
Demmig-Adams, B. and Adams, W.W. 1992. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 599–626.
Duckham, S.C., Linforth, R.S.T. and Taylor, I.B. 1991. Abscisicacid-deficient mutants at the aba gene locus of Arabidopsis thaliana are impaired in the epoxidation of zeaxanthin. Plant Cell Environ. 14: 601–606.
Guerrero, F. and Mullet, J.E. 1986. Increased abscisic acid biosynthesis during plant dehydration requires transcription. Plant Physiol. 80: 588–590.
Guerineau, F. and Mullineaux, P. 1993. Plant transformation and expression vectors. In: R.R.D. Croy (Ed.), Plant Molecular Biology LABFAX, BIOS Scientific Publishers, Oxford, pp. 121–147.
Marin, E., Nussaume, L., Quesada, A., Gonneau, M., Sotta, B., Hugueney, P., Frey, A. and Marion-Poll, A. 1996. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J. 15: 2331–2342.
Martin, D.N., Proebsting, W.M., Parks, T.D., Dougherty, W.G., Lange, T., Lewis, M.J., Gaskin, P. and Hedden, P. 1996. Feedback regulation of gibberellin biosynthesis and gene expression in Pisum sativum L. Planta 200: 159–166.
Melton, D.A., Kreig, P.A., Rebagliat, M.R., Maniatis, T., Zinn, K. and Green, M.R. 1984. Efficient in vitro synthesis of biologically active RNA and RNA hybridisation probes from plasmids containing a bacteriophage promoter. Nucl. Acids Res. 12: 7035–7056.
Mulholland, B.J. 1994. Soil compaction and plant growth: the role of root-sourced chemical signals. PhD thesis, University of Nottingham, UK.
Neill, S.J., Burnett, E.C., Desikan, R. and Hancock, J.T. 1998. Cloning of a wilt-responsive cDNA from an Arabidopsis thaliana suspension culture cDNA library that encodes a putative 9-cis-epoxycarotenoid dioxygenase. J. Exp. Bot. 49: 1893–1894.
Oelmuller, R., Schneiderbauer, A., Herrmann, R.G. and Kloppstech, K. 1995. The steady-state mRNA levels for the thylakoid proteins exhibit a co-ordinated diurnal regulation. Mol. Gen. Genet. 246: 478–484.
Parry, A.D., Neill, S.J. and Horgan, R. 1988. Xanthoxin levels and metabolism in the wild-type and wilty mutants of tomato. Planta 173: 397–404.
Parry, A.D., Babiano, M.J. and Horgan, R. 1990. The role of ciscarotenoids in abscisic acid biosynthesis. Planta 182: 118–128.
Parry, A.D., Griffiths, A. and Horgan, R. 1992. Abscisic acid biosynthesis in roots. II. The effects of water stress in wildtype and abscisic acid-deficient mutant (notabilis) plants of Lycopersicon esculentum Mill. Planta 187: 192–197.
Pichersky, E., Bernatzky, R., Tanksley, S.D., Breidenbach, R.B., Kausch, A.P. and Cashmore, A.R. 1985. Molecular characterisation and genetic mapping of 2 clusters of genes encoding chlorophyll a/b binding proteins in Lycopersicon esculentum (tomato). Gene 40: 247–258.
Piechulla, B. and Gruissem, W. 1987. Diurnal mRNA fluctuations of nuclear and plastid genes in developing tomato fruits. EMBO J. 6: 3593–3599.
Pierce, M. and Raschke, K. 1980. Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta 148: 174–182.
Quarrie, S.A., Whitford, P.N., Appleford, N.E.J., Wang, T.L., Cook, S.K., Henson, I.E. and Loveys, B.R. 1988. A monoclonal antibody to (S)-abscisic acid: its characterisation and use in an radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173: 330–339.
Riesselmann, S. and Piechulla, B. 1992. Diurnal and circadian lightharvesting complex and quinone B-binding protein synthesis in leaves of tomato (Lycopersicon esculentum). Plant Physiol. 100: 1840–1845.
Rock, C.D. and Zeevaart, J.A.D. 1991. The abamutant of Arabidopsis thaliana is impaired in epoxycarotenoid biosynthesis. Proc. Natl. Acad. Sci. USA 88: 7496–7499.
Schwartz, S.H., Leon-Kloosterziel, K.M., Koornneef, M. and Zeevaart, J.A.D. 1997a. Biochemical characterisation of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiol. 114: 161–166.
Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A.D. and Mc-Carty, D.R. 1997b. Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276: 1872–1874.
Sindhu, R.K. and Walton, D.C. 1987. Xanthoxin metabolism in cellfree preparations from wild-type and wilty mutants of tomato. Plant Physiol. 88: 178–182.
Slovik, S. and Hartung, W. 1992. Compartmental distribution and redistribution of abscisic acid in intact leaves. II. Model analysis. Planta 187: 26–36.
Tan, B.C., Schwartz, S.H., Zeevaart, J.A.D. and McCarty, D.R. 1997. Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. USA 94: 12235–12240.
Taylor, H.I. and Burden, R.S. 1973. Preparation and metabolism of 2-[14C]-cis, trans-xanthoxin. J. Exp. Bot. 24: 873–880.
Taylor, I.B. 1991. Genetics of ABA synthesis. In: W.J. Davies and H.G. Jones (Eds.), Abscisic Acid Physiology and Biochemistry, Bios Scientific Publishers, Oxford, pp. 23–37.
Thompson, A.J. and Corlett, J.E. 1995. mRNA levels of four tomato (Lycopersicon esculentum Mill. L.) genes related to fluctuating plant and soil water status. Plant Cell Environ. 18: 773–780.
van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.-P., Pereira, A. and Stiekema, W.J. 1995. pBINPLUS: an improved plant transformation vector based on pBIN19. Transgen. Res. 4: 288–290.
Wilkinson, S. and Davies, W.J. 1997. Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol. 113: 559–573.
Zeevaart, J.A.D. and Creelman, R.A. 1988. Metabolism and physiology of abscisic acid. Annu. Rev. Plant Physiol. PlantMol. Biol. 39: 439–473.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Thompson, A.J., Jackson, A.C., Parker, R.A. et al. Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol 42, 833–845 (2000). https://doi.org/10.1023/A:1006448428401
Issue Date:
DOI: https://doi.org/10.1023/A:1006448428401