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Role of desiccation in the termination of expression of genes for storage proteins

Published online by Cambridge University Press:  19 September 2008

L. Jiang
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, BC, CanadaV5A 1S6
A. R. Kermode*
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, BC, CanadaV5A 1S6
*
* Correspondence

Abstract

The final stage of development of orthodox seeds is maturation drying, a process often accompanied by a dramatic decline in storage-protein synthesis. When desiccation is imposed prematurely at certain stages prior to the completion of development, a switch in synthetic events is elicited. events unique to development, such as synthesis of storage protein, are terminated, while syntheses associated with germination and growth are initiated. We investigated whether desiccation plays a key role in effecting a decline in expression of genes for storage proteins by acting directly upon the regulatory regions of these developmental genes. The desiccation responsiveness of the 5′ and 3′ regulatory regions of the gene for the pea storage protein vicilin was tested in transgenic tobacco seed. Chimaeric genes were introduced into tobacco, these genes consisted of the coding region of the reporter gene for β-glucuronidase (GUS) and 5′ and 3′ regions from the vicilin gene, or, as controls, the same regions derived from constitutively expressed genes, presumed to be desiccation-insensitive – those from the cauliflower mosaic virus (35S) and nopaline synthase genes. In transgenic seed expressing the gene constructs containing the vicilin 5′ upstream region, GUS activities declined dramatically after imbibition in mature seed and after rehydration of prematurely dried tobacco seed. In contrast, GUS activities increased after seed rehydration when the constitutive viral (35S) promoter replaced the vicilin 5′ upstream region. The 3′ downstream region of the gene construct did not significantly affect the patterns of changes in GUS activities after seed rehydration. In studies of transient gene expression in castor bean cotyledons, premature desiccation led to termination of GUS gene expression only when the gene construct contained the vicilin 5′ upstream region. This region may respond directly to desiccation; alternatively, changes to trans-acting factors important for expression of genes for storage-proteins may occur as a result of drying.

Type
Short Communication
Copyright
Copyright © Cambridge University Press 1994

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References

Ackerson, R.C. (1984) Abscisic acid and precocious germination in soybeans. Journal of Experimental Botany 35, 414421.Google Scholar
Adams, C.A. and Rinne, R.W. (1981) Seed maturation in soybeans (Glycine max L. Merr.) is independent of seed mass and of the parent plant, yet is necessary for production of viable seeds. Journal of Experimental Botany 32, 615620.Google Scholar
Adams, C.A., Fjerstad, M.C. and Rinne, R.W. (1983) Characteristics of soybean seed maturation: necessity for slow dehydration. Crop Science 23, 265267.CrossRefGoogle Scholar
Allen, R.D., Trelease, R.N. and Thomas, T.L. (1988) Regulation of isocitrate lyase gene expression in sunflower. Plant Physiology 86, 527532.Google Scholar
Armstrong, C., Black, M., Chapman, J.M., Norman, H.A., and Angold, K. (1982) The induction of sensitivity to gibberellin in aleurone tissue of developing wheat grains. I. The effect of dehydration. Planta 154, 573577.Google Scholar
Berge, S.K., Bartholomew, D.W. and Quatrano, R. S. (1989) Control of the expression of wheat embryo genes by abscisic acid. pp 193201 in Goldberg, R.L. (Ed.) Molecular basis of plant development. New York, Alan R. Liss.Google Scholar
Bewley, J.D. (1988) Challenges in seed physiology. pp 5170 in Burris, J.S. (Ed.) Challenges for the second decade. Proceeding of the Tenth Annual Seed Technology Conference. Ames, IA, Iowa State University Press.Google Scholar
Bewley, J.D. and Black, M. (1985) Seeds. Physiology of development and germination. New York, Plenum Press.Google Scholar
Bewley, J.D. and Marcus, A. (1990) Gene expression in seed development and germination. pp 165193 in Cohn, W.E. and Moldave, K. (Eds) Progress in nucleic acid research and molecular biology. Vol. 38. Orlando, FL, Academic Press.Google Scholar
Bewley, J.D. and Oliver, M.J. (1992) Desiccation tolerance in vegetative plant tissues and seeds: protein synthesis in relation to desiccation and a potential role for protection and repair mechanisms. pp 141160 in Somero, G.N., Osmond, C.B. and Bolis, C.L. (Eds) Water and life: comparative analysis of water relationships at the organismic, cellular and molecular levels. Berlin, Springer-Verlag.Google Scholar
Bewley, J.D., Kermode, A.R. and Misra, S. (1989) Desiccation and minimal drying (‘undrying’) treatments of seeds of castor bean and Phaseolus vulgaris which terminate development and promote germination cause changes in protein and messenger RNA synthesis. Annals of Botany 63, 317.CrossRefGoogle Scholar
Black, M. (1983) Abscisic acid in seed germination and dormancy. pp 334363. in Addicott, F.T. (Ed.) Abscisic acid. New York, Praeger Publisher.Google Scholar
Black, M. (1991) Involvement of ABA in the physiology of developing and mature seeds. pp 99124 in Davies, W.J. and Jones, H.G. (Eds) Abscisic acid physiology and biochemistry. Oxford, BIOS Scientific Publishers Ltd.Google Scholar
Boulter, D., Evans, I.M., Ellis, J.R., Shirsat, A.H., Gatehouse, J.A. and Croy, R.R.D. (1987) Differential gene expression in the development of Pisum sativum. Plant Physiology and Biochemistry 25, 283289.Google Scholar
Brown, J.W.S., Wandelt, C., Feix, G., Neuhaus, G. and Schweiger, H.G. (1986) The upstream regions of zein genes: sequence analysis and expression in the unicellular alga Acetabularia. European Journal of Cell Biology 42, 161170.Google Scholar
Chandler, P.M., Spencer, D., Randall, P.J. and Higgins, T.J.V. (1984) Influence of sulfur nutrition on developmental patterns of some major seed proteins and their mRNAs. Plant Physiology 75, 651657.Google Scholar
Chen, Z-L., Schuler, M.A. and Beachy, R.N. (1986) Functional analysis of regulatory elements in a plant embryo-specific gene. Proceedings of the National Academy of Sciences, USA 83, 85608564.Google Scholar
Choinski, J.S., Trelease, R.N. and Doman, D.C. (1981) Control of enzyme activities in cotton cotyledons during maturation and germination. III. In vitro embryo development in the presence of abscisic acid. Planta 152, 428435.CrossRefGoogle ScholarPubMed
Comai, L. and Harada, J.J. (1990) Transcriptional activities in dry nuclei indicate the timing of the transition from embryogeny to germination. Proceedings of the National Academy of Sciences, USA 87, 26712674.CrossRefGoogle ScholarPubMed
Comai, L., Matsudaira, K.L., Heupel, R.C., Dietrich, R.A. and Harada, J.J. (1992) Expression of a Brassica napus malate synthase gene in transgenic tomato plants during the transition from late embryogeny to germination. Plant Physiology 98, 5361.Google Scholar
Cornford, C.A., Black, M., Chapman, J.M. and Baulcombe, D.C. (1986) Expression of α-amylase and other gibberellin-regulated genes in aleurone tissue of developing wheat grains. Planta 169, 420428.CrossRefGoogle ScholarPubMed
Cornford, C.A., Black, M. and Chapman, J.M. (1987a) Sensitivity of developing wheat grains to gibberellin and production of alpha-amylase during grain development and maturation. pp 283292 in Mares, D.J. (Ed.) Fourth international symposium on pre-har-vest sprouting in cereals. Boulder, CO, Westview Press.Google Scholar
Cornford, C.A., Black, M., Daussant, J. and Murdoch, K.M. (1987b) α-Amylase production by premature wheat (Triticum aestivum L.) Journal of Experimental Botany 38, 277285.CrossRefGoogle Scholar
Croissant-Sych, Y. and Bopp, M. (1988) Formation and degradation of storage proteins in the embryo of Sinapis alba. Journal of Plant Physiology 132, 520528.CrossRefGoogle Scholar
Crouch, M.L., Tenbarge, K., Simon, A., Finkelstein, R., Scofield, S. and Solberg, L. (1985) Storage protein mRNA levels can be regulated by abscisic acid in Brassica embryos. pp 555566 in van Vloten-Doting, L., Groot, G.S.P. and Hall, T.C. (Eds) Molecular form and function of the plant genome. New York, Plenum Press.Google Scholar
Dasgupta, J. and Bewley, J.D. (1982) Desiccation of axes of Phaseolus vulgaris during development causes a switch from a developmental pattern of protein synthesis to a germination pattern. Plant Physiology 70, 12241227.Google Scholar
Dasgupta, J., Bewley, J.D. and Yeung, E.C. (1982) Desiccation-tolerant and desiccation-intolerant stages during development and germination of Phaseolus vulgaris seeds. Journal of Experimental Botany 33, 10451057.CrossRefGoogle Scholar
Datta, K, Parker, H., Averyhart-Fullard, V., Schmidt, A. and Marcus, A. (1987) Gene expression in the soybean seed axis during germination and early seedling growth. Planta 170, 209216.CrossRefGoogle ScholarPubMed
DeLisle, A.J. and Crouch, M.L. (1989) Seed storage protein transcription and mRNA levels in Brassica napus during development and in response to exogenous abscisic acid. Plant Physiology 91, 617623.Google Scholar
Duchartre, M.P. (1952) Note sur la germination des céréales recoltées avant leur maturité. Comptes rendus hebdomadaires des Séances de l'Académie des Sciences, Paris 35, 940942.Google Scholar
Dure, L.S., III (1985) Embryogenesis and gene expression during seed formation. Oxford Surveys of Plant Molecular and Cell Biology 2, 179188.Google Scholar
Dure, L.S., III, Crouch, M., Harada, J., Ho, T.H.D., Mundy, J., Quatrano, R., Thomas, T. and Sung, Z.R. (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Molecular Biology 12, 475486.Google Scholar
Eisenberg, A.J. and Mascarenhas, J.P. (1985) Abscisic acid and the regulation of the synthesis of specific seed proteins and their messenger RNAs during culture of soybean embryos. Planta 166, 505514.CrossRefGoogle ScholarPubMed
Evans, M., Black, M. and Chapman, J.M. (1975) Induction of hormone sensitivity by dehydration is the one positive role for drying in cereal seed. Nature 258, 144145.Google Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1988) Recalcitrance – a current assessment. Seed Science and Technology 16, 155166.Google Scholar
Finkelstein, R.R., Tenbarge, K.M., Shumway, J.E. and Crouch, M.L. (1985) Role of ABA in maturation of rapeseed embryos. Plant Physiology 78, 630636.Google Scholar
Fischer, W., Bergfeld, R. and Schopfer, P. (1987) Induction of storage protein synthesis in embryos of mature plant seeds. Naturwissenschaften 74, 8688.CrossRefGoogle Scholar
Frevert, J., Koller, W. and Kindl, H. (1980) Occurrence and biosynthesis of glyoxysomal enzymes in ripening cucumber seeds. Hoppe-Seyler's Zeitschrift für Physiologische Chemie 361, 15571565.Google Scholar
Galau, G.A., Bijaisoradat, N. and Hughes, D.W. (1987) Accumulation kinetics of cotton late embryogenesis-abundant mRNAs: coordinate regulation during embryogenesis and the role of abscisic acid. Developmental Biology 123, 198212.Google Scholar
Galau, G.A. and Dure, L.S., III (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing mRNA populations as shown by reciprocal heterologous cDNA-mRNA hybridization. Biochemistry 20, 41694178.CrossRefGoogle Scholar
Galau, G.A., Jakobsen, K.S. and Hughes, W.D. (1991) The control of late dicot embryogenesis and early germination. Physiologia Plantarum 81, 280288.CrossRefGoogle Scholar
Garcia-Maya, M., Chapman, J.M. and Black, M. (1990) Regulation of α-amylase formation and gene expression in the developing wheat embryo. Role of abscisic acid, the osmotic environment and gibberellin. Planta 181, 296303.CrossRefGoogle ScholarPubMed
Goldberg, R.B. (1986) Regulation of plant gene expression. Philosophical Transactions of the Royal Society of London, B 314, 343353.Google Scholar
Goldberg, R.B., Barker, S.J. and Perez-Grau, L. (1989) Regulation of gene expression during plant embryogenesis. Cell 56, 149160.Google Scholar
Goldberg, R.B., Hoschek, G., Ditta, G.S. and Breidenbach, R.W. (1981a) Developmental regulation of cloned super abundant embryo mRNAs in soybean. Developmental Biology 83, 218231.CrossRefGoogle Scholar
Goldberg, R.B., Hoschek, G., Tam, S.H., Ditta, G.S. and Breidenbach, R.W. (1981b) Abundance, diversity and regulation of mRNA sequence sets in soybean embryogenesis. Developmental Biology 83, 201217.Google Scholar
Harada, J.J., Baden, C.S. and Comai, L. (1988) Spatially regulated genes expressed during seed germination and postgerminative development are activated during embryogeny. Molecular and General Genetics 212, 466473.Google Scholar
Harlan, H.V. and Pope, M.N. (1922) The germination of barley seeds harvested at different stages of growth. Journal of Heredity 13, 7275.CrossRefGoogle Scholar
Higgins, T.J.V. (1984) Synthesis and regulation of major proteins in seeds. Annual Review of Plant Physiology 35, 191221.Google Scholar
Higgins, T.J.V., Newbigin, E.J., Spencer, D., Llewellyn, D.J. and Craig, S. (1988) The sequence of a pea vicilin gene and its expression in transgenic tobacco plants. Plant Molecular Biology 11, 683695.Google Scholar
Hughes, D.W., Wyatt, R.E. and Galau, G.A. (1988) Modular accumulation of transcripts in maturing cotton embryos. Journal of Cellular Biochemistry (Supplement 12C), p. 181.Google Scholar
Jefferson, R.A. (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Molecular Biology Reporter 5, 387405.CrossRefGoogle Scholar
Kermode, A.R. (1990) Regulatory mechanisms involved in the transition from seed development to germination. Critical Reviews in Plant Sciences 9, 155195.CrossRefGoogle Scholar
Kermode, A.R. (1994) Regulatory mechanisms in the transition from seed development to germination: interactions between the embryo and the seed environment. pp 273332 in Galili, G. and Kigel, J. (Eds) Seed development and germination. New York, Marcel Dekker, Inc.Google Scholar
Kermode, A.R. and Bewley, J.D. (1985a) The role of maturation drying in the transition from seed development to germination. I. Acquisition of desiccation-tolerance and germinability during development of Ricinus communis L. seeds. Journal of Experimental Botany 36, 19061915.Google Scholar
Kermode, A.R. and Bewley, J.D. (1985b) The role of maturation drying in the transition from seed development to germination. II. Post-germinative enzyme production and soluble protein synthetic pattern changes within the endosperm of Ricinus communis L. seeds. Journal of Experimental Botany 36, 19161927.CrossRefGoogle Scholar
Kermode, A.R. and Bewley, J.D. (1986a) Alteration of genetically regulated syntheses in developing seeds by desiccation. pp 5984 in Leopold, A.C. (Ed.) Membranes, metabolism and dry organisms. Ithaca, NY, Cornell University Press.Google Scholar
Kermode, A.R. and Bewley, J.D. (1986b) The role of maturation drying in the transition from seed development to germination. IV. Protein synthesis and enzyme activity changes within the cotyledons of Ricinus communis L. seeds. Journal of Experimental Botany 37, 18871898.CrossRefGoogle Scholar
Kermode, A.R. and Bewley, J.D. (1987) Regulatory processes involved in the switch from seed development to germination: possible roles for desiccation and ABA. pp 5976 in Monti, L. and Porceddu, E. (Eds) Drought resistance in plants. Physiological and genetic aspects. Brussels, Commission of the European Communities.Google Scholar
Kermode, A.R. and Bewley, J.D. (1989) Developing seeds of Ricinus communis L., when detached and maintained in an atmosphere of high relative humidity, switch to a germinative mode without the requirement for complete desiccation. Plant Physiology 90, 702707.Google Scholar
Kermode, A.R., Gifford, D.J. and Bewley, J.D. (1985) The role of maturation drying in the transition from seed development to germination. III. Insoluble protein synthetic pattern changes within the endosperm of Ricinus communis L. seeds. Journal of Experimental Botany 36, 19281936.CrossRefGoogle Scholar
Kermode, A.R., Bewley, J.D., Dasgupta, J. and Misra, S. (1986) The transition from seed development to germination: a key role for desiccation? Horticultural Science 21 (special supplement), 11131118.Google Scholar
Kermode, A.R., Dumbroff, E.B. and Bewley, J.D. (1989a) The role of maturation drying in the transition from seed development to germination. VII. Effects of partial and complete desiccation on abscisic acid levels and sensitivity in Ricinus communis L. seeds. Journal of Experimental Botany 40, 303313.Google Scholar
Kermode, A.R., Oishi, M.Y. and Bewley, J.D. (1989b) Regulatory roles for desiccation and abscisic acid in seed development: a comparison of the evidence from whole seeds and isolated embryos. pp 2350 in Stanwood, P.C. and McDonald, M.B. (Eds) Seed moisture. (special publication No. 14), Madison, WI, Crop Science Society of America.Google Scholar
Kermode, A.R., Pramanik, S.K. and Bewley, J.D. (1989c) The role of maturation drying in the transition from seed development to germination. VI. Desiccation-induced changes in messenger RNA populations within the endosperm of Ricinus communis L. seeds. Journal of Experimental Botany 40, 3341.Google Scholar
King, R.W. (1976) Abscisic acid in developing wheat grains and its relationship to grain growth and maturation. Planta 132. 4351.Google Scholar
King, R.W. (1979) Abscisic acid synthesis and metabolism in wheat ears. Australian Journal of Plant Physiology 6, 99108.Google Scholar
King, R.W. (1982) Abscisic acid and seed development. pp 157181 in Khan, A.A. (Ed.) The physiology and biochemistry of seed development, dormancy and germination. Amsterdam, Elsevier Biomedical Press.Google Scholar
King, R.W., Salminen, S.O., Hill, R.D. and Higgins, T.J.V. (1979) Abscisic-acid and gibberellin action in developing kernels of triticale (cv. 6A190). Planta 146, 249255.Google Scholar
Krishna, T.G. and Murray, D.R. (1988) Effects of cycloheximide and actinomycin D on glycosidase activities in the cotyledons of legume seeds following imbibition. Journal of Plant Physiology 132, 745749.Google Scholar
Kriz, A.R., Wallace, M.S. and Paiva, R. (1990) Globulin gene expression in embryos of maize viviparous mutants. Evidence of regulation of the Glb 1 gene by ABA. Plant Physiology 92, 538542.CrossRefGoogle Scholar
Lalonde, L. and Bewley, J.D. (1986) Patterns of protein synthesis during the germination of pea axes, and the effects of an interrupting desiccation period. Planta 167, 504510.Google Scholar
Lane, B. (1991) Cellular desiccation and hydration: developmentally regulated proteins, and the maturation and germination of seed embryos. Biogenesis 5, 28932901.Google Scholar
Long, S.R., Dale, R.M.K. and Sussex, I.M. (1981) Maturation and germination of Phaseolus vulgaris embryonic axes in culture. Planta 153, 405415.Google Scholar
Marcus, A. and Rodaway, S. (1982) Nucleic acid and protein synthesis during germination. pp 337361 in Smith, H. (Ed.) The molecular biology of plant development. Berkeley, CA, University of California Press.Google Scholar
McDaniel, S., Smith, J.D. and Price, H.J. (1977) Response of viviparous mutants to abscisic acid. Maize Genetics Newsletter 51, 8586.Google Scholar
McWha, J.A. (1975) Changes in abscisic acid levels in developing grains of wheat (Triticum aestivum L.). Journal of Experimental Botany 26, 823827.Google Scholar
Misra, S. and Bewley, J.D. (1985) Reprogramming of protein synthesis from a developmental to a germinative mode induced by desiccation of the axes of Phaseolus vulgaris. Plant Physiology 78, 876882.CrossRefGoogle ScholarPubMed
Mitchell, B.A., Armstrong, C., Black, M. and Chapman, J.M. (1980) Physiological aspects of sprouting and spoilage in developing Triticum aestivum L. (wheat grains). pp 339356 in Hebblethwaite, P.B. (Ed.) Seed production. London, Butterworths.Google Scholar
Muntz, K. (1987) Developmental control of storage protein formation and its modulation by some internal and external factors during embryogenesis in plant seeds. Biochimie und Physiologie der Pflanzen 182, 93116.Google Scholar
Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15, 473497.Google Scholar
Nicholls, P.B. (1979) Induction of sensitivity to gibberellic acid in developing wheat caryopses: effect of rate of desiccation. Australian Journal of Plant Physiology 6, 229240.Google Scholar
Nicholls, P.B. (1986) Induction of sensitivity to gibberellic acid in developing wheat caryopses: effect of sugars in the culture medium. Australian Journal of Plant Physiology 13, 795801.Google Scholar
Norman, H.A., Black, M. and Chapman, J.M. (1982) Induction of sensitivity to gibberellic acid in aleurone tissue of developing wheat grains. II. Evidence for temperature-dependent membrane transitions. Planta 154, 578586.Google Scholar
Norman, H.A., Black, M. and Chapman, J.M. (1983) The induction of sensitivity to gibberellin in aleurone tissue of developing wheat grains. III. Sensitization of isolated protoplasts. Planta 158, 264271.CrossRefGoogle ScholarPubMed
Oishi, M.Y. and Bewley, J.D. (1990) Distinction between the responses of developing maize kernels to fluridone and desiccation in relation to germinability, α-amylase activity and abscisic acid content. Plant Physiology 94, 592598.Google Scholar
Oishi, M.Y. and Bewley, J.D. (1992) Premature drying, fluridone-treatment and embryo isolation during development of maize kernels (Zea mays L.) induce germination, but the protein synthetic responses are different. Potential regulation of germination and protein synthesis by abscisic acid. Journal of Experimental Botany 43, 759767.Google Scholar
Oliver, M.J., Armstrong, J. and Bewley, J.D. (1993) Desiccation and the control of expression of β-phaseolin in transgenic tobacco seeds. Journal of Experimental Botany 44, 12391244.Google Scholar
Quatrano, R.S. (1986) Regulation of gene expression by abscisic acid during angiosperm embryo development. Oxford Surveys of Plant Molecular and Cell Biology 3, 467477.Google Scholar
Quatrano, R.S., Litts, J., Colwell, G., Chakerian, R. and Hopkins, R. (1986) Regulation of gene expression in wheat embryos by ABA: characterization of cDNA clones for the Em and putative globulin proteins and localization of the lectin wheat germ agglutinin. pp 127136 in Shannon, L.M. and Chrispeels, M.J. (Eds) Molecular biology of seed storage proteins and lectins. Baltimore, MD, American Society of Plant Physiology.Google Scholar
Radley, M. (1976) The development of wheat grain in relation to endogenous growth substances. Journal of Experimental Botany 27, 10091021.Google Scholar
Robertson, M., Walker-Simmons, M., Munro, D. and Hill, R.D. (1989) Induction of α-amylase inhibitor synthesis in barley embryos and seedlings by abscisic acid and dehydration stress. Plant Physiology 91, 415420.CrossRefGoogle ScholarPubMed
Robichaud, C., Wong, J. and Sussex, I.M. (1980) Control of in vitro growth of viviparous embryo mutants of maize by abscisic acid. Developmental Genetics 2, 325330.Google Scholar
Rosenberg, L.A. and Rinne, R.W. (1986) Moisture loss as a prerequisite for seedling growth in soybean seeds (Glycine max L. Merr.). Journal of Experimental Botany 37, 16631674.Google Scholar
Skriver, K. and Mundy, J. (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 21, 503512.Google Scholar
Smith, J.D., McDaniel, S. and Lively, S. (1978) Regulation of embryo growth by abscisic acid in vitro. Maize Genetics Cooperative Newsletter 52, 107108.Google Scholar
Sussex, I.M. (1975) Growth and metabolism of the embryo and attached seedlings of the viviparous mangrove, Rhizophora mangle. American Journal of Botany 62, 948953.Google Scholar
Thomas, T.L., Vivekananda, J. and Bogue, M.A. (1991) ABA regulation of gene expression in embryos and mature plants. pp 125135 in Davies, W.J. and Jones, H.G. (Eds) Abscisic acid physiology and biochemistry. Oxford, BIOS Scientific Publishers Ltd.Google Scholar
Weintraub, H. and Izant, J.G. (1984) Developmental control of globulin gene expression. Journal of Cellular Biochemistry (Supplement 8B), 14.Google Scholar
Wellington, P.S. (1956) Studies on the germination of cereals. I. The germination of wheat grains in the ear during development, ripening, and after-ripening. Annals of Botany 20, 105120.Google Scholar
Williamson, J.D. and Quatrano, R.S. (1988) ABA-regulation of two classes of embryo-specific sequences in mature wheat embryos. Plant Physiology 86, 208215.Google Scholar
Williamson, J.D., Quatrano, R.S. and Cuming, A.C. (1985) Em polypeptide and its messenger RNA levels are modulated by abscisic acid during embryogenesis in wheat. European Journal of Biochemistry 152, 501507.CrossRefGoogle ScholarPubMed
Xu, N. and Bewley, J.D. (1991) Sensitivity to abscisic acid and osmoticum changes during embryogenesis of alfalfa (Medicago sativa). Journal of Experimental Botany 42, 821826.Google Scholar