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Histo-differentiation and molecular biology of developing cereal endosperm

Published online by Cambridge University Press:  19 September 2008

O.-A. Olsen ,
R. H. Potter  and
R. Kalla
O.-A. Olsen
Affiliation:
Laboratory for Plant Molecular Biology, Norwegian Agricultural Research Council, PO Box 5051, N-1432 Ås, Norway
R. H. Potter
Affiliation:
Cell and Tissue Culture Group, Norwegian Agricultural Research Council, PO Box 5051, N-1432 Ås, Norway
R. Kalla
Affiliation:
Laboratory for Plant Molecular Biology, Norwegian Agricultural Research Council, PO Box 5051, N-1432 Ås, Norway
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Abstract

To elucidate the molecular aspects of cereal endosperm development, a good understanding of the histo-differentiation process is necessary. Reviewing the extensive history of lightand electron-microscopic investigations has revealed similarities between cereals with respect to cell ontogeny. Thus, using barley as a model and taking into account many developmental mutants in this and other species, a model for endosperm differentiation is proposed. Based on this model, molecular studies on endosperm gene-regulation are discussed and the available techniques for further investigations are considered.

Keywords

histo-differentiationcell ontogenydevelopmental stagesaleuronestarchy endospermtissue-specific gene expressionhierarchical gene regulationcereals
Type
Invited Review
Information
Seed Science Research , Volume 2 , Issue 3 , September 1992 , pp. 117 - 131
Copyright
Copyright © Cambridge University Press 1992

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References

Bajer, A.S. and Mole-Bajer, J. (1986) Reorganization of microtubules in endosperm cells and cell fragments of higher plant Haemanthus in vivo. Journal of Cell Biology 102, 263–281.CrossRefGoogle ScholarPubMed
Bartels, D., Singh, M. and Salamini, F. (1988) Onset of desiccation tolerance during development of the barley embryo. Planta 175, 485–492.CrossRefGoogle ScholarPubMed
Bass, H.W., Webster, C., O'Brian, G.R., Roberts, J.K.M. and Boston, R.S. (1992) A maize ribosome-inactivating protein is controlled by the transcriptional activator opaque-2. Plant Cell 4, 225–234.Google ScholarPubMed
Bechtel, D.B. and Juliano, B.O. (1980) Formation of protein bodies in the starchy endosperm of rice (Oryza sativa L.): a re-investigation. Annals of Botany 45, 503–509.CrossRefGoogle Scholar
Bechtel, D.B. and Pomeranz, Y. (1981) Ultrastructure and chemistry of the mature oat (Avena sativa) endosperm: the aleurone layer and starchy endosperm. Cereal Chemistry 58, 61–69.Google Scholar
Bennett, M.D., Smith, J.B. and Barclay, I. (1975) Early seed development in the Triticeae. Philosophical Transactions of the Royal Society, London, Biological Sciences 272, 199–227.Google Scholar
Bosnes, M. and Olsen, O.-A. (1992) The rate of transcription in barley endosperm syncytia increases six-fold prior to endosperm cell wall formation. Planta 186, 376–383.CrossRefGoogle Scholar
Bosnes, M., Harris, E., Aigeltinger, L. and Olsen, O.-A. (1987) Morphology and ultrastructure of 11 barley shrunken endosperm mutants. Theoretical and Applied Genetics 74, 177–187.CrossRefGoogle ScholarPubMed
Bosnes, M., Widemann, F. and Olsen, O.-A. (1992) Endosperm differentiation in barley wild-type and sex-mutants. Plant Journal 2, 661–674.CrossRefGoogle Scholar
Brenchley, W.E. (1909) On the strength and development of the grain of wheat (Triticum vulgare). Annals of Botany 23, 117–142.CrossRefGoogle Scholar
Brink, R.A. and Cooper, D.C. (1947a) The endosperm in seed development. Botanical Review 13, 423–541.CrossRefGoogle Scholar
Brink, R.A. and Cooper, D.C. (1947b) Effect of the de 17 allele on the development of the maize caryopsis. Genetics 32, 350–368.CrossRefGoogle Scholar
Buttrose, M.S. (1963) Ultrastructure of developing aleurone cells of the wheat grain. Australian Journal of Biological Sciences 16, 768–774.CrossRefGoogle Scholar
Cameron-Mills, V. and von Wettstein, D. (1980) Protein body formation in the developing barley endosperm. Carlsberg Research Communications 45, 577–594.CrossRefGoogle Scholar
Chandra, S. and Bhatnagar, S.P. (1974) Reproductive biology of Triticum. II. Pollen germination, pollen tube growth and its entry into the ovule. Phytomorphology 24, 211–217.Google Scholar
Chojecki, A.J.S., Bayliss, M.W. and Gale, M.D. (1986) Cell production and DNA accumulation in the wheat endosperm, and their association with grain weight. Annals of Botany 58, 809–817.CrossRefGoogle Scholar
Clark, J.K. and Sheridan, W.F. (1986) Developmental profiles of the maize embryo-lethal mutants dek-22 and dek-23. Journal of Heredity 77, 83–92.CrossRefGoogle Scholar
Cochrane, M.P. and Duffus, C.M. (1980) The nucellar projection and modified aleurone in the crease region of developing caryopses of barley (Hordeum vulgare L. var. disticum). Protoplasma 103, 361–375.CrossRefGoogle Scholar
Cochrane, M.P. and Duffus, C.M. (1981) Endosperm cell number in barley. Nature 289, 399–401.CrossRefGoogle Scholar
Cochrane, M.P. and Duffus, C.M. (1983) Endosperm cell number in cultivars of barley differing in grain weight. Annals of Applied Botany 102, 177–181.CrossRefGoogle Scholar
Daynard, T.B. and Duncan, W.G. (1969) The black layer and grain maturity in corn. Crop Science 9, 473–476.CrossRefGoogle Scholar
Dellaporta, S.L., Greenblatt, I., Kermicle, J.L., Hick, J.B. and Wessler, S., (1988) Molecular cloning of the R-nj allele by transposon tagging with Ac. pp. 263–282 in Gustafson, J.P. and Appels, R. (Eds) Chromosome structure and function: impact of new concepts, 18th Stadler Genetics Symposium. New York, Plenum Press.CrossRefGoogle Scholar
Diboll, A.G. (1968) Fine structure development of the megagametophyte of Zea mays following fertilization. American Journal of Botany 55, 787–806.CrossRefGoogle Scholar
Diboll, A.G. and Larson, D.A. (1966) An electronmicroscopy study of the mature megagametophyte in Zea mays. American Journal of Botany 53, 391–402.CrossRefGoogle Scholar
Dooner, H.K., Robbins, T.P. and Jorgensen, R.A. (1991) Genetic and developmental control of anthocyanin biosynthesis. Annual Review of Genetics 25, 173–199.CrossRefGoogle ScholarPubMed
Driever, W. and Nusslein-Volhard, C. (1989) The Bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 337, 138–143.CrossRefGoogle ScholarPubMed
Ellis, J.R., Gates, P.J. and Boulter, D. (1987) Storage protein deposition in the developing rice caryopsis in relation to the transport tissues. Annals of Botany 60, 663–670.CrossRefGoogle Scholar
Engell, K. (1989) Embryology of barley: time course and analysis of controlled fertilization and early embryo formation based on serial sections. Nordic Journal of Botany 9, 265–280.CrossRefGoogle Scholar
Evers, A.D. (1970) Development of the endsperm of wheat. Annals of Botany 34, 547–555.CrossRefGoogle Scholar
Eyster, W.H. (1934) The genetics of Zea mays L. Bibliographia Genetica 11, 187–392.Google Scholar
Felker, F.C., Peterson, D.M. and Nelson, O.N. (1985) Anatomy of immature grains of eight maternal effect shrunken endosperm barley mutants. American Journal of Botany 72, 248–256.CrossRefGoogle Scholar
Fineran, B.A., Wild, D.J.C. and Ingerfeld, M., (1982) Initial endosperm formation in the endosperm of wheat; a reevaluation. Canadian Journal of Botany 60, 1776–1795.CrossRefGoogle Scholar
Forster, B.P. and Dale, J.E. (1983) A comparative study of early seed development in genotypes of barley and rye. Annals of Botany 52, 603–612.CrossRefGoogle Scholar
Friedman, W.E. (1992) Evidence of a pre-angiosperm origin of endosperm: implications for the evolution of flowering plants. Science 255, 336–339.CrossRefGoogle ScholarPubMed
Fulcher, R.G., O'Brien, T.P. and Lee, J.W. (1972) Studies on the aleurone layer. 1. Conventional and fluorescence microscopy of the cell wall with emphasis on phenolcarbohydrate complexes in wheat. Australian Journal of Biological Sciences 25, 23–34.CrossRefGoogle Scholar
Gordon-Kamm, W.J., Spencer, T.M., Mangano, M.L., Adams, T.R., Daines, R.J., Start, W.G., O'Brien, J.V., Chambers, S.A., Adams, W.R., Willetts, N.G., Rice, T.B., Mackey, C.J., Krueger, R.W., Kausch, A.P. and Lemaux, P.G. (1990) Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell 2, 603–618.CrossRefGoogle ScholarPubMed
Gustafson, J.P. and Lukaszewski, A.J. (1985) Early seed development in Triticum and Secale amphiploids. Canadian Journal of Genetics and Cytology 27, 542–548.CrossRefGoogle Scholar
Hartings, H., Maddaloni, M., Lazzaroni, N., Di Fonzo, N., Motto, M., Salamini, F. and Thompson, R. (1989) The 02 gene which regulates zein deposition in maize endosperm encodes a protein with structural homologies to transcriptional activators. EMBO Journal 8, 2795–2801.CrossRefGoogle Scholar
Huber, A.G. and Grabe, D.F. (1987a) Endosperm morphogenesis in wheat: transfer of nutrients from the antipodals to the lower endosperm. Crop Science 27, 1248–1252.CrossRefGoogle Scholar
Huber, A.G. and Grabe, D.F. (1987b) Endosperm morphogenesis in wheat: termination of nuclear division. Crop Science 27, 252–1256.CrossRefGoogle Scholar
Ingham, P.W. (1988) The molecular genetics of embryonic pattern formation in Drosophila. Nature 355, 25–34.CrossRefGoogle Scholar
Jakobsen, K., Klemsdal, S., Aalen, R., Bosnes, M., Alexander, D. and Olsen, O.-A. (1989) Barley aleurone cell development: molecular cloning of aleurone-specific cDNAs from immature grains. Plant Molecular Biology 12, 285–293.CrossRefGoogle ScholarPubMed
Johannsen, W. (1884) Om frøhviden og dens udvikling hos Byg. Meddelelser fra Carlsberg Laboratoriet, (1883–1888) Kopenhagen, Bind II, 103–133.Google Scholar
Keown, A.C., Taiz, L. and Jones, R.L. (1977) The nuclear DNA content of developing barley aleurone cells. American Journal of Botany 64, 1248–1253.CrossRefGoogle Scholar
Kiesselbach, T.A. (1949) The structure and reproduction of corn. Research Bulletin, University of Nebraska College of Agriculture, Experimental Station 161.Google Scholar
Klemsdal, S.S., Hughes, W., Lønneborg, A., Aalen, R.B. and Olsen, O.-A. (1991) Primary structure of a novel barley gene differentially expressed in mature aleurone layers. Molecular and General Genetics 228, 9–16.CrossRefGoogle Scholar
Knudsen, S. and Müller, M. (1991) Transformation of the developing barley endosperm by particle bombardment. Planta 185, 330–336.CrossRefGoogle ScholarPubMed
Kowles, R.V. and Phillips, R.L. (1988) Endosperm development in maize. International Review of Cytology 112, 97–136.CrossRefGoogle Scholar
Kreis, M., Williamson, M.S., Forde, J., Schmutz, D., Clark, J., Buxton, B., Pywell, J., Marris, C., Henderson, J., Harris, N., Shewry, P.R., Forde, B-G. and Miflin, B.J. (1986) Differential gene expression in the developing barley endosperm. Philosophical Transactions of the Royal Society, London, Biological Sciences 314, 355–365.Google Scholar
Kuwada, Y. (1909) On the development of pollen and the embryo sac, and the formation of the endosperm, etc. of Oryza sativa L. Botanical Magazine (Tokyo) 23, 334–343.Google Scholar
Kvaale, A. and Olsen, O.-A. (1986) Rates of cell division in developing barley endosperms. Annals of Botany 57, 829–833.CrossRefGoogle Scholar
Kyle, D.J. and Styles, E.D. (1977) Development of aleurone and sub-aleurone layers in maize. Planta 137, 185–193.CrossRefGoogle ScholarPubMed
Lee, B.T., Murdoch, K., Topping, J., Kreis, M. and Jones, M.G.K. (1989) Transient gene expression in aleurone protoplasts isolated from developing caryopses of barley and wheat. Plant Molecular Biology 13, 21–29.CrossRefGoogle ScholarPubMed
Lee, B.T., Murdoch, K., Topping, J., Jones, M.G.K. and Kreis, M. (1991) Transient expression of foreign genes introduced into barley endosperm protoplasts by PEG-mediated transfer or into intact endosperm tissue by microprojectile bombardment. Plant Science 78, 237–246.CrossRefGoogle Scholar
Linnestad, C., Lønneborg, A., Kalla, R. and Olsen, O.-A. (1991) The promoter of a lipid transfer protein gene expressed in barley aleurone cells contains similar myb and myc recognition sites as the maize Bz-McC allele. Plant Physiology 97, 841–843.CrossRefGoogle ScholarPubMed
Lohmer, S., Maddaloni, M., Motto, M., Di Fonzo, N., Hartings, H., Salamini, F. and Thompson, R. (1991) The maize regulatory locus opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. EMBO Journal 10, 617–624.CrossRefGoogle ScholarPubMed
Lowe, J. and Nelson, O.E. (1947) Miniature seed — a study in the development of a defective caryopsis in maize. Genetics 31, 525–533.CrossRefGoogle Scholar
Ludwig, S.R., Habera, L.F., Dellaporta, S.L. and Wessler, S.R. (1989) Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proceedings of the National Academy of Sciences of the USA 86, 7092–7096.CrossRefGoogle Scholar
Mangelsdorf, P.C. (1926) The genetics and morphology of some endosperm characters in maize. Connecticut Experimental Station Bulletin 279, 513–614.Google Scholar
Manzocchi, L.A., Daminati, M.G. and Gentinetta, E., (1980) Viable endosperm mutants in maize. II. Kernel weight, nitrogen and zein accumulation during endosperm development. Maydica XXV, 199–210.Google Scholar
McCarty, D.R. and Carson, C.B. (1991) The molecular genetics of seed maturation in maize. Physiologia Plantarum. 81, 267–272.CrossRefGoogle Scholar
McCarty, D.R., Carson, C.B., Stinard, P.S. and Robertson, D.S. (1989) Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. Plant Cell 1, 523–532.CrossRefGoogle ScholarPubMed
McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M. and Vasil, I.K. (1991) The viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66, 895–905.CrossRefGoogle ScholarPubMed
McClintock, B., (1978) Development of the maize endosperm as revealed by clones. pp. 217–237 in Subtelny, S. and Sussex, I.M. (Eds) The clonal basis of development. New York, Academic Press.Google Scholar
Morrison, I.N., Kuo, J. and O'Brian, T.P. (1975) Histochemistry and fine structure of developing wheat aleurone cells. Planta 123, 105–116.CrossRefGoogle ScholarPubMed
Morrison, I.N., O'Brien, T.P. and Kuo, J., (1978) Initial cellularization and differentiation of the aleurone cells in the ventral region of the developing wheat grain. Planta 140, 19–30.CrossRefGoogle Scholar
Mundy, J., Hejgaard, J., Hansen, A., Hallgren, L., Jørgensen, K.G. and Munck, L., (1986) Differential synthesis in vitro of barley aleurone and starchy endosperm proteins. Plant Physiology 81, 630–636.CrossRefGoogle ScholarPubMed
Nawaschin, S., (1898) Resultate eine revision der Befruchtungsvorgange bei Lilium martagon und Fritillaria tenella. Bulletin of the Academy of Imperial Sciences, St. Petersburg 9, 377–382.Google Scholar
Neuffer, M.G. and Sheridan, W.G. (1980) Defective kernel mutants of maize. I. Genetic and lethality studies. Genetics 95, 929–944.CrossRefGoogle Scholar
Olsen, O.-A., Jakobsen, K.S. and Schmelzer, E., (1990) Development of barley aleurone cells: temporal and spatial patterns of accumulation of cell specific mRNAs. Planta 181, 462–566.CrossRefGoogle ScholarPubMed
Oparka, K.J. and Gates, P. (1981) Transport of assimilates in the developing caryopsis of rice (Oryza sativa): Ultrastructure of the pericarp vascular bundle and its connections with the aleurone layer. Planta 151, 561–572.CrossRefGoogle ScholarPubMed
Parker, M.L. (1981) The structure of mature rye endosperm. Annals of Botany 47, 181–186.CrossRefGoogle Scholar
Paz-Ares, J., Ghosal, D., Wienand, U., Peterson, P.A. and Saedler, H., (1987) The regulatory cl locus of Zea mays encodes a protein with a homology to myb protoncogene products and with a structural similarities to transcriptional activators. EMBO Journal 6, 3553–3558.CrossRefGoogle Scholar
Peterson, D.M., Saigo, R.H. and Holy, J., (1985) Development of oat aleurone cells and their protein bodies. Cereal Chemistry 62, 366–371.Google Scholar
Qu, R., Wang, S.M., Lin, Y.H., Vance, V.B. and Huang, A.H.C. (1986) Characteristics and biosynthesis of membrane proteins of lipid bodies in the scutella of maize (Zea mays L.). Biochemical Journal 235, 57–65.CrossRefGoogle ScholarPubMed
Ramachandran, C. and Raghavan, V., (1989) Changes in the nuclear DNA content of endosperm cells during grain development in rice (Oryza sativa). Annals of Botany 64, 459–468.CrossRefGoogle Scholar
Ramage, R.T. and Crandall, C.L. (1981a) A proposed gene symbol for defective endosperm mutants that express xenia. Barley Genetics Newsletter 11, 30–31.Google Scholar
Ramage, R.T. and Crandall, C.L. (1981b) Defective endosperm xenia (dex) mutants. Barley Genetics Newsletter 11, 32–33.Google Scholar
Randolph, L.F. (1936) Developmental morphology of the caryopsis in maize. Journal of Agricultural Research 53, 881–916.Google Scholar
Roth, B.A., Goff, S.A., Klein, T.M. and Fromm, M.E. (1991) Cl- and R-dependent expression of the maize Bzl gene requires sequences with homology to mammalian myb and myc binding sites. Plant Cell 3, 317–325.Google Scholar
Saigo, R.H., Peterson, D.M. and Holy, J., (1983) Development of protein bodies in oat starchy endosperm. Canadian Journal of Botany 61, 1206–1215.CrossRefGoogle Scholar
Scandalios, J.G. (1982) Developmental genetics of maize. Annual Review of Genetics 16, 85–112.CrossRefGoogle ScholarPubMed
Schel, J.H.N., Kiett, H. and Vann Lammeren, A.A. (1984) Interactions between embryo and endosperm during early developmental stages of maize caryopses (Zea mays). Canadian Journal of Botany 62, 2842–2853.CrossRefGoogle Scholar
Schmidt, R.J., Burr, F.J., Aukerman, M.J. and Burr, B. (1990) Maize regulatory gene opaque-2 encodes a protein with a ‘leucine-zipper’ motif that binds to zein DNA. Proceedings of the National Academy of Sciences of the USA. 87, 46–50.CrossRefGoogle ScholarPubMed
Sheridan, W.F. and Neuffer, M.G. (1980) Defective kernal mutants of maize. II. Morphological and embryo culture studies. Genetics 95, 945–960.CrossRefGoogle Scholar
Sheridan, W.F. and Neuffer, M.G. (1981) Maize mutants altered in embryo development. pp. 137–156 in Subtelny, S. (Ed.) Levels of genetic control and development. New York, Liss.Google Scholar
Shimamoto, K., Terada, R., Izawa, T. and Fujimoto, H., (1989) Fertile transgenic rice plants regenerated from transformed protoplasts. Nature 338, 274–276.CrossRefGoogle Scholar
Soave, C. and Salamini, F., (1984) The role of structural and regulatory genes in the development of maize endosperm. Developmental Genetics 5, 1–25.CrossRefGoogle Scholar
Sørensen, M.B., Cameron-Mills, V. and Brandt, A. (1989) Transcriptional and post-transcriptional regulation of gene expression in developing barley endosperm. Molecular and General Genetics 217, 195–201.CrossRefGoogle Scholar
Strasburger, E., (1900) Einige Bemenrkungen zur Frage nach der ‘Doppelten Befruchtung’ bei Angiospermen. Botanische Zeitung 58, 293–316.Google Scholar
Tanaka, K. and Sugiyama, Y., (1991) Construction of aleurone tissue specific cDNA library from a single rice grain using polymerase chain reaction and detection of aleurone specific gene expression. p. 638 in Molecular biology of plant growth and development: proceedings of the third meeting of the International Society for Plant Molecular Biology, Tucson, Arizona.Google Scholar
True, R.H. (1893) On the development of the caryopsis. Botanical Gazette 18, 212–226.CrossRefGoogle Scholar
Van Lammeren, A.A.M. (1988) Structure and function of the microtubular cytoskeleton during endosperm development in wheat: an immuno-fluorescent study. Protoplasma 146, 18–27.CrossRefGoogle Scholar
Vijayaraghavan, M.R. and Prabhakart, K. (1984) The endosperm. pp. 319–376 in Johri, B.M. (Ed.) Embryology of angiosperms. Berlin, Springer Verlag.CrossRefGoogle Scholar
Wheeler, A.H. (1972) Changes in growth-substance content during growth of wheat. Annals of Applied Biology 72, 327–34.CrossRefGoogle Scholar
Yatsu, L.Y. and Jacks, T.J. (1972) Spherosome membranes. Plant Physiology 49, 937–943.CrossRefGoogle ScholarPubMed