Abstract
The cereal endosperm develops from a coenocyte to a cellular storage organ through formation of nucleo-cytoplasmic domains and cell wall deposition in the interzones between these domains. During its early stages, the endosperm develops in close contact with nucellus, the sporophytic tissue which gives rise to the megagametophyte. Owing to the positioning of the two tissues deeply within the ovary, neither cell types have been easily accessible for molecular studies. In this paper we report for the first time the cloning of molecular markers for the barley endosperm coenocyte and the nucellus. The novel END1 and NUC1 cDNAs were isolated by differential screening of a cDNA library from 5 DAP (days after pollination) ovaries using a positive probe from hand-dissected embryo sacs with adhering nucellus and testa cell layers, and a negative probe from pericarp. In situ and northern blot hybridization data show that END1 transcripts are asymmetrically distributed in teh endosperm coenocyte limited to an area over the nucellar projection. In the cellular endosperm, END1 transcripts are present in modified aleurone cells and a few layers of ventral starchy endosperm cells. The second clone, NUC1, hybridizes to transcripts in the nucellus before fertilization and in autolyzing nucellus cells after fertilization. At later stages, after the disappearance of nucellus, NUC1 transcripts are present in the nucellar epidermis and in the lateral cells of the nucellar projection. This work provide tools for future elucidation of the genes specifying endosperm histogenesis.
Similar content being viewed by others
References
Aalen RB, Opsahl-Ferstad HG, Linnestad C, Olsen O-A: Transcripts encoding an oleosin and a dormancy related protein are present both in the aleurone layer and the embryo of developing barley (Hordeum vulgare L.) seeds. Plant J 5: 385–396 (1994).
Berger F, Taylor A, Brownlee C: Cell fate determination by the cell wall in early Fucus development. Science 263: 1421–1423 (1994).
Bosnes M, Olsen O-A: The rate of nuclear gene transcription in barley endosperm syncytia increases sixfold before cell wall formation. Planta 186: 376–383 (1992).
Bosnes M, Weideman F, Olsen O-A: Endosperm differentiation in barley wild-type and sex mutants. Plant J 2: 661–674 (1992).
Brown RC, Lemmon BE: Cytoplasmic domain: A model for spatial control of cytokinesis in reproductive cells of plants, EMSA Bull 22: 48–53 (1992).
Brown RC, Lemmon BE: Diversity of cell division in simple land plants holds clues to evolution of the mitotic and cytokinetic apparatus in higher plants Mem Torrey Bot Club 25: 45–62 (1993).
Brown RC, Lemmon BE, Olsen O-A: Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6: 1241–1252 (1994).
Cass DD, Peteya DJ, Robertson BL: Megagametophyte development in Hordeum vulgare. 1. Early megagametogenesis and the nature of cell wall formation. Can J Bot 63: 2164–2171 (1985).
Cory S: Apoptosis. Fascinating death factor. Nature 367: 317–318 (1994).
Cochrane MP, Duffus CM: The nucellar projection and modified aleurone in the crease region of developing caryopses of barley (Hordeum vulgare L. var. distichum). Protoplasma 103: 361–375 (1980).
Decroocq-Ferrant V, Decroocq S, vanWent J, Schmidt E, Kreis M: A homologue of the MAP/ERK family of protein kinase genes is expressed in vegetative and in female reproductive organs of Petunia hybrida. Plant Mol Biol 27: 339–350 (1995).
Driever W, Thoma G, Nusslein-Vollard C: Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 304: 363–367 (1989).
Duffus CM, Cohrane MP: Grain structure and composition. In: Shewry PR (ed) Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology, pp. 291–317 CAB Intl., UK (1992).
Engell K: Embryology of barley: time course and analysis of controlled fertilization and early embryo formation based on serial sections. Nord J Bot 9: 265–280 (1989).
Engell K: Embryology of barley. IV. Ultrastructure of the antipodal cells of Hordeum vulgare L. cv. Bomi before and after fertilization of the egg cell. Sex Plant Reprod 7: 333–346 (1994).
Esau K: Plant Anatomy, 2nd ed. John Wiley, New York (1965).
Espelund M, Stacy RAP, Jakobsen KS: A simple method for generating single-stranded DNA probes labelled to high activities. Nucl Acids Res 18: 6157–6158 (1990).
Felker FC, Peterson DM, Nelson OE: Anatomy of immature grains of eight maternal effect shrunken barley mutants. Am J Bot 72: 248–256 (1985).
Guignard L: Sur les anthérozoides et la double copulation sexuelles chez les végétaux angiosperme. Rev Gén Bot 11: 129–135 (1899).
Gunning BES: The cytokinetic apparatus: Its development and spatial regulation. In: Loyd CW (ed) The Cytoskeleton in Plant Growth and Development, pp. 229–292. Academic Press. London (1982).
Hueros G, Varotto S, Salamini F, Thompson RD: Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7: 747–757 (1995).
Jakobsen KS, Breivold E, Hornes E: Purification of mRNA directly from crude plant tissue in 15 minutes using magnetic oligo dT microspheres. Nucl Acids Res 18: 3669 (1990).
Kalla R, Shimamoto K, Potter R, Nielsen PS, Linnestad C, Olsen O-A: The promoter of the barley aleurone specific gene encoding a putative 7 kDa lipid transfer protein confers aleurone cell specific expression in transgenic rice. Plant J 4: 849–860 (1994).
Kvaale A, Olsen O-A: Rate of cell division in developing barley endosperms. Ann Bot 57: 829–833 (1986).
Lloyd CW: The plant cytoskeleton: the impact of fluorescence microscopy. Annu Rev Plant Physiol 38: 119–139 (1987).
Lloyd CW, Barlow PB: the co-ordination of cell division and elongation: the role of the cytoskeleton. In: Lloyd CW (ed) The Cytoskeleton in Plant Growth and Development, pp. 203–228. Academic Press, New York/London (1982).
Lopes MA, Larkins BA: Ehdosperm origin, development, and function. Plant Cell 5: 1383–1399 (1993).
Maheshwari P: An introduction to the embryology of angio-sperms. McGraw-Hill London/New York (1950).
Menzel D, Jonitz H, Elsner-Menzel C: The cytoskeleton in the life cycle of Acetabularia and other related species of dasyclad green alga. In: Menzel D (ed) The Cytoskeleton of the Algae, pp. 195–217. CRC Press, Boca Raton, FL (1992).
Mol R, Matthys-Rochon E, Dumas C: In vitro culture of fertilized embryo sacs of maize: zygotes and two-celled proembryos can develop into plants. Planta 189: 213–217 (1993).
Nawaschin SG: Resultate einer Revision der Befruchtungs-vorgänge beim Liliummartagon and Fritillaria tenella. Bull Acad Imp Sci St Petersburg 9: 377–382 (1898).
Norstog K: Nucellus during early embryogeny in barley: fine structure. Bot Gazette 35: 97–103 (1974).
Olsen O-A, Potter RH, Kalla R: Histo-differentiation and molecular biology of developing cereal endosperm. Seed Sci Res 2: 117–131 (1992).
Olsen O-A, Lemmon B, Brown R: Pattern and process of wall formation in developing endosperm. BioEssays 17: 1–10 (1995).
Raghavan V, Olmedilla A: Spatial patterns of histone mRNA expression during grain development and gerimination in rice. Cell Diff Devel 27: 183–196 (1989).
Reiser L, Fischer RL: The ovule and the embryo sac. Plant Cell 5: 1291–1301 (1993).
Sambrook J, Frisch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Col Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Staiger CJ, Lloyd CW: The plant cytoskeleton. Curr Opin Cell Biol 3: 33–42 (1991).
Wagner VT, Song YC, Matthys-Rochon E, Dumas C: Observations on the isolated embryo sac of Zea mays L. Plant Sci 59: 127–132 (1989).
Wang N, Fisher DB: Monitoring phloem unloading and post-phloem transport by microperfusion of attached wheat grains. Plant Physiol 104: 7–16 (1994).
Wang S, Hazelrigg T: Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. Nature 369: 400–403 (1994).
Warn RM: The cytoskeleton of the early Drosophila embryo. J Cell Sci Suppl 5: 311–328 (1986).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Doan, D.N.P., Linnestad, C. & Olsen, OA. Isolation of molecular markers from the barley endosperm coenocyte and the surrounding nucellus cell layers. Plant Mol Biol 31, 877–886 (1996). https://doi.org/10.1007/BF00019474
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00019474