Abstract
Two novel maize genes expressed specifically in the central cell of the female gametophyte and in two compartments of the endosperm (the basal endosperm transfer layer and the embryo surrounding region) were characterized. The ZmEBE (embryo sac/basal endosperm transfer layer/embryo surrounding region) genes were isolated by a differential display between the upper and the lower half of the kernel at 7 days after pollination (DAP). Sequence analysis revealed ORFs coding for two closely related proteins of 304 amino acids (ZmEBE-1) and 286 amino acids (ZmEBE-2). This size difference was due to differences in the splicing of the two genes. Both protein sequences showed significant similarity to the DUF239 family of Arabidopsis, a group of 22 proteins of unknown function, a small number of which are putative peptidases. ZmEBE genes had a novel cell type-specific expression pattern in the central cell before and the resulting endosperm after fertilization. RT-PCR analysis showed that the expression of both genes started before pollination in the central cell and continued in the kernel up to 20 DAP with a peak at 7 DAP. In situ hybridization revealed that the expression in the kernel was restricted to the basal transfer cell layer and the embryo surrounding region of the endosperm. The expression of ZmEBE-1 was at least 10 times lower than that of ZmEBE-2. Similarly to other genes expressed in the endosperm, ZmEBE-1 expression was subject to a parent-of-origin effect, while no such effect was detected in ZmEBE-2. Sequence analysis of upstream regions revealed a potential cis element of 33 bp repeated 7 times in ZmEBE-1 and ZmEBE-2 between positions −900 and −100. The 1.6 kb ZmEBE-2 upstream sequence containing the seven R7 elements was able to confer expression in the basal endosperm to a Gus reporter gene. These data indicate that ZmEBE is potentially involved in the early development of specialized domains of the endosperm and that this process is possibly already initiated in the central cell, which is at the origin of the endosperm.
Similar content being viewed by others
References
Alleman, M. and Doctor, J. 2000. Genomic imprinting in plants: observations and evolutionary implications. Plant Mol. Biol. 43: 147–161.
Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.
Barloy, D., Denis, L. and Beckert, M. 1989. Comparison of the aptitude for anther culture in some androgenetic doubled haploid maize lines. Maydica 34: 303–308.
Batley, J., Barker, G., O'Sullivan, H., Edwards, K.J. and Edwards, D. 2003. Mining for single nucleotide polymorphisms and insertions/ deletions in maize expressed sequence tag data. Plant Physiol. 132: 84–91.
Bonello, J.-F., Opsahl-Ferstad, H.-G., Perez, P., Dumas, C. and Rogowsky, P.M. 2000. Esr genes show different levels of expression in the same region of maize endosperm. Gene 246: 219–227.
Bradley, D., Carpenter, R., Sommer, H., Hartley, N. and Coen, E. 1993. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72: 85–95.
Burr, B. and Burr, F.A. 1991. Recombinant inbreds for molecular mapping in maize: theoretical and practical considerations. Trends Genet. 7: 55–60.
Charlton, W.L., Keen, C.L., Merriman, C., Lynch, P., Greenland, A.J. and Dickinson, H.G. 1995. Endosperm development in Zea mays: implication of gametic imprinting and paternal excess in regulation of transfer layer development. Development 121: 3089–3097.
Chaudhury, A.M., Craig, S., Dennis, E. and Peacock, W. 1998. Ovule and embryo development, apomixis and fertilization. Curr. Opin. Plant Biol. 1: 26–31.
Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E. and Fischer, R.L. 2002. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell 110: 33–42.
Coen, E.S., Romero, J.M., Doyle, S., Elliott, R., Murphy, G. and Carpenter, R. 1990. floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63: 1311–1322.
Cordts, S., Bantin, J., Wittich, P.E., Kranz, E., Lorz, H. and Dresselhaus, T. 2001. ZmES genes encode peptides with structural homology to defensins and are specifically expressed in the female gametophyte of maize. Plant J. 25: 103–114.
Danilevskaya, O.N., Hermon, P., Hantke, S., Muszynski, M.G., Kollipara, K. and Ananiev, E.V. 2003. Duplicated fie genes in maize: Expression pattern and imprinting suggest distinct functions. Plant Cell 15: 425–438.
Davis, R.W., Smith, J.D. and Cobb, B.G. 1990. A light and electron microscope investigation of the transfer cell region of maize caryopses. Can. J. Bot. 68: 471–479.
Doan, D.N., Linnestad, C. and Olsen, O.A. 1996. Isolation of molecular markers from the barley endosperm coenocyte and the surrounding nucellus cell layers. Plant Mol. Biol. 31: 877–886.
Dresselhaus, T., Cordts, S., Heuer, S., Sauter, M., Lorz, H. and Kranz, E. 1999a. Novel ribosomal genes from maize are differentially expressed in the zygotic and somatic cell cycles. Mol. Gen. Genet. 261: 416–427.
Dresselhaus, T., Cordts, S. and Lorz, H. 1999b. A transcript encoding translation initiation factor eIF-5A is stored in unfertilized egg cells of maize. Plant Mol. Biol. 39: 1063–1071.
Drews, G.N., Lee, D. and Christensen, C.A. 1998. Genetic analysis of female gametophyte development and function. Plant Cell 10: 5–17.
Gerdes, J.T. and Tracy, W.F. 1993. Pedigree diversity within the Lancaster surecrop heterotic group of maize. Crop Sci. 33: 334–337.
Gomez, E., Royo, J., Guo, Y., Thompson, R. and Hueros, G. 2002. Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14: 599–610.
Grossniklaus, U., Spillane, C., Page, D.R. and Kohler, C. 2001. Genomic imprinting and seed development: endosperm formation with and without sex. Curr. Opin. Plant Biol. 4: 21–27.
Guo, M., Rupe, M.A., Danilevskaya, O.N., Yang, X. and Hu, Z. 2003. Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J. 36: 30–44.
Helentjaris, T. 1995. Atlas of duplicated sequences. Maize Genet. Coop. Newsl. 69: 67–82.
Heuer, S., Hansen, S., Bantin, J., Brettschneider, R., Kranz, E., Lorz, H. and Dresselhaus, T. 2001. The maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development, in egg cells, and early embryogenesis. Plant Physiol. 127: 33–45.
Higo, K., Ugawa, Y., Iwamoto, M. and Korenaga, T. 1999. Plant cisacting regulatory DNA elements (PLACE) database: 1999. Nucl. Acids Res. 27: 297–300.
Hueros, G., Gomez, E., Cheikh, N., Edwards, J., Weldon, M., Salamini, F. and Thompson, R.D. 1999a. Identification of a promoter sequence from the BETL1 gene cluster able to confer transfer-cell-specific expression in transgenic maize. Plant Physiol. 121: 1143–1152.
Hueros, G., Royo, J., Maitz, M., Salamini, F. and Thompson, R.D. 1999b. Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol. Biol. 41: 403–414.
Hueros, G., Varotto, S., Salamini, F. and Thompson, R.D. 1995. Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7: 747–757.
Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.
Lin, B.-Y. 1982. Association of endosperm reduction with parental imprinting in maize. Genetics 100: 475–786.
Luo, M., Bilodeau, P., Dennis, E.S., Peacock, W.J. and Chaudhury, A. 2000. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 97: 10637–10642.
Magnard, J.L., Le Deunff, E., Domenech, J., Rogowsky, P.M., Testillano, P.S., Rougier, M., Risueno, M.C., Vergne, P. and Dumas, C. 2000. Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Mol. Biol. 44: 559–574.
Nadeau, J.A., Zhang, X.S., Li, J. and O'Neill, S.D. 1996. Ovule development: identification of stage-specific and tissue-specific cDNAs. Plant Cell 8: 213–239.
Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10: 1–6.
Olsen, O.A., Linnestad, C. and Nichols, S.E. 1999. Developmental biology of the cereal endosperm. Trends Plant Sci. 4: 253–257.
Opsahl-Ferstad, H.G., Le Deunff, E., Dumas, C. and Rogowsky, P.M. 1997. ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J. 12: 235–246.
Pischke, M.S., Jones, L.G., Otsuga, D., Fernandez, D.E., Drews, G.N. and Sussman, M.R. 2002. An Arabidopsis histidine kinase is essential for megagametogenesis. Proc. Natl. Acad. Sci. USA 99: 15800–15805.
Richert, J., Kranz, E., Lörz, H. and Dresselhaus, T. 1996. A reverse transcriptase-polymerase chain reaction assay for gene expression studies at the single cell level. Plant Sci. 114: 93–99.
Rombauts, S., Dehais, P., Van Montagu, M. and Rouze, P. 1999. PlantCARE, a plant cis-acting regulatory element database. Nucl. Acids Res. 27: 295–296.
Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Sauter, M., von Wiegen, P., Lörz, H. and Kranz, E. 1998. Cell cycle regulatory genes from maize are differentially controlled during fertilization and first embryonic cell division. Sex. Plant Reprod. 11: 41–48.
Schel, J.H.N., Kieft, H. and van Lammeren, A.A.M. 1984. Interaction between embryo and endosperm during early developmental stages of maize caryopses (Zea mays). Can. J. Bot. 62: 2842–2853.
Scott, R.J., Spielman, M., Bailey, J. and Dickinson, H.G. 1998. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125: 3329–3341.
Serna, A., Maitz, M., O'Connell, T., Santandrea, G., Thevissen, K., Tienens, K., Hueros, G., Faleri, C., Cai, G., Lottspeich, F. and Thompson, R.D. 2001. Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J. 25: 687–698.
Sevilla-Lecoq, S., Deguerry, F., Matthys-Rochon, E., Perez, P., Dumas, C. and Rogowsky, P.M. 2003. Analysis of ZmAE3 upstream sequences in maize endosperm and androgenic embryos. Sex. Plant Reprod. 16: 1–8.
Sorensen, M.B., Chaudhury, A.M., Robert, H., Bancharel, E. and Berger, F. 2001. Polycomb group genes control pattern formation in plant seed. Curr. Biol. 11: 277–281.
Spillane, C., MacDougall, C., Stock, C., Kohler, C., Vielle-Calzada, J.P., Nunes, S.M., Grossniklaus, U. and Goodrich, J. 2000. Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes. Curr. Biol. 10: 1535–1538.
Springer, P.S., Holding, D.R., Groover, A., Yordan, C. and Martienssen, R.A. 2000. The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127: 1815–1822.
Stalberg, K., Ellerstom, M., Ezcurra, I., Ablov, S. and Rask, L. 1996. Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199: 515–519.
Vielle-Calzada, J.P., Thomas, J., Spillane, C., Coluccio, A., Hoeppner, M.A. and Grossniklaus, U. 1999. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13: 2971–2982.
Weschke, W., Panitz, R., Sauer, N., Wang, Q., Neubohn, B., Weber, H. and Wobus, U. 2000. Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J. 21: 455–467.
Wessler, S.R., Bureau, T.E. and White, S.E. 1995. LTRretrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5: 814–821.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Magnard, JL., Lehouque, G., Massonneau, A. et al. ZmEBE genes show a novel, continuous expression pattern in the central cell before fertilization and in specific domains of the resulting endosperm after fertilization. Plant Mol Biol 53, 821–836 (2003). https://doi.org/10.1023/B:PLAN.0000023672.37089.00
Issue Date:
DOI: https://doi.org/10.1023/B:PLAN.0000023672.37089.00