Abstract
Fertilization triggers a unique and complex developmental program leading to embryogenesis and seed set. Recently, mutations affecting chromatin-remodeling enzymes in plants have shown their key roles in development as demonstrated before in animal cells. Using a negative selection screen to isolate genes expressed in ovary tissues upon fertilization, we have identified a histone deacetylase gene (named ScHD2a) of the plant-specific HD2 family, which is predominantly expressed in ovaries of the self-incompatible species Solanum chacoense. The ScHD2a is the probable orthologue of the Arabidopsis thaliana AtHD2a gene, which upon antisense suppression leads to aborted seeds formation. Transcription of the ScHD2a gene is strongly triggered by fertilization and transcripts accumulate predominantly in the micropylar region of the ovule's integument. Interestingly, this fertilization-induced accumulation pattern was also observed for other genes involved in transcriptional repression but not for a MYST-family histone acetyltransferase. The strong increase in ScHD2a mRNA levels in ovules after fertilization suggests an important and localized role for transcriptional repression in seed development, and indicates why silencing of the AtHD2a gene leads to aborted seed formation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahringer, J. 2000. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 16: 351–356.
Brandstadter, J., Rossbach, C. and Theres, K. 1994. The pattern of histone H4 expression in the tomato shoot apex changes during development. Planta 192: 69–74.
Burge, C.B., Padgett, R.A. and Sharp, P.A. 1998. Evolutionary fates and origins of U12-type introns. Mol. Cell 2: 773–785.
Chaudhury, A.M. and Berger, F. 2001. Maternal control of seed development. Semin. Cell Dev. Biol. 12: 381–386.
Dangl, M., Brosch, G., Haas, H., Loidl, P. and Lusser, A. 2001. Comparative analysis of HD2 type histone deacetylases in higher plants. Planta 213: 280–285.
Goodrich, J. and Tweedie, S. 2002. Remembrance of things past: chromatin remodeling in plant development. Annu. Rev. Cell Dev. Biol. 18: 707–746.
Heinzel, T., Lavinsky, R.M., Mullen, T.M., Soderstrom, M., Laherty, C.D., Torchia, J., Yang, W.M., Brard, G., Ngo, S.D., Davie, J.R., Seto, E., Eisenman, R.N., Rose, D.W., Glass, C.K. and Rosenfeld, M.G. 1997. A complex containing NCoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 387: 43–48.
Holstege, F.C., Jennings, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S. and Young, R.A. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717–728.
Jasencakova, Z., Meister, A., Walter, J., Turner, B.M. and Schubert, I. 2000. Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12: 2087–2100.
Jones, J.D.G., Dunsmuir, P. and Bedbrook, J. 1985. High level expression of introduced chimeric genes in regenerated transformed plants. EMBO J. 4: 2411–2418.
Lantin, S., O'Brien, M. and Matton, D.P. 1999. Pollination, wounding and jasmonate treatments induce the expression of a developmentally regulated pistil dioxygenase at a distance, in the ovary, in the wild potato Solanum chacoense Bitt. Plant Mol Biol. 41: 371–386.
Li, Z. and Thomas, T.L. 1998. PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 10: 383–398.
Lohe, A.R. and Chaudhury, A. 2002. Genetic and epigenetic processes in seed development. Curr. Opin. Plant Biol. 5: 19–25.
Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. and Richmond, T.J. 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389: 251–260.
Lusser, A., Kolle, D. and Loidl, P. (2001). Histone acetylation: lessons from the plant kingdom. Trends Plant Sci. 6: 59–65.
Lusser, A., Brosch, G., Loidl, A., Haas, H. and Loidl, P. 1997. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science 277: 88–91.
Matton, D.P., Maes, O., Laublin, G., Xike, Q., Bertrand, C., Morse, D. and Cappadocia, M. 1997. Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9: 1757–1766.
Murfett, J., Wang, X.J., Hagen, G. and Guilfoyle, T.J. 2001. Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13: 1047–1061.
Ogas, J., Kaufmann, S., Henderson, J. and Somerville, C. 1999. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 13839–13844.
Pazin, M.J. and Kadonaga, J.T. 1997. What's up and down with histone deacetylation and transcription? Cell 89: 325–328.
Reichheld, J.P., Gigot, C. and Chaubet-Gigot, N. 1998. Multilevel regulation of histone gene expression during the cell cycle in tobacco cells. Nucl. Acids Res 26: 3255–3262.
Reiter, R.S., Young, R.M. and Scolnik, P.A. 1992. Genetic linkage of the Arabidopsis genome: methods for mapping with recombinant inbreds and Random Amplified Polymorphic DNAs (RAPDs). In: Methods in Arabidopsis Research, C. Koncz, N.-H. Chua and J. Schell, eds, World Scientific Publishing Co., Singapore, pp. 170–190.
Reyes, J.C., Hennig, L. and Gruissem, W. 2002. Chromatinremodeling and memory factors. New regulators of plant development. Plant Physiol. 130: 1090–1101.
Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Strahl, B.D. and Allis, C.D. 2000. The language of covalent histone modifications. Nature 403: 41–45.
Sudarsanam, P. and Winston, F. 2000. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 16: 345–351.
Sudarsanam, P., Iyer, V.R., Brown, P.O. and Winston, F. 2000. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97: 3364–3369.
Swofford, D.L. 1998. PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer, Sunderland, MA.
Tian, L. and Chen, Z.J. 2001. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc. Natl. Acad. Sci. USA 98: 200–205.
Turner, B.M. 2000. Histone acetylation and an epigenetic code. Bioessays 22: 836–845.
Utley, R.T. and Côte, J. 2003. The MYST family of histone acetyltransferases. Curr. Top. Microbiol. Immunol. 274: 203–236.
Wagner, D. 2003. Chromatin regulation of plant development. Curr. Opin. Plant Biol. 6: 20–28.
Wagner, D. and Meyerowitz, E.M. 2002. SPLAYED, a novel SWI/SNF ATPase homolog, controls reproductive development in Arabidopsis. Curr. Biol. 12: 85–94.
Wang, L., Ding, L., Jones, C.A. and Jones, R.S. 2002. Drosophila Enhancer of zeste protein interacts with dSAP18. Gene 285: 119–125.
Wu, K., Malik, K., Tian, L., Brown, D. and Miki, B. 2000a. Functional analysis of a RPD3 histone deacetylase homologue in Arabidopsis thaliana. Plant Mol. Biol. 44: 167–176.
Wu, K., Tian, L., Malik, K., Brown, D. and Miki, B. 2000b. Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana. Plant J. 22: 19–27.
Zhu, W., Foehr, M., Jaynes, J.B. and Hanes, S.D. 2001. Drosophila SAP18, a member of the Sin3/Rpd3 histone deacetylase complex, interacts with Bicoid and inhibits its activity. Dev. Genes Evol. 211: 109–117.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lagacé, M., Chantha, SC., Major, G. et al. Fertilization induces strong accumulation of a histone deacetylase (HD2) and of other chromatin-remodeling proteins in restricted areas of the ovules. Plant Mol Biol 53, 759–769 (2003). https://doi.org/10.1023/B:PLAN.0000023665.36676.89
Issue Date:
DOI: https://doi.org/10.1023/B:PLAN.0000023665.36676.89