Abstract
Cell fate is determined when the commitment of cells to a particular fate is autonomously maintained, irrespective of their environment. In Drosophila, fate determination is maintained through the action of the Polycomb-group and trithorax-group genes, which are required so that states of homeotic gene activity are inherited through cell division. It is shown here that the CURLY LEAF gene of Arabidopsis is necessary for stable repression of a floral homeotic gene and encodes a protein with homology to the product of the Polycomb-group gene Enhancer of zeste. We suggest that Polycomb-group genes have a similar role in fate determination in plants and animals.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Coen, E. S. & Meyerowitz, E. M. The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37 (1991).
Lewis, E. B. A gene complex controlling segmentation in Drosophila. Nature 276, 565–570 (1978).
Bowman, J. L, Smyth, D. R. & Meyerowitz, E. M. Genes directing flower development in Arabidopsis. Plant Cell 1, 37–52 (1989).
Carpenter, R. & Coen, E. S. Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum jamus. Genes Dev. 4, 1483–1493 (1990).
Struhl, G. Genes controlling segmentation specification in the Drosophila thorax. Proc. Natl Acad. Sci. USA 79, 7380–7384 (1982).
Ingham, P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature 335, 25–33 (1988).
Weigel, D. & Meyerowitz, E. M. The ABCs of floral homeotic genes. Cell 78, 203–209 (1994).
Heemskerk, J., DiNardo, S., Kostriken, R. & O'Farrell, P. H. Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 352, 404–410 (1991).
Simcox, A. A. & Sang, J. H. When does determination occur in Drosophila embryos? Dev. Biol. 97, 212–221 (1983).
Lawrence, P. A. & Morata, G. in Insect Development (ed. Lawrence, P. A.) 132–148 (Blackwell, Oxford, 1976).
Simon, J. Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr. Opin. Cell Biol. 7, 376–385 (1995).
Kennison, J. A. Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet. 9, 75–79 (1993).
Struhl, G. & Akam, M. Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 4, 3259–3264 (1985).
Jones, R. S. & Gelbart, W. M. Genetic analysis of the Enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 126, 185–199 (1990).
Breene, T. R. & Harte, P. J. trithorax regulates multiple homeotic genes in the bithorax and Antennapedia complexes and exerts different tissue-specific, parasegment-specific and promoter-specific effects on each. Development 117, 119–134 (1993).
Grindhart, J. G. J. & Kaufman, T. C. Identification of polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene sex combs reduced. Genetics 139, 797–814 (1995).
Muller, J. Transcriptional silencing by the Polycomb protein in Drosophila embryos. EMBO J. 14, 1209–1220 (1995).
Paro, R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 6, 416–421 (1990).
Weigel, D. & Doerner, P. Cell–cell interactions—taking cues for the neighbors. Curr. Biol. 6, 10–12 (1996).
Irish, E. E. & Nelson, T. M. Identification of multiple stages in the conversion of maize meristems from vegetative to floral development. Development 112, 891–898 (1991).
Bradley, D., Vincent, C., Carpenter, R. & Coen, E. Pathways for inflorescence and floral induction in Antirrhinum. Development 122, 1535–1544 (1996).
Yanofsky, M. F. et al. The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346, 35–39 (1990).
Drews, G. N., Bowman, J. L. & Meyerowitz, E. M. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991–1002 (1991).
Long, D. et al. The maize transposable element system Ac/Ds as a mutagen in Arabidopsis: Identification of an albino mutation induced by Ds insertion. Proc. Natl Acad. Sci. USA 90, 10370–10374 (1993).
Mizukami, Y. & Ma, H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119–131 (1992).
Jack, T., Fox, G. L. & Meyerowitz, E. M. Arabidopsis homeotic gene APETALA3 ectopic expression—transcriptional and posttranscriptional regulation determined floral organ identity. Cell 76, 703–716 (1994).
Liu, Z. & Meyerowitz, E. M. LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975–991 (1995).
Sutton, W. D., Gerlach, W. L., Schwartz, D. & Peacock, W. J. Molecular analysis of ds controlling element mutations at the ADH1 locus of maize. Science 223, 1265–1268 (1984).
Lüttke, H. A. et al. Selection of AUG initiation codons differs in plants and animals. EMBO J. 6, 43–48 (1987).
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman Basic local alignment search tool. J. Mol. Biol. 215 403–410 (1990).
Jones, R. S. & Gelbart, W. M. The Drosophila Polycomb-group gene Enhancer of zeste contains region with a sequence similarity to trithorax. Mol. Cell. Biol. 13, 6357–6366 (1993).
Tschiersch, B. et al. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var) 3–9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 13, 3822–3831 (1994).
Carrington, E. A. & Jones, R. S. The Drosophila Enhancer of zeste gene encodes a chromosomal protein: examination of wild-type and mutant protein distribution. Development 122, 4073–4083 (1996).
Paro, R. & Hogness, D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc. Natl Acad. Sci. USA 88, 263–267 (1991).
Rastelli, L., Chan, C. S. & Pirotta, V. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 12, 1513–1522 (1993).
Tsukiyama, T., Becker, P. B. & Wu, C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367, 525–532 (1994).
Côté, J., Quinn, J., Workman, J. L. & Peterson, C. L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265, 53–60 (1994).
Finnegan, E. J., Peacock, W. J. & Dennis, E. S. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl Acad. Sci. USA 93, 8449–8454 (1996).
Ronemus, M. J., Galbiati, M., Ticknor, C., Chen, J. C. & Dellaporta, S. L. Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273, 654–657 (1996).
Jofuku, D., van den Boer, B., Van Montagu, M. & Okamuro, J. Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211–1225 (1994).
van der Lugt, N. M. T. et al. Posterior transformation, neurological abnormalities, and severe hematapoietic defects in mice with a targeted deletion of the bmi-1 protooncogene. Genes Dev. 8, 757–769 (1994).
Akaseka, T. et al. A role for mel-18, a Polycomb group-related vertebrate gene, during the anteroposterior specification of the axial skeleton. Development 122, 1513–1522 (1996).
Krumlauf, R. Hox genes in vertebrate development. Cell 78, 191–201 (1994).
van den Berg, C., Willemsen, V., Hage, W., Weisbeek, P. & Scheres, B. Determination of cell fate in the Arabidopsis root meristem by directional signalling. Nature 378, 62–65 (1995).
Tröbner, W. et al. Globosa—A homeotic gene which interacts with deficiens in the control of Antirrhinum floral organogenesis. EMBO J. 11, 4693–4704 (1992).
Putterill, J., Robson, F., Lee, K., Simon, R. & Coupland, G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847–857 (1995).
Coen, E. S., Carpenter, R. & Martin, C. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell 47, 285–296 (1986).
Jack, T., Brockman, L. L. & Meyerowitz, E. M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68, 683–697 (1992).
Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F. & Meyerowitz, E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843–859 (1992).
Coen, E. S. et al. Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63, 1311–1322 (1990).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Goodrich, J., Puangsomlee, P., Martin, M. et al. A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44–51 (1997). https://doi.org/10.1038/386044a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/386044a0
This article is cited by
-
Analysis of polycomb repressive complex 2 (PRC2) subunits in Picea abies with a focus on embryo development
BMC Plant Biology (2023)
-
An optimized pipeline for live imaging whole Arabidopsis leaves at cellular resolution
Plant Methods (2023)
-
Genome-wide analysis of SET domain genes and the function of GhSDG51 during salt stress in upland cotton (Gossypium hirsutum L.)
BMC Plant Biology (2023)
-
An Overview of Molecular Basis and Genetic Modification of Floral Organs Genes: Impact of Next-Generation Sequencing
Molecular Biotechnology (2023)
-
Induction of leaf curling in cassava plants by the cassava mealybug Phenacoccus manihoti (Hemiptera: Pseudococcidae)
Applied Entomology and Zoology (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.