Abstract
One of the great unanswered questions in the biology of both plants and animals is “How do simple groups of embryonic cells develop into complex and highly structured organisms, or parts of organisms?” The answers are only beginning to be known; the processes involved include establishment of positional information, and its interpretation into patterns of cell division and cellular differentiation. One remarkable and attractive example of the formation of a complex structure from a simple group of cells is the development of a flower, with its characteristic types, numbers and patterns of floral organs. Because of the ease with which plants (especially the plantArabidopsis thaliana) can be manipulated in the laboratory, flowers provide a unique opportunity to learn some of the fundamental rules of development.
Similar content being viewed by others
References
Aida, M., Ishida, T., Fukaki, H., Fujisawa, H. andTasaka, M. 1997. Genes involved in organ separation in Arabidopsis: An analysis of thecup-shaped cotyledon mutant. Plant Cell9: 841–857.
Angenent, G.C., Franken, J., Busscher, M., Colombo, L. andvan Tunen, A.J. 1993. Petal and stamen formation in petunia is regulated by the homeotic genefbp1. Plant J.4: 101–112.
Aoyama, T. andChua, N.-H. 1997. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J.11: 605–612.
Bateson, W. 1894. Materials for the Study of Variation. Cambridge, Cambridge University Press.
Bowman, J.L., Alvarez, J., Weigel, D., Meyerowitz, E.M. andSmyth, D.R. 1993. Control of flower development inArabidopsis thaliana byAPETALA1 and interacting genes. Development119: 721–743.
Bowman, J.L., Smyth, D.R. andMeyerowitz, E.M. 1989. Genes directing flower development inArabidopsis. Plant Cell1: 37–52.
Bowman, J.L., Smyth, D.R. andMeyerowitz, E.M. 1991. Genetic interactions among floral homeotic genes ofArabidopsis. Development112: 1–20.
Bowman, J.L., Yanofsky, M.F. and Meyerowitz, E.M. 1988.Arabidopsis thaliana: a review.In B.J. Miflin, ed., Oxford Surveys of Plant Molecular and Cell Biology, vol. 5, Oxford, pp. 57–87.
Bradley, D., Carpenter, R., Sommer, H., Hartley, N. andCoen, E. 1993. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at theplena locus of Antirrhinum. Cell72: 85–95.
Coen, E.S. 1991. The role of homeotic genes in flower development and evolution. Annu. Rev. Plant Physiol. Plant Mol. Biol.42: 241–279.
Coen, E.S. andMeyerowitz, E.M. 1991. The war of the whorls: genetic interactions controlling flower development. Nature353: 31–37.
Dalman, F.C., Scherrer, L.C., Taylor, L.P., Akil, H. andPratt, W.B. 1991. Localisation of the 90 kDa heat shock protein-binding site within the hormone-binding domain of the glucocorticoid receptor by peptide competition. J. Biol. Chem.266: 3482–3490.
Davies, B., Dirosa, A., Eneva, T., Saedler, H. andSommer, H. 1996. Alteration of tobacco floral organ identity by expression of combinations ofAntirrhinum MADS-Box genes. Plant J.10: 663–677.
Drews, G.N., Bowman, J.L. andMeyerowitz, E.M. 1991. Negative regulation of the Arabidopsis homeotic geneAGAMOUS by theAPETALA2 product. Cell65: 991–1002.
Goodrich, J., Puangsomlee, P., Long, D., Martin, M., Meyerowitz, E.M. andCoupland, G. 1997.CURLY LEAF: A Polycomb group gene that regulates homeotic gene expression inArabidopsis. Nature386: 44–51.
Goto, K. andMeyerowitz, E.M. 1994. Function and regulation of theArabidopsis floral homeotic genePISTILLATA. Genes Devel.8: 1548–1560.
Gustafson-Brown, C., Savidge, B. andYanofsky, M.F. 1994. Regulation of the Arabidopsis floral homeotic geneAPETALA1. Cell76: 131–143.
Huala, E. andSussex, I.M. 1992.LEAFY interacts with floral homeotic genes to regulateArabidopsis floral development. Plant Cell4: 901–913.
Jack, T., Brockman, L.L. andMeyerowitz, E.M. 1992. The homeotic geneAPETALA3 ofArabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell68: 683–697.
Jack, T., Sieburth, L. andMeyerowitz, E.M. 1997. Targeted misexpresion ofAGAMOUS in whorl 2 ofArabidopsis flowers. Plant J.11: 825–839.
Jofuku, K.D., den Boer, B.G.W., Van Montagu, M. andOkamuro, J.K. 1994. Control of Arabidopsis flower and seed development by the homeotic geneAPETALA2. Plant Cell6: 1211–1225.
Krizek, B.A. andMeyerowitz, E.M. 1996a. TheArabidopsis homeotic genesAPETALA3 andPISTILLATA are sufficient to provide the B class organ identity function. Development122: 11–22.
Krizek, B.A. andMeyerowitz, E.M. 1996b. Mapping the protein regions responsible for the functional specificities of theArabidopsis MADS domain organ-identity proteins. Proc. Natl. Acad. Sci. USA93: 4063–4070.
Lee, I., Wolfe, D.S., Nilsson, O. andWeigel, D. 1997.A LEAFY coregulator encoded byUNUSUAL FLORAL ORGANS. Curr. Biol.7: 95–104.
Levin, J.Z. andMeyerowitz, E.M. 1995.UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell7: 529–548.
Liang, P. andPardee, A.B. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science257: 967–971.
Liu, Z. andMeyerowitz, E.M. 1995.LEUNIG regulatesAGAMOUS expression inArabidopsis flowers. Development121: 975–991.
Lloyd, A.M., Schena, M., Walbot, V. andDavis, R. 1994. Epidermal cell fate determination inArabidopsis: Patterns defined by a steroid-inducible regulator. Science266: 436–439.
Mandel, M.A., Bowman, J.L., Kempin, S.A., Ma, H., Meyerowitz, E.M. andYanofsky, M.F. 1992b. Manipulation of flower structure in transgenic tobacco. Cell71: 133–143.
Mandel, M.A., Gustafson-Brown, C., Savidge, B. andYanofsky, M.F. 1992a. Molecular characterization of theArabidopsis floral homeotic geneAPETALA1. Nature360: 273–277.
Mandel, M.A. andYanofsky, M.F. 1995. A gene triggering flower formation in Arabidopsis. Nature377: 522–524.
Meyerowitz, E.M. 1987.Arabidopsis thaliana. Ann. Rev. Genet.21: 93–111.
Meyerowitz, E.M., Bowman, J.L., Brockman, L.L., Drews, G.N., Jack, T., Sieburth, L.E. andWeigel, D. 1991. A genetic and molecular model for flower development inArabidopsis thaliana. Development112: suppl. 1, 157–168.
Meyerowitz, E.M. andPruitt, R.E. 1985.Arabidopsis thaliana and plant molecular genetics. Science229: 1214–1218. [Reprinted in Biotechnology: The Renewable Frontier, ed. D.E. Koshland, Jr., AAAS, pp. 311–320, 1986].
Meyerowitz, E.M., Smyth, D.R. andBowman, J.L. 1989. Abnormal flowers and pattern formation in floral development. Development106: 209–217.
Mizukami, Y. andMa, H. 1992. Ectopic expression of the floral homeotic geneAGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell71: 119–131.
Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M.F., andLifshitz, E. 1994. Isolation of the tomatoAGAMOUS geneTAG1 and analysis of its homeotic role in transgenic plants. Plant Cell6: 163–173.
Riechmann, J.-L., Krizek, B.A. andMeyerowitz, E.M. 1996. Dimerization specificity ofArabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Proc. Natl. Acad. Sci. USA93: 4793–4798.
Riechmann, J.L. andMeyerowitz, E.M. 1997. MADS domain proteins in plant development. Biol. Chem.378: 1079–1101.
Sablowski, R.W.M. andMeyerowitz, E.M. 1998. A homologue ofNO APICAL MERISTEM is an immediate target of the floral homeotic genesAPETALA3/PISTILLATA. Cell92: 93–103.
Schultz, E.A. andHaughn, G.W. 1991.LEAFY, a homeotic gene that regulates inflorescence development inArabidopsis. Plant Cell3: 771–781.
Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H. andSommer, H. 1990. Genetic control of flower development: homeotic genes inAntirrhinum majus. Science250: 931–936.
Simon, R., Igeño, M.I. andCoupland, G. 1996. Activation of floral meristem identity genes inArabidopsis. Nature384: 59–62.
Smyth, D.R., Bowman, J.L. andMeyerowitz, E.M. 1990. Early flower development inArabidopsis. Plant Cell2: 755–767.
Sommer, H., Beltrán, J.P., Huijser, P., Pape, H., Lönnig, W.E., Saedler, H. andSchwarz-Sommer, Z. 1990.Deficiens, a homeotic gene involved in the control of flower morphogenesis inAntirrhinum majus: the protein shows homology to transcription factors. EMBO J.9: 605–613.
Souer, E., van Houwelingen, A., Kloos D., Mol, J. andKoes, R. 1996. TheNo Apical Meristem gene of Petunia is required for pattern formation in embryos and flowers and expressed at meristem and primordia boundaries. Cell85: 159–170.
Tröbner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lönnig, W.-E., Saedler, H., Sommer, H. andSchwarz-Sommer, Z. 1992.GLOBOSA: a homeotic gene which interacts withDEFICIENS in the control ofAntirrhinum floral organogenesis. EMBO J.11: 4693–4704.
Weigel, D., Alvarez, J., Smyth, D.R., Yanofsky, M.F. andMeyerowitz, E.M. 1992.LEAFY controls floral meristem identity inArabidopsis. Cell69: 843–859.
Weigel, D. andMeyerowitz, E.M. 1993. Activation of floral homeotic genes inArabidopsis. Science261: 1723–1726.
Weigel, D. andMeyerowitz, E.M. 1994. The ABCs of floral homeotic genes. Cell78: 203–209.
Wilkinson, M.G. andHaughn, G.W. 1995.UNUSUAL FLORAL ORGANS controls meristem identity and organ primordia fate inArabidopsis. Plant Cell7: 1485–1499.
Wolpert, L., Beddington, R., Brockes, J., Jessell, T., Lawrence, P. and Meyerowitz, E.M. 1998. Principles of Development. Current Biology, London.
Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A. andMeyerowitz, E.M. 1990. The protein encoded by theArabidopsis homeotic geneagamous resembles transcription factors. Nature346: 35–39.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Meyerowitz, E.M. Genetic and molecular mechanisms of pattern formation inArabidopsis flower development. J. Plant Res. 111, 233–242 (1998). https://doi.org/10.1007/BF02512176
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02512176