[en] The identity and developmental pattern of the four organ types constituting the flower is governed by three developmental functions, A, B and C, which are defined by homeotic genes and established in two adjacent whorls. In this report we morphologically and genetically characterise mutants of two genes, STYLOSA (STY) and FISTULATA (FIS) which control floral homeotic meristem- and organ-identity genes and developmental events in all floral whorls. The morphology of the reproductive organs in the first and second whorls of sty fis double mutant flowers indicate that the two genes are part of the mechanism to prevent ectopic expression of the C-function in the perianth of wild-type flowers. This is verified by the detection of the expansion of the expression domain of the class C gene PLENA (PLE) towards the perianth. Interestingly, in the second whorl of sty and fis mutants, spatial differences in stamenoid features and in the pattern of ectopic expression of the PLE gene were observed. This suggests that, with respect to the negative control of PLE, petals are composed of two regions, a lateral and a central one. Mutation in ple is epistatic to most of the sty/fis-related homeotic defects. PLE, however, is not the primary target of STY/FIS control, because dramatic reduction of expression of FIMBRIATA, meristem identity genes (FLORICAULA and SQUAMOSA) and of class B organ identity genes (GLOBOSA) occur before changes in the PLE expression pattern. We propose that STY/FIS are hierarchically high-ranking genes that control cadastral component(s) of the A-function. SQUAMOSA as a potential target of this control is discussed. Retarded growth of second whorl organs, subdivision of third whorl primordia and the failure to initiate them in sty/fis mutants may be mediated by the FIMBRIATA gene.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Motte, Patrick ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Saedler, H.
Schwarz-Sommer, Z.
Language :
English
Title :
STYLOSA and FISTULATA: regulatory components of the homeotic control of Antirrhinum floral organogenesis.
Bowman, J. L., Alvarez, J., Weigel, D., Meyerowitz, E. and Smyth, D. R. (1993). Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721-743.
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.
Carpenter, R. and Coen, E. S. (1990). Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 4, 1483-1493.
Carpenter, R., Copsey, L., Vincent, C., Doyle, S., Magrath, R. and Coen, E. (1995). Control of flower development and phyllotaxy by meristem identity genes in Antirrhinum. Plant Cell 7, 2001-2011.
Coen, E. S. and Meyerowitz, E. M. (1991). The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37.
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.
Davies, B. and Schwarz-Sommer, Z. (1994). Control of floral organ identity by homeotic MADS-box transcription factors. Results and Problems in Cell Differentiation. In Plant Promoters and Transcription Factors 20, 235-258.
Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E. M. and Coupland, G. (1997). A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44-51.
Gustafson-Brown, C., Savidge, B. and Yanofsky, M. F. (1994). Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76, 131-143.
Hantke, S. S., Carpenter, R. and Coen, E. S. (1995). Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems. Development 121, 27-35.
Haughn, G. W., Schultz, E. A. and Martinez-Zapater, J. M. (1995). The regulation of flowering in Arabidopsis thaliana - meristems, morphogenesis, and mutants. Can. J. Bot. 73, 959-981.
Haughn, G. W. and Somerville, C. R. (1988). Genetic control of morphogenesis in Arabidopsis. Dev. Genet. 9, 73-89.
Huijser, P., Klein, J., Lönnig, W. -E., Meijer, H., Saedler, H. and Sommer, H. (1992). Bractomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J. 11, 1239-1249.
Ingram, C. G., Doyle, S. D., Carpenter, R., Schultz, E. A., Simon, R. and Coen, E. S. (1997). Dual role for fimbriata in regulating floral homeotic genes and cell division in Antirrhinum. EMBO J. (in press).
Jack, T., Sieburth, L. and Meyerowitz, M. (1997). Targeted misexpression of AGAMOUS in whorl 2 of Arabidopsis flowers. Plant J. 11, 825-839.
Jofuku, K. D., den Boer, B. G. W., Van Montagu, M. and Okamuro, J. K. (1994). Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6, 1211-1225.
Liu, Z. and Meyerowitz, E. M. (1995). LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975-991.
Lönnig, W. E. and Saedler, H. (1994). The homeotic Macho mutant of Antirrhinum majus reverts to wild-type or mutates to the homeotic plena phenotype. Mol. Gen. Genet. 245, 636-643.
Mandel, M. A., Gustafson-Brown, C., Savidge, B. and Yanofsky, M. F. (1992). Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273-277.
Okamuro, J. K., den Boer, B. G. W. and Jofuku, K. D. (1993). Regulation of Arabidopsis flower development. Plant Cell 5, 1183-1193.
Okamuro, J. K., Szeto, W., Lotys-Prass, C. and Jofuku, K. D. (1997). Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1. Plant Cell 9, 37-47.
Perbal, M. -C., Haughn, G., Saedler, H. and Schwarz-Sommer, Z. (1996). Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122, 3433-3441.
Samach, A., Kohalmi, S. E., Motte, P., Datla, R. and Haughn, G. W. (1997). Divergence of function and regulation of class B floral organ identity genes. Plant Cell 9, 559-570.
Scanlon, M. J., Scheeberger, R. G. and Freeling, M. (1996). The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 122, 1683-1691.
Schultz, E. A. and Haughn, G. W. (1993). Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development 119, 745-765.
Schwarz-Sommer, Z., Hue, I., Huijser, P., Flor, P. J., Hansen, R., Tetens, F., Lönnig, W. -E., Saedler, H. and Sommer, H. (1992). Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 11, 251-263.
Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H. and Sommer, H. (1990). Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250, 931-936.
Simon, R., Carpenter, R., Doyle, S. and Coen, E. (1994). Fimbriata controls flower development by mediating between meristem and organ identity genes. Cell 78, 99-107.
Sommer, H., Beltran, J. P., Huijser, P., Pape, H., Lönnig, W. E., Saedler, H. and Schwarz-Sommer, Z. (1990). Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 9, 605-613.
Stubbe, H. (1974). Neue Mutanten von Antirrhinum majus L. Kulturpflanze. XXII, 189-213.
Tröbner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lönnig, W. -E., Saedler, H., Sommer, H. and Schwarz-Sommer, Z. (1992). GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J. 11, 4693-4704.
Tsuchimoto, S., van der Krol, A. R. and Chua, N. H. (1993). Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell 5, 843-853.
Weigel, D. and Meyerowitz, E. M. (1994). The ABCs of floral homeotic genes. Cell 78, 203-209.
Yanofsky, M. F., Ma, H., Bowman, J. L., Drews, G. N., Feldmann, K. A. and Meyerowitz, E. M. (1990). The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35-39.
Zachgo, S., de Andrade Silva, E., Motte, P., Tröbner, W., Saedler, H. and Schwarz-Sommer, Z. (1995). Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. Development 121, 2861-2875.
