THE PLANT CELL, Vol 7, Issue 11 1859-1868, Copyright © 1995 by American Society of Plant Biologists

RESEARCH ARTICLES

The Petunia MADS Box Gene FBP11 Determines Ovule Identity

L. Colombo, J. Franken, E. Koetje, J. van Went, HJM. Dons, G. C. Angenent and A. J. van Tunen
Department of Developmental Biology, DLO-Centre for Plant Breeding and Reproduction Research, P.O. Box 16, 6700 AA Wageningen, The Netherlands

In contrast to the wealth of information relating to genes regulating floral meristem and floral organ identity, only limited data are available concerning genes that are involved in determining and regulating the identity and development of an ovule. We have recently isolated the floral binding protein 11 (FBP11) MADS box gene from petunia and found that it is expressed exclusively in ovule primordia and subsequently in the ovules, suggesting a role for this gene in ovule formation. To test this hypothesis, we constructed a recombinant gene in which the full-size FBP11 cDNA was placed under the control of a strong cauliflower mosaic virus 35S promoter. Transgenic petunia plants expressing this chimeric gene have ovulelike structures on the adaxial side of the sepals and the abaxial side of the petals. Detailed morphological studies showed that these ovulelike structures are true ovules. RNA gel blot analysis was performed to investigate ectopic FBP11 expression in relation to the expression of the closely related FBP7 gene and the putative petunia class C-type homeotic genes FBP6 and pMADS3. Our results indicate that FBP11 represents an ovule identity gene. A new model describing the mode of action of FBP11 as an additional class D MADS box gene is presented.

This article has been cited by other articles:

				C. H. Leseberg, C. L. Eissler, X. Wang, M. A. Johns, M. R. Duvall, and L. Mao Interaction study of MADS-domain proteins in tomato J. Exp. Bot., May 17, 2008; (2008) ern094v1. [Abstract] [Full Text] [PDF]

				T. R. Meagher Linking the Evolution of Gender Variation to Floral Development Ann. Bot., August 1, 2007; 100(2): 165 - 176. [Abstract] [Full Text] [PDF]

				D. E. Soltis, A. S. Chanderbali, S. Kim, M. Buzgo, and P. S. Soltis The ABC Model and its Applicability to Basal Angiosperms Ann. Bot., August 1, 2007; 100(2): 155 - 163. [Abstract] [Full Text] [PDF]

				H. Adam, S. Jouannic, Y. Orieux, F. Morcillo, F. Richaud, Y. Duval, and J. W. Tregear Functional characterization of MADS box genes involved in the determination of oil palm flower structure J. Exp. Bot., April 1, 2007; 58(6): 1245 - 1259. [Abstract] [Full Text] [PDF]

				C. Damerval, M. L. Guilloux, M. Jager, and C. Charon Diversity and Evolution of CYCLOIDEA-Like TCP Genes in Relation to Flower Development in Papaveraceae Plant Physiology, February 1, 2007; 143(2): 759 - 772. [Abstract] [Full Text] [PDF]

				M. Gray-Mitsumune, M. O'Brien, C. Bertrand, F. Tebbji, A. Nantel, and D. P. Matton Loss of ovule identity induced by overexpression of the fertilization-related kinase 2 (ScFRK2), a MAPKKK from Solanum chacoense J. Exp. Bot., December 1, 2006; 57(15): 4171 - 4187. [Abstract] [Full Text] [PDF]

				T. H. Teeri, A. Uimari, M. Kotilainen, R. Laitinen, H. Help, P. Elomaa, and V. A. Albert Reproductive meristem fates in Gerbera J. Exp. Bot., October 1, 2006; 57(13): 3445 - 3455. [Abstract] [Full Text] [PDF]

				C. P. Scutt, M. Vinauger-Douard, C. Fourquin, C. Finet, and C. Dumas An evolutionary perspective on the regulation of carpel development J. Exp. Bot., July 1, 2006; 57(10): 2143 - 2152. [Abstract] [Full Text] [PDF]

				S. Ferrario, A. V. Shchennikova, J. Franken, R. G.H. Immink, and G. C. Angenent Control of Floral Meristem Determinacy in Petunia by MADS-Box Transcription Factors Plant Physiology, March 1, 2006; 140(3): 890 - 898. [Abstract] [Full Text] [PDF]

				I. A. N. Tonaco, J. W. Borst, S. C. de Vries, G. C. Angenent, and R. G. H. Immink In vivo imaging of MADS-box transcription factor interactions J. Exp. Bot., January 1, 2006; 57(1): 33 - 42. [Abstract] [Full Text] [PDF]

				S. Drea, D. J. Leader, B. C. Arnold, P. Shaw, L. Dolan, and J. H. Doonan Systematic Spatial Analysis of Gene Expression during Wheat Caryopsis Development PLANT CELL, August 1, 2005; 17(8): 2172 - 2185. [Abstract] [Full Text] [PDF]

				L. M. Zahn, J. Leebens-Mack, C. W. dePamphilis, H. Ma, and G. Theissen To B or Not to B a Flower: The Role of DEFICIENS and GLOBOSA Orthologs in the Evolution of the Angiosperms J. Hered., May 1, 2005; 96(3): 225 - 240. [Abstract] [Full Text] [PDF]

				J.-I. Itoh, K.-I. Nonomura, K. Ikeda, S. Yamaki, Y. Inukai, H. Yamagishi, H. Kitano, and Y. Nagato Rice Plant Development: from Zygote to Spikelet Plant Cell Physiol., January 15, 2005; 46(1): 23 - 47. [Abstract] [Full Text] [PDF]

				C. J. Whipple, P. Ciceri, C. M. Padilla, B. A. Ambrose, S. L. Bandong, and R. J. Schmidt Conservation of B-class floral homeotic gene function between maize and Arabidopsis Development, December 15, 2004; 131(24): 6083 - 6091. [Abstract] [Full Text] [PDF]

				T. Payne, S. D. Johnson, and A. M. Koltunow KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium Development, August 1, 2004; 131(15): 3737 - 3749. [Abstract] [Full Text] [PDF]

				F. Fornara, L. Parenicova, G. Falasca, N. Pelucchi, S. Masiero, S. Ciannamea, Z. Lopez-Dee, M. M. Altamura, L. Colombo, and M. M. Kater Functional Characterization of OsMADS18, a Member of the AP1/SQUA Subfamily of MADS Box Genes Plant Physiology, August 1, 2004; 135(4): 2207 - 2219. [Abstract] [Full Text] [PDF]

				V. A. Benedito, P. B. Visser, J. M. van Tuyl, G. C. Angenent, S. C. de Vries, and F. A. Krens Ectopic expression of LLAG1, an AGAMOUS homologue from lily (Lilium longiflorum Thunb.) causes floral homeotic modifications in Arabidopsis J. Exp. Bot., June 1, 2004; 55(401): 1391 - 1399. [Abstract] [Full Text] [PDF]

				S. Ferrario, J. Busscher, J. Franken, T. Gerats, M. Vandenbussche, G. C. Angenent, and R. G.H. Immink Ectopic Expression of the Petunia MADS Box Gene UNSHAVEN Accelerates Flowering and Confers Leaf-Like Characteristics to Floral Organs in a Dominant-Negative Manner PLANT CELL, June 1, 2004; 16(6): 1490 - 1505. [Abstract] [Full Text] [PDF]

				T. Jack Molecular and Genetic Mechanisms of Floral Control PLANT CELL, June 1, 2004; 16(suppl_1): S1 - S17. [Full Text] [PDF]

				D. J. Skinner, T. A. Hill, and C. S. Gasser Regulation of Ovule Development PLANT CELL, June 1, 2004; 16(suppl_1): S32 - S45. [Full Text] [PDF]

				H. Nakagawa, S. Ferrario, G. C. Angenent, A. Kobayashi, and H. Takatsuji The Petunia Ortholog of Arabidopsis SUPERMAN Plays a Distinct Role in Floral Organ Morphogenesis PLANT CELL, April 1, 2004; 16(4): 920 - 932. [Abstract] [Full Text] [PDF]

				A. V. Shchennikova, O. A. Shulga, R. Immink, K. G. Skryabin, and G. C. Angenent Identification and Characterization of Four Chrysanthemum MADS-Box Genes, Belonging to the APETALA1/FRUITFULL and SEPALLATA3 Subfamilies Plant Physiology, April 1, 2004; 134(4): 1632 - 1641. [Abstract] [Full Text] [PDF]

				E. M. Kramer, M. A. Jaramillo, and V. S. Di Stilio Patterns of Gene Duplication and Functional Evolution During the Diversification of the AGAMOUS Subfamily of MADS Box Genes in Angiosperms Genetics, February 1, 2004; 166(2): 1011 - 1023. [Abstract] [Full Text] [PDF]

				R. Favaro, A. Pinyopich, R. Battaglia, M. Kooiker, L. Borghi, G. Ditta, M. F. Yanofsky, M. M. Kater, and L. Colombo MADS-Box Protein Complexes Control Carpel and Ovule Development in Arabidopsis PLANT CELL, November 1, 2003; 15(11): 2603 - 2611. [Abstract] [Full Text] [PDF]

				M. Vandenbussche, J. Zethof, E. Souer, R. Koes, G. B. Tornielli, M. Pezzotti, S. Ferrario, G. C. Angenent, and T. Gerats Toward the Analysis of the Petunia MADS Box Gene Family by Reverse and Forward Transposon Insertion Mutagenesis Approaches: B, C, and D Floral Organ Identity Functions Require SEPALLATA-Like MADS Box Genes in Petunia PLANT CELL, November 1, 2003; 15(11): 2680 - 2693. [Abstract] [Full Text] [PDF]

				E. W. Harding, W. Tang, K. W. Nichols, D. E. Fernandez, and S. E. Perry Expression and Maintenance of Embryogenic Potential Is Enhanced through Constitutive Expression of AGAMOUS-Like 15 Plant Physiology, October 1, 2003; 133(2): 653 - 663. [Abstract] [Full Text] [PDF]

				M. Jager, A. Hassanin, M. Manuel, H. L. Guyader, and J. Deutsch MADS-Box Genes in Ginkgo biloba and the Evolution of the AGAMOUS Family Mol. Biol. Evol., May 1, 2003; 20(5): 842 - 854. [Abstract] [Full Text] [PDF]

				N. A. Eckardt MADS Monsters: Controlling Floral Organ Identity PLANT CELL, April 1, 2003; 15(4): 803 - 805. [Full Text] [PDF]

				S. Ferrario, R. G. H. Immink, A. Shchennikova, J. Busscher-Lange, and G. C. Angenent The MADS Box Gene FBP2 Is Required for SEPALLATA Function in Petunia PLANT CELL, April 1, 2003; 15(4): 914 - 925. [Abstract] [Full Text] [PDF]

				T.-Y. Tzeng, H.-Y. Chen, and C.-H. Yang Ectopic Expression of Carpel-Specific MADS Box Genes from Lily and Lisianthus Causes Similar Homeotic Conversion of Sepal and Petal in Arabidopsis Plant Physiology, December 1, 2002; 130(4): 1827 - 1836. [Abstract] [Full Text] [PDF]

				R. G. H. Immink, T. W. J. Gadella Jr., S. Ferrario, M. Busscher, and G. C. Angenent Analysis of MADS box protein-protein interactions in living plant cells PNAS, February 19, 2002; 99(4): 2416 - 2421. [Abstract] [Full Text] [PDF]

				S. Heuer, S. Hansen, J. Bantin, R. Brettschneider, E. Kranz, H. Lorz, and T. Dresselhaus 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 Physiology, September 1, 2001; 127(1): 33 - 45. [Abstract] [Full Text] [PDF]

				M. W. Frohlich MADS about Gnetales PNAS, August 3, 1999; 96(16): 8811 - 8813. [Full Text] [PDF]

				M. M. Kater, L. Colombo, J. Franken, M. Busscher, S. Masiero, M. M. Van Lookeren Campagne, and G. C. Angenent Multiple AGAMOUS Homologs from Cucumber and Petunia Differ in Their Ability to Induce Reproductive Organ Fate PLANT CELL, February 1, 1998; 10(2): 171 - 182. [Abstract] [Full Text] [PDF]

				K Schneitz, S. Baker, C. Gasser, and A Redweik Pattern formation and growth during floral organogenesis: HUELLENLOS and AINTEGUMENTA are required for the formation of the proximal region of the ovule primordium in Arabidopsis thaliana Development, January 7, 1998; 125(14): 2555 - 2563. [Abstract] [PDF]

				T. Munster, J. Pahnke, A. Di Rosa, J. T. Kim, W. Martin, H. Saedler, and G. Theissen Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants PNAS, March 18, 1997; 94(6): 2415 - 2420. [Abstract] [Full Text] [PDF]

				K Schneitz, M Hulskamp, S. Kopczak, and R. Pruitt Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana Development, January 4, 1997; 124(7): 1367 - 1376. [Abstract] [PDF]