Patterns of Gene Duplication and Functional Evolution During the Diversification of the AGAMOUS Subfamily of MADS Box Genes in Angiosperms

Corresponding author: Elena M. Kramer, Harvard University, 16 Divinity Ave., Cambridge, MA 02138., ekramer{at}oeb.harvard.edu (E-mail)

Communicating editor: D. WEIGEL

Members of the AGAMOUS (AG) subfamily of MIKC-type MADS-box genes appear to control the development of reproductive organs in both gymnosperms and angiosperms. To understand the evolution of this subfamily in the flowering plants, we have identified 26 new AG-like genes from 15 diverse angiosperm species. Phylogenetic analyses of these genes within a large data set of AG-like sequences show that ancient gene duplications were critical in shaping the evolution of the subfamily. Before the radiation of extant angiosperms, one event produced the ovule-specific D lineage and the well-characterized C lineage, whose members typically promote stamen and carpel identity as well as floral meristem determinacy. Subsequent duplications in the C lineage resulted in independent instances of paralog subfunctionalization and maintained functional redundancy. Most notably, the functional homologs AG from Arabidopsis and PLENA (PLE) from Antirrhinum are shown to be representatives of separate paralogous lineages rather than simple genetic orthologs. The multiple subfunctionalization events that have occurred in this subfamily highlight the potential for gene duplication to lead to dissociation among genetic modules, thereby allowing an increase in morphological diversity.

This article has been cited by other articles:

				D. E. Soltis, C. D. Bell, S. Kim, and P. S. Soltis Origin and Early Evolution of Angiosperms Ann. N.Y. Acad. Sci., June 1, 2008; 1133(1): 3 - 25. [Abstract] [Full Text] [PDF]

				R. Tuberosa, S. Salvi, S. Giuliani, M. C. Sanguineti, M. Bellotti, S. Conti, and P. Landi Genome-wide Approaches to Investigate and Improve Maize Response to Drought Crop Sci., December 18, 2007; 47(Supplement_3): S-120 - S-141. [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]

				T. Hernandez-Hernandez, L. P. Martinez-Castilla, and E. R. Alvarez-Buylla Functional Diversification of B MADS-Box Homeotic Regulators of Flower Development: Adaptive Evolution in Protein-Protein Interaction Domains after Major Gene Duplication Events Mol. Biol. Evol., February 1, 2007; 24(2): 465 - 481. [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]

				L. C. Hileman, J. F. Sundstrom, A. Litt, M. Chen, T. Shumba, and V. F. Irish Molecular and Phylogenetic Analyses of the MADS-Box Gene Family in Tomato Mol. Biol. Evol., November 1, 2006; 23(11): 2245 - 2258. [Abstract] [Full Text] [PDF]

				R. M. Bateman, J. Hilton, and P. J. Rudall Morphological and molecular phylogenetic context of the angiosperms: contrasting the 'top-down' and 'bottom-up' approaches used to infer the likely characteristics of the first flowers J. Exp. Bot., October 1, 2006; 57(13): 3471 - 3503. [Abstract] [Full Text] [PDF]

				E. R. Alvarez-Buylla, B. Garcia-Ponce, and A. Garay-Arroyo Unique and redundant functional domains of APETALA1 and CAULIFLOWER, two recently duplicated Arabidopsis thaliana floral MADS-box genes J. Exp. Bot., September 1, 2006; 57(12): 3099 - 3107. [Abstract] [Full Text] [PDF]

				G. de Martino, I. Pan, E. Emmanuel, A. Levy, and V. F. Irish Functional Analyses of Two Tomato APETALA3 Genes Demonstrate Diversification in Their Roles in Regulating Floral Development PLANT CELL, August 1, 2006; 18(8): 1833 - 1845. [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]

				D. G. Howarth and M. J. Donoghue Phylogenetic analysis of the "ECE" (CYC/TB1) clade reveals duplications predating the core eudicots PNAS, June 13, 2006; 103(24): 9101 - 9106. [Abstract] [Full Text] [PDF]

				S. Konishi, T. Izawa, S. Y. Lin, K. Ebana, Y. Fukuta, T. Sasaki, and M. Yano An SNP Caused Loss of Seed Shattering During Rice Domestication Science, June 2, 2006; 312(5778): 1392 - 1396. [Abstract] [Full Text] [PDF]

				J. M. Duarte, L. Cui, P. K. Wall, Q. Zhang, X. Zhang, J. Leebens-Mack, H. Ma, N. Altman, and C. W. dePamphilis Expression Pattern Shifts Following Duplication Indicative of Subfunctionalization and Neofunctionalization in Regulatory Genes of Arabidopsis Mol. Biol. Evol., February 1, 2006; 23(2): 469 - 478. [Abstract] [Full Text] [PDF]

				T. Yamaguchi, D. Y. Lee, A. Miyao, H. Hirochika, G. An, and H.-Y. Hirano Functional Diversification of the Two C-Class MADS Box Genes OSMADS3 and OSMADS58 in Oryza sativa PLANT CELL, January 1, 2006; 18(1): 15 - 28. [Abstract] [Full Text] [PDF]

				J. Leebens-Mack, L. A. Raubeson, L. Cui, J. V. Kuehl, M. H. Fourcade, T. W. Chumley, J. L. Boore, R. K. Jansen, and C. W. dePamphilis Identifying the Basal Angiosperm Node in Chloroplast Genome Phylogenies: Sampling One's Way Out of the Felsenstein Zone Mol. Biol. Evol., October 1, 2005; 22(10): 1948 - 1963. [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]

				L. M. Zahn, H. Kong, J. H. Leebens-Mack, S. Kim, P. S. Soltis, L. L. Landherr, D. E. Soltis, C. W. dePamphilis, and H. Ma The Evolution of the SEPALLATA Subfamily of MADS-Box Genes: A Preangiosperm Origin With Multiple Duplications Throughout Angiosperm History Genetics, April 1, 2005; 169(4): 2209 - 2223. [Abstract] [Full Text] [PDF]

				Y. Tanabe, M. Hasebe, H. Sekimoto, T. Nishiyama, M. Kitani, K. Henschel, T. Munster, G. Theissen, H. Nozaki, and M. Ito Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes PNAS, February 15, 2005; 102(7): 2436 - 2441. [Abstract] [Full Text] [PDF]

				W. E. Friedman, R. C. Moore, and M. D. Purugganan The evolution of plant development Am. J. Botany, October 1, 2004; 91(10): 1726 - 1741. [Abstract] [Full Text] [PDF]