Molecular Evolution of Flower Development: Diversification of the Plant MADS-Box Regulatory Gene Family

INVESTIGATIONS

Molecular Evolution of Flower Development: Diversification of the Plant MADS-Box Regulatory Gene Family

M. D. Purugganan, S. D. Rounsley, R. J. Schmidt and M. F. Yanofsky
Department of Biology, University of California at San Diego, La Jolla, California 92093

Floral homeotic genes that control the specification of meristem and organ identity in developing flowers have been isolated from both Arabidopsis thaliana and Antirrhinum majus. Most of these genes belong to a large family of regulatory genes and possess a characteristic DNA binding domain known as the MADS-box. Members of this gene family display primarily floral-specific expression and are homologous to transcription factors found in several animal and fungal species. Molecular evolutionary analyses reveal that there are appreciable differences in the substitution rates between different domains of these plant MADS-box genes. Phylogenetic analyses also demonstrate that members of the plant MADS-box gene family are organized into several distinct gene groups: the AGAMOUS, APETALA3/PISTILLATA and APETALA1/AGL9 groups. The shared evolutionary history of members of a gene group appear to reflect the distinct functional roles these MADS-box genes play in flower development. Molecular evolutionary analyses also suggest that these different gene groups were established in a relatively short span of evolutionary time and that the various floral homeotic loci originated even before the appearance of the flowering plants.

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[Abstract] [Full Text] [PDF]

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J. Biol. Chem., August 1, 1997; 272(31): 19176 - 19186.
[Abstract] [Full Text] [PDF]

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[Abstract] [Full Text] [PDF]

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				S. Kim, M.-J. Yoo, V. A. Albert, J. S. Farris, P. S. Soltis, and D. E. Soltis Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication Am. J. Botany, December 1, 2004; 91(12): 2102 - 2118. [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]

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				W.-C. Tsai, C.-S. Kuoh, M.-H. Chuang, W.-H. Chen, and H.-H. Chen Four DEF-Like MADS Box Genes Displayed Distinct Floral Morphogenetic Roles in Phalaenopsis Orchid Plant Cell Physiol., July 15, 2004; 45(7): 831 - 844. [Abstract] [Full Text] [PDF]

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				T.-Y. Tzeng, H.-C. Liu, and C.-H. Yang The C-terminal Sequence of LMADS1 Is Essential for the Formation of Homodimers for B Function Proteins J. Biol. Chem., March 12, 2004; 279(11): 10747 - 10755. [Abstract] [Full Text] [PDF]

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				A. Litt and V. F. Irish Duplication and Diversification in the APETALA1/FRUITFULL Floral Homeotic Gene Lineage: Implications for the Evolution of Floral Development Genetics, October 1, 2003; 165(2): 821 - 833. [Abstract] [Full Text] [PDF]

				H.-F. Hsu, C.-H. Huang, L.-T. Chou, and C.-H. Yang Ectopic Expression of an Orchid (Oncidium Gower Ramsey) AGL6-like Gene Promotes Flowering by Activating Flowering Time Genes in Arabidopsis thaliana Plant Cell Physiol., August 15, 2003; 44(8): 783 - 794. [Abstract] [Full Text] [PDF]

				L. Parenicova, S. de Folter, M. Kieffer, D. S. Horner, C. Favalli, J. Busscher, H. E. Cook, R. M. Ingram, M. M. Kater, B. Davies, et al. Molecular and Phylogenetic Analyses of the Complete MADS-Box Transcription Factor Family in Arabidopsis: New Openings to the MADS World PLANT CELL, July 1, 2003; 15(7): 1538 - 1551. [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]

				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]

				M. E. Schranz, P. Quijada, S.-B. Sung, L. Lukens, R. Amasino, and T. C. Osborn Characterization and Effects of the Replicated Flowering Time Gene FLC in Brassica rapa Genetics, November 1, 2002; 162(3): 1457 - 1468. [Abstract] [Full Text] [PDF]

				H.-F. Hsu and C.-H. Yang An Orchid (Oncidium Gower Ramsey) AP3-like MADS Gene Regulates Floral Formation and Initiation Plant Cell Physiol., October 15, 2002; 43(10): 1198 - 1209. [Abstract] [Full Text] [PDF]