MBE Advance Access published online on November 29, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl182
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1 Laboratorio de Genética Molecular, Desarrollo y Evolución de Plantas, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, 3er Circuito Exterior Junto al Jardín Botánico, Coyoacán, México D.F. 04510. México
* To whom correspondence should be addressed. B class MADS-Box genes have been shown to be key regulators of petal and stamen specification in several eudicot model species such as Arabidopsis thaliana, Antirrhinum majus and Petunia hybrida. Orthologs of these genes have been found across angiosperms and gymnosperms, and it is thought that the basic regulatory function of B proteins is conserved in seed plant lineages. The evolution of B genes is characterized by numerous duplications that might represent key elements fostering the functional diversification of duplicates with a deep impact on their role in the evolution of the floral developmental program. To evaluate this we performed a rigorous statistical analysis with B gene sequences. Using maximum likelihood and Bayesian methods, we estimated molecular substitution rates and determined the selective regimes operating at each residue of B proteins. We implemented tests that rely on phylogenetic hypotheses and codon substitution models to detect significant differences in substitution rates (DSR) and sites under positive adaptive selection (PS) in specific lineages before and after duplication events. With these methods we identified several protein residues fixed by PS shortly after the origin of PI-like and AP3-like lineages in angiosperms and shortly after the origin of the euAP3-like lineage in core eudicots, the two main B gene duplications. The residues inferred to have been fixed by positive selection lie mostly within the K domain of the protein, which is key to promote heterodimerization. Additionally we used a likelihood method that accommodates differences in substitution rates among lineages to estimate duplication dates for AP3-PI and euAP3-TM6, calibrating with data from the fossil record. The dates obtained are consistent with angiosperm origins and diversification of core eudicots. Our results strongly suggest that novel multimer formation with other MADS proteins could have been crucial for the functional divergence of B MADS-box genes. We thus propose a mechanism of functional diversification and persistence of gene duplicates by the appearance of novel multimerization capabilities after duplications. Multimer formation in different combinations of regulatory proteins can be a mechanistic basis for the origin of novel regulatory functions and a gene regulatory mechanism for the appearance of morphological innovations.
Accepted November 8, 2006
Research Article
Functional Diversification of B MADS-Box Homeotic Regulators of Flower Development: Adaptive Evolution in Protein-Protein Interaction Domains After Major Gene Duplication Events
Tania Hernández-Hernández 1, León Patricio Martínez-Castilla 1, and Elena R. Alvarez-Buylla 1 *
Elena R. Alvarez-Buylla, E-mail: ealvarez{at}miranda.ecologia.unam.mx
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