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Positive Selection and Ancient Duplications in the Evolution of Class

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Positive Selection and Ancient Duplications in the Evolution of Class BMC Evolutionary Biology BioMed Central Research article Open Access Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses Mariana Mondragón-Palomino*1, Luisa Hiese1, Andrea Härter1, Marcus A Koch2 and Günter Theißen1 Address: 1Department of Genetics, Friedrich Schiller University Jena, Philosophenweg 12, D-07743 Jena, Germany and 2Institute for Plant Science, Ruprecht Karls University, Im Neuenheimer Feld 360, 69120 Heidelberg, Germany Email: Mariana Mondragón-Palomino* - [email protected]; Luisa Hiese - [email protected]; Andrea Härter - [email protected]; Marcus A Koch - [email protected]; Günter Theißen - [email protected] * Corresponding author Published: 21 April 2009 Received: 30 November 2008 Accepted: 21 April 2009 BMC Evolutionary Biology 2009, 9:81 doi:10.1186/1471-2148-9-81 This article is available from: http://www.biomedcentral.com/1471-2148/9/81 © 2009 Mondragón-Palomino et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Positive selection is recognized as the prevalence of nonsynonymous over synonymous substitutions in a gene. Models of the functional evolution of duplicated genes consider neofunctionalization as key to the retention of paralogues. For instance, duplicate transcription factors are specifically retained in plant and animal genomes and both positive selection and transcriptional divergence appear to have played a role in their diversification. However, the relative impact of these two factors has not been systematically evaluated. Class B MADS-box genes, comprising DEF-like and GLO-like genes, encode developmental transcription factors essential for establishment of perianth and male organ identity in the flowers of angiosperms. Here, we contrast the role of positive selection and the known divergence in expression patterns of genes encoding class B-like MADS-box transcription factors from monocots, with emphasis on the family Orchidaceae and the order Poales. Although in the monocots these two groups are highly diverse and have a strongly canalized floral morphology, there is no information on the role of positive selection in the evolution of their distinctive flower morphologies. Published research shows that in Poales, class B-like genes are expressed in stamens and in lodicules, the perianth organs whose identity might also be specified by class B-like genes, like the identity of the inner tepals of their lily- like relatives. In orchids, however, the number and pattern of expression of class B-like genes have greatly diverged. Results: The DEF-like genes from Orchidaceae form four well-supported, ancient clades of orthologues. In contrast, orchid GLO-like genes form a single clade of ancient orthologues and recent paralogues. DEF-like genes from orchid clade 2 (OMADS3-like genes) are under less stringent purifying selection than the other orchid DEF- like and GLO-like genes. In comparison with orchids, purifying selection was less stringent in DEF-like and GLO- like genes from Poales. Most importantly, positive selection took place before the major organ reduction and losses in the floral axis that eventually yielded the zygomorphic grass floret. Conclusion: In DEF-like genes of Poales, positive selection on the region mediating interactions with other proteins or DNA could have triggered the evolution of the regulatory mechanisms behind the development of grass-specific reproductive structures. Orchidaceae show a different trend, where gene duplication and transcriptional divergence appear to have played a major role in the canalization and modularization of perianth development. Page 1 of 26 (page number not for citation purposes) BMC Evolutionary Biology 2009, 9:81 http://www.biomedcentral.com/1471-2148/9/81 Background involved in multimeric complex formation (reviewed in One important goal of contemporary biology is to under- [26]). stand how changes in developmental processes generate evolutionary novelties at the morphological level. The The ABCDE model of flower development (reviewed in growing field of evolutionary developmental biology [26]), describes the genetic interactions of the five major ('evo-devo'), approaches this question by determining classes of floral homeotic selector genes termed class A, B, how changes in the number, sequence and expression of C, D and E genes, almost all of which are MIKC-type developmental regulatory genes bring about formation of genes. Each of these gene classes determines the identity new structures. In plants and animals, these developmen- of different floral organs: Class A and E genes specify tal regulatory factors have expanded during evolution sepals; class A, B and E genes determine petals; the combi- (e.g. by gene and genome duplication) to form large and nation of class B, C and E genes specifies stamens (male diverse gene families linked by complex genetic and phys- reproductive organs); class C and E genes determine car- ical interactions [1-3]. pels (female reproductive organs); and class D genes determine ovules. Mutations in transcriptional regulators of development often do not significantly affect the complete organism Of special interest to our study are class B MADS-box because their function is generally confined to a single cat- genes encoding transcription factors, key to the specifica- egory of organs or modules [4]. Thus, it has been hypoth- tion of petal and stamen identity [27-32]. A gene duplica- esized that developmental transcription factors are more tion event that preceded the origin of extant angiosperms likely to evolve new functions and so coordinate the gave rise to DEF- and GLO-like genes, the two major line- development of viable morphological novelty [4]. The ages of class B genes in angiosperms [33-35]. The regula- importance of duplication and diversification of genes tory role of class B genes in some model plants such as encoding transcription factors (e.g. Hox genes) is substan- Arabidopsis thaliana and Antirrhinum majus involves oblig- tiated by genomic analyses showing that these kinds of atory heterodimerization of proteins from the DEF and genes are specifically retained in plant [5] and animal GLO lineages [27,29,36]. Moreover, these heterodimers genomes [6,7]. Additionally, these genes show diverging form higher order complexes with other classes of MADS- patterns of expression, unequal rates of substitution and domain proteins [37-39]. positive selection [6-11]. Recent analyses of the molecular evolution of class B-like Positive selection is also involved in the diversification of MADS-box genes in angiosperms detected positive selec- several groups of plant developmental transcription fac- tion after two key duplication events that generated first tors [12-17]. Recent research has focused on those DEF- and GLO-like genes and later euAP3-type and TM6- encoded by members of the MIKC-type MADS-box gene type genes, which are the major sublineages of DEF-like family because of their key role in the development and genes [22]. The analysis of Hernández-Hernández et al. evolutionary diversification of the angiosperm flower [18- showed that during evolution, positive selection probably 22]. Thus, characterizing their patterns of molecular evo- modified the central property of protein complex forma- lution is essential to understanding their function and the tion because most of the selected sites belong to the K- mechanisms of morphological evolution. Because differ- domain mediating protein – protein interactions in the ent functional classes of MADS-box genes form distinct complexes of MADS-domain transcription factors [22]. clades [23-25], their phylogeny is an important aid to Thus, the evolutionary emergence and divergence of DEF- identify and test hypotheses explaining the different selec- and GLO-like genes after duplication enabled the forma- tive regimes that are generally considered to drive their tion of obligate heterodimeric complexes involved in the evolution. determination of floral organ identity, while the evolu- tion of the class B gene lineages of euAP3-type and TM6- The plant-specific proteins encoded by MIKC-type MADS- type genes may be associated with the morphological box genes have an unique and highly-conserved domain canalization of the core eudicot flower [22,40]. structure that includes MADS- (M-), intervening (I-), ker- atin-like (K-) and C-terminal (C-) domains [26]. The Flowers of many monocots are actinomorphic, with two MADS-domain is mostly involved in DNA-binding and, trimerous whorls of highly similar petaloid organs called together with the I-domain, mediates the formation of tepals. In contrast, at least three kinds of organ identity dimers. The K-domain plays an important role in protein exist in the zygomorphic orchid perianth: in the first floral – protein interaction during both dimerization and the whorl there are three outer tepals (T1–T3; often also formation of multimeric complexes. The C-terminal termed 'sepals'). In the second whorl there are two lateral domain is the most variable region. In some cases it is inner tepals (t1, t2; 'petals') and a median inner tepal (t3) involved in transcription activation, but it may also be called lip or labellum [41,42]. The orchid
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