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Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses

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 speci...

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Autores principales: Mondragón-Palomino, Mariana, Hiese, Luisa, Härter, Andrea, Koch, Marcus A, Theißen, Günter
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2680841/
https://www.ncbi.nlm.nih.gov/pubmed/19383167
http://dx.doi.org/10.1186/1471-2148-9-81
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author Mondragón-Palomino, Mariana
Hiese, Luisa
Härter, Andrea
Koch, Marcus A
Theißen, Günter
author_facet Mondragón-Palomino, Mariana
Hiese, Luisa
Härter, Andrea
Koch, Marcus A
Theißen, Günter
author_sort Mondragón-Palomino, Mariana
collection PubMed
description 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.
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spelling pubmed-26808412009-05-13 Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses Mondragón-Palomino, Mariana Hiese, Luisa Härter, Andrea Koch, Marcus A Theißen, Günter BMC Evol Biol Research Article 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. BioMed Central 2009-04-21 /pmc/articles/PMC2680841/ /pubmed/19383167 http://dx.doi.org/10.1186/1471-2148-9-81 Text en Copyright © 2009 Mondragón-Palomino et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 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.
spellingShingle Research Article
Mondragón-Palomino, Mariana
Hiese, Luisa
Härter, Andrea
Koch, Marcus A
Theißen, Günter
Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses
title Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses
title_full Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses
title_fullStr Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses
title_full_unstemmed Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses
title_short Positive selection and ancient duplications in the evolution of class B floral homeotic genes of orchids and grasses
title_sort positive selection and ancient duplications in the evolution of class b floral homeotic genes of orchids and grasses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2680841/
https://www.ncbi.nlm.nih.gov/pubmed/19383167
http://dx.doi.org/10.1186/1471-2148-9-81
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