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      Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis

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          Abstract

          Background

          Ancient whole genome duplications have been implicated in the vertebrate and teleost radiations, and in the emergence of diverse angiosperm lineages, but the evolutionary response to such a perturbation is still poorly understood. The African clawed frog Xenopus laevis experienced a relatively recent tetraploidization ~40 million years ago. Analysis of the considerable amount of EST sequence available for this species together with the genome sequence of the related diploid Xenopus tropicalis provides a unique opportunity to study the genomic response to whole genome duplication.

          Results

          We identified 2218 gene triplets in which a single gene in X. tropicalis corresponds to precisely two co-orthologous genes in X. laevis – the largest such collection published from any duplication event in animals. Analysis of these triplets reveals accelerated evolution or relaxation of constraint in the peptides of the X. laevis pairs compared with the orthologous sequences in X. tropicalis and other vertebrates. In contrast, single-copy X. laevis genes do not show this acceleration. Duplicated genes can differ substantially in expression levels and patterns. We find no significant difference in gene content in the duplicated set, versus the single-copy set based on molecular and biological function ontologies.

          Conclusion

          These results support a scenario in which duplicate genes are retained through a process of subfunctionalization and/or relaxation of constraint on both copies of an ancestral gene.

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          Most cited references30

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          Orthologs, paralogs, and evolutionary genomics.

          Orthologs and paralogs are two fundamentally different types of homologous genes that evolved, respectively, by vertical descent from a single ancestral gene and by duplication. Orthology and paralogy are key concepts of evolutionary genomics. A clear distinction between orthologs and paralogs is critical for the construction of a robust evolutionary classification of genes and reliable functional annotation of newly sequenced genomes. Genome comparisons show that orthologous relationships with genes from taxonomically distant species can be established for the majority of the genes from each sequenced genome. This review examines in depth the definitions and subtypes of orthologs and paralogs, outlines the principal methodological approaches employed for identification of orthology and paralogy, and considers evolutionary and functional implications of these concepts.
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            The genome of the social amoeba Dictyostelium discoideum.

            The social amoebae are exceptional in their ability to alternate between unicellular and multicellular forms. Here we describe the genome of the best-studied member of this group, Dictyostelium discoideum. The gene-dense chromosomes of this organism encode approximately 12,500 predicted proteins, a high proportion of which have long, repetitive amino acid tracts. There are many genes for polyketide synthases and ABC transporters, suggesting an extensive secondary metabolism for producing and exporting small molecules. The genome is rich in complex repeats, one class of which is clustered and may serve as centromeres. Partial copies of the extrachromosomal ribosomal DNA (rDNA) element are found at the ends of each chromosome, suggesting a novel telomere structure and the use of a common mechanism to maintain both the rDNA and chromosomal termini. A proteome-based phylogeny shows that the amoebozoa diverged from the animal-fungal lineage after the plant-animal split, but Dictyostelium seems to have retained more of the diversity of the ancestral genome than have plants, animals or fungi.
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              Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution.

              To study the evolutionary effects of polyploidy on plant gene functions, we analyzed functional genomics data for a large number of duplicated gene pairs formed by ancient polyploidy events in Arabidopsis thaliana. Genes retained in duplicate are not distributed evenly among Gene Ontology or Munich Information Center for Protein Sequences functional categories, which indicates a nonrandom process of gene loss. Genes involved in signal transduction and transcription have been preferentially retained, and those involved in DNA repair have been preferentially lost. Although the two members of each gene pair must originally have had identical transcription profiles, less than half of the pairs formed by the most recent polyploidy event still retain significantly correlated profiles. We identified several cases where groups of duplicated gene pairs have diverged in concert, forming two parallel networks, each containing one member of each gene pair. In these cases, the expression of each gene is strongly correlated with the other nonhomologous genes in its network but poorly correlated with its paralog in the other network. We also find that the rate of protein sequence evolution has been significantly asymmetric in >20% of duplicate pairs. Together, these results suggest that functional diversification of the surviving duplicated genes is a major feature of the long-term evolution of polyploids.
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                Author and article information

                Journal
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                2007
                25 July 2007
                : 5
                : 31
                Affiliations
                [1 ]Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA
                [2 ]Center for Integrative Genomics and Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, CA 94720, USA
                Article
                1741-7007-5-31
                10.1186/1741-7007-5-31
                1949811
                17651506
                68a55436-e1b3-4600-b577-4d84eb6e2392
                Copyright © 2007 Hellsten 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.

                History
                : 30 January 2007
                : 25 July 2007
                Categories
                Research Article

                Life sciences
                Life sciences

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