Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis

BackgroundAncient 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.ResultsWe 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.ConclusionThese 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.

[1]  E. Koonin Orthologs, Paralogs, and Evolutionary Genomics 1 , 2005 .

[2]  Guillaume Blanc,et al.  Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution , 2004, The Plant Cell Online.

[3]  R. Tinsley,et al.  Biology of Xenopus , 1998 .

[4]  Xun Gu,et al.  Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution , 2002, Nature Genetics.

[5]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[6]  M. Itoh,et al.  Systematic screening for genes specifically expressed in the anterior neuroectoderm during early Xenopus development. , 2005, The International journal of developmental biology.

[7]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[8]  H. Kobel,et al.  Genetics of Xenopus laevis. , 1991, Methods in cell biology.

[9]  E. Koonin Orthologs, paralogs, and evolutionary genomics. , 2005, Annual review of genetics.

[10]  Joachim Wittbrodt,et al.  More genes in fish , 1998 .

[11]  B. Trask,et al.  The sense of smell: genomics of vertebrate odorant receptors. , 2002, Human molecular genetics.

[12]  Ronald W. Davis,et al.  Mechanisms of Haploinsufficiency Revealed by Genome-Wide Profiling in Yeast , 2005, Genetics.

[13]  Peter W. H. Holland,et al.  Ancient origin of the Hox gene cluster , 2001, Nature Reviews Genetics.

[14]  Frédéric J. J. Chain,et al.  Multiple Mechanisms Promote the Retained Expression of Gene Duplicates in the Tetraploid Frog Xenopus laevis , 2006, PLoS genetics.

[15]  H. Kobel,et al.  Chapter 2 Genetics of Xenopus laevis , 1991 .

[16]  Daniel G Peterson,et al.  Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity. , 2004, Current opinion in biotechnology.

[17]  Y L Wang,et al.  Zebrafish hox clusters and vertebrate genome evolution. , 1998, Science.

[18]  K. H. Wolfe Yesterday's polyploids and the mystery of diploidization , 2001, Nature Reviews Genetics.

[19]  L. Zimmerman,et al.  Xenopus, the next generation: X. Tropicalis genetics and genomics , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[21]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[22]  Eugene V Koonin,et al.  Duplicated genes evolve slower than singletons despite the initial rate increase , 2004, BMC Evolutionary Biology.

[23]  John Postlethwait,et al.  Subfunction partitioning, the teleost radiation and the annotation of the human genome. , 2004, Trends in genetics : TIG.

[24]  Gregory S. Whitt,et al.  Evolution of the differential regulation of duplicate genes after polyploidization , 1979, Journal of Molecular Evolution.

[25]  R. Harland,et al.  In situ hybridization: an improved whole-mount method for Xenopus embryos. , 1991, Methods in cell biology.

[26]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[27]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[28]  A. Wilson,et al.  Albumin phylogeny for clawed frogs (Xenopus). , 1977, Science.

[29]  Nancy Papalopulu,et al.  Techniques and probes for the study of Xenopus tropicalis development , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[30]  A. Hughes,et al.  Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. , 1993, Molecular biology and evolution.

[31]  John Quackenbush,et al.  The TIGR Gene Indices: clustering and assembling EST and known genes and integration with eukaryotic genomes , 2004, Nucleic Acids Res..

[32]  D. Kelley,et al.  A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. , 2004, Molecular phylogenetics and evolution.

[33]  Alan Christoffels,et al.  Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. , 2004, Molecular biology and evolution.

[34]  David L. Steffen,et al.  The genome of the social amoeba Dictyostelium discoideum , 2005, Nature.

[35]  Sarah Barber,et al.  Sequencing and analysis of 10,967 full-length cDNA clones from Xenopus laevis and Xenopus tropicalis reveals post-tetraploidization transcriptome remodeling. , 2006, Genome research.

[36]  Anushya Muruganujan,et al.  Applications for protein sequence–function evolution data: mRNA/protein expression analysis and coding SNP scoring tools , 2006, Nucleic Acids Res..

[37]  T. Ohta,et al.  On some principles governing molecular evolution. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Campbell,et al.  PANTHER: a library of protein families and subfamilies indexed by function. , 2003, Genome research.

[39]  Karsten Hokamp,et al.  Extensive genomic duplication during early chordate evolution , 2002, Nature Genetics.

[40]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.