Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis

Hellsten, Uffe; Khokha, Mustafa K.; Grammer, Timothy C.; Harland, Richard M.; Richardson, Paul; Rokhsar, Daniel S.

doi:10.1186/1741-7007-5-31

Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis

Journal Article · Wed Jul 25 00:00:00 EDT 2007 · BMC Biology

DOI:https://doi.org/10.1186/1741-7007-5-31· OSTI ID:1904069

Hellsten, Uffe ^[1]; Khokha, Mustafa K. ^[2]; Grammer, Timothy C. ^[2]; Harland, Richard M. ^[2]; Richardson, Paul ^[2]; Rokhsar, Daniel S. ^[2]

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); OSTI
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States). Center for Integrative Genomics. Dept. of Molecular and Cell Biology

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.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1904069

Journal Information:: BMC Biology, Journal Name: BMC Biology Journal Issue: 1 Vol. 5; ISSN 1741-7007

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (36)

More genes in fish? Wittbrodt, J.; Meyer, A.; Schartl, M. BioEssays, Vol. 20, Issue 6 https://doi.org/10.1002/(SICI)1521-1878(199806)20:6<511::AID-BIES10>3.0.CO;2-3	journal	June 1998
Xenopus, the next generation:X. Tropicalis genetics and genomics Hirsch, Nicolas; Zimmerman, Lyle B.; Grainger, Robert M. Developmental Dynamics, Vol. 225, Issue 4 https://doi.org/10.1002/dvdy.10178	journal	November 2002
Techniques and probes for the study ofXenopus tropicalis development Khokha, Mustafa K.; Chung, Christina; Bustamante, Erika L. Developmental Dynamics, Vol. 225, Issue 4 https://doi.org/10.1002/dvdy.10184	journal	November 2002
Evolution by Gene Duplication Ohno, Susumu Springer Berlin, Heidelberg https://doi.org/10.1007/978-3-642-86659-3	book	January 1970
Evolution of the differential regulation of duplicate genes after polyploidization Ferris, Stephen D.; Whitt, Gregory S. Journal of Molecular Evolution, Vol. 12, Issue 4 https://doi.org/10.1007/BF01732026	journal	December 1979
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Genetics of Xenopus laevis Graf, Jean-Daniel; Kobel, Hans Rudolf Methods in Cell Biology, Vol. 36 https://doi.org/10.1016/S0091-679X(08)60270-8	book	January 1991
Appendix G: In Situ Hybridization: An Improved Whole-Mount Method for Xenopus Embryos Harland, Richard M. Methods in Cell Biology, Vol. 36, 685-695 https://doi.org/10.1016/S0091-679X(08)60307-6	book	January 1991
Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity Paterson, Andrew H.; Bowers, John E.; Chapman, Brad A. Current Opinion in Biotechnology, Vol. 15, Issue 2 https://doi.org/10.1016/j.copbio.2004.03.001	journal	April 2004
Subfunction partitioning, the teleost radiation and the annotation of the human genome Postlethwait, John; Amores, Angel; Cresko, William Trends in Genetics, Vol. 20, Issue 10 https://doi.org/10.1016/j.tig.2004.08.001	journal	October 2004
A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution Evans, Ben J.; Kelley, Darcy B.; Tinsley, Richard C. Molecular Phylogenetics and Evolution, Vol. 33, Issue 1 https://doi.org/10.1016/j.ympev.2004.04.018	journal	October 2004
Ancient origin of the Hox gene cluster Ferrier, David E. K.; Holland, Peter W. H. Nature Reviews Genetics, Vol. 2, Issue 1 https://doi.org/10.1038/35047605	journal	January 2001
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana No authors listed Nature, Vol. 408, Issue 6814, p. 796-815 https://doi.org/10.1038/35048692	journal	December 2000
Yesterday's polyploids and the mystery of diploidization Wolfe, Kenneth H. Nature Reviews Genetics, Vol. 2, Issue 5 https://doi.org/10.1038/35072009	journal	May 2001
Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Jaillon, Olivier; Aury, Jean-Marc; Brunet, Frédéric Nature, Vol. 431, Issue 7011 https://doi.org/10.1038/nature03025	journal	October 2004
The genome of the social amoeba Dictyostelium discoideum Eichinger, L.; Pachebat, J. A.; Glöckner, G. Nature, Vol. 435, Issue 7038 https://doi.org/10.1038/nature03481	journal	May 2005
Extensive genomic duplication during early chordate evolution McLysaght, Aoife; Hokamp, Karsten; Wolfe, Kenneth H. Nature Genetics, Vol. 31, Issue 2 https://doi.org/10.1038/ng884	journal	May 2002
Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution Gu, Xun; Wang, Yufeng; Gu, Jianying Nature Genetics, Vol. 31, Issue 2 https://doi.org/10.1038/ng902	journal	May 2002
On Some Principles Governing Molecular Evolution Kimura, M.; Ohta, T. Proceedings of the National Academy of Sciences, Vol. 71, Issue 7 https://doi.org/10.1073/pnas.71.7.2848	journal	July 1974
Preservation of Duplicate Genes by Complementary, Degenerative Mutations Force, Allan; Lynch, Michael; Pickett, F. Bryan Genetics, Vol. 151, Issue 4 https://doi.org/10.1093/genetics/151.4.1531	journal	April 1999
The sense of smell: genomics of vertebrate odorant receptors Young, J. M. Human Molecular Genetics, Vol. 11, Issue 10 https://doi.org/10.1093/hmg/11.10.1153	journal	May 2002
Fugu Genome Analysis Provides Evidence for a Whole-Genome Duplication Early During the Evolution of Ray-Finned Fishes Christoffels, Alan; Koh, Esther G. L.; Chia, Jer-ming Molecular Biology and Evolution, Vol. 21, Issue 6 https://doi.org/10.1093/molbev/msh114	journal	June 2004
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
The TIGR Gene Indices: clustering and assembling EST and known genes and integration with eukaryotic genomes Lee, Y. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki064	journal	December 2004
Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools Thomas, P. D.; Kejariwal, A.; Guo, N. Nucleic Acids Research, Vol. 34, Issue Web Server https://doi.org/10.1093/nar/gkl229	journal	July 2006
Sequencing and analysis of 10,967 full-length cDNA clones from Xenopus laevis and Xenopus tropicalis reveals post-tetraploidization transcriptome remodeling Morin, R. D. Genome Research, Vol. 16, Issue 6 https://doi.org/10.1101/gr.4871006	journal	June 2006
PANTHER: A Library of Protein Families and Subfamilies Indexed by Function Thomas, P. D. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.772403	journal	September 2003
Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution Blanc, Guillaume; Wolfe, Kenneth H. The Plant Cell, Vol. 16, Issue 7 https://doi.org/10.1105/tpc.021410	journal	June 2004
Zebrafish hox Clusters and Vertebrate Genome Evolution Amores, A. Science, Vol. 282, Issue 5394 https://doi.org/10.1126/science.282.5394.1711	journal	November 1998
The Evolutionary Fate and Consequences of Duplicate Genes Lynch, M. Science, Vol. 290, Issue 5494 https://doi.org/10.1126/science.290.5494.1151	journal	November 2000
Albumin phylogeny for clawed frogs (Xenopus) Bisbee, C.; Baker, M.; Wilson, A. Science, Vol. 195, Issue 4280 https://doi.org/10.1126/science.65013	journal	February 1977
Orthologs, Paralogs, and Evolutionary Genomics Koonin, Eugene V. Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.114725	journal	December 2005
Duplicated genes evolve slower than singletons despite the initial rate increase Jordan, I. King; Wolf, Yuri I.; Koonin, Eugene V. BMC Evolutionary Biology, Vol. 4, Issue 1, p. 22 https://doi.org/10.1186/1471-2148-4-22	journal	January 2004
Multiple Mechanisms Promote the Retained Expression of Gene Duplicates in the Tetraploid Frog Xenopus laevis Chain, Frédéric J. J.; Evans, Ben J. PLoS Genetics, Vol. 2, Issue 4 https://doi.org/10.1371/journal.pgen.0020056	journal	April 2006
Systematic screening for genes specifically expressed in the anterior neuroectoderm during early Xenopus development Takahashi, Noriyuki; Tochimoto, Naoko; Ohmori, Shin-Ya The International Journal of Developmental Biology, Vol. 49, Issue 8 https://doi.org/10.1387/ijdb.052083nt	journal	January 2005
Mechanisms of Haploinsufficiency Revealed by Genome-Wide Profiling in Yeast Deutschbauer, Adam M.; Jaramillo, Daniel F.; Proctor, Michael Genetics, Vol. 169, Issue 4 https://doi.org/10.1534/genetics.104.036871	journal	February 2005

Similar Records

Accelerated Gene Evolution and Subfunctionalization in thePseudotetraploid Frog Xenopus Laevis

Journal Article · Wed Feb 28 23:00:00 EST 2007 · BMC Biology · OSTI ID:919498

Sequencing and analysis of 10967 full-length cDNA clones from Xenopus laevis and Xenopus tropicalis

Journal Article · Sun Oct 30 23:00:00 EST 2005 · Genome Research , vol. 16, no. 6, June 1, 2006, pp. 796-803 · OSTI ID:889991

The Genome of the Western Clawed Frog Xenopus tropicalis

Journal Article · Thu Oct 01 00:00:00 EDT 2009 · Science · OSTI ID:1010537

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Life Sciences & Biomedicine - Other Topics

Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis

Citation Formats

References (36)

Similar Records

Related Subjects