Extensive genomic duplication during early chordate evolution
Abstract
Opinions on the hypothesis that ancient genome duplications contributed to the vertebrate genome range from strong skepticism to strong credence. Previous studies concentrated on small numbers of gene families or chromosomal regions that might not have been representative of the whole genome, or used subjective methods to identify paralogous genes and regions. Here we report a systematic and objective analysis of the draft human genome sequence to identify paralogous chromosomal regions (paralogons) formed during chordate evolution and to estimate the ages of duplicate genes. We found that the human genome contains many more paralogons than would be expected by chance. Molecular clock analysis of all protein families in humans that have orthologs in the fly and nematode indicated that a burst of gene duplication activity took place in the period 350 650 Myr ago and that many of the duplicate genes formed at this time are located within paralogons. Our results support the contention that many of the gene families in vertebrates were formed or expanded by large-scale DNA duplications in an early chordate. Considering the incompleteness of the sequence data and the antiquity of the event, the results are compatible with at least one round of polyploidy.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The estimate of 23,300 genes in the sea urchin is similar to estimates for vertebrates, despite two whole-genome duplications believed to have occurred in the chordate lineage after divergence from echinoderms.
“Our estimate of 23,300 genes is similar to estimates for vertebrates, despite the fact that two whole-genome duplications are believed to have occurred in the chordate lineage after divergence from the lineage leading to the echinoderms (25)(26)(27).”
From The Genome of the Sea Urchin <i>Strongylocentrotus purpuratus</i> (2006) · cites this paper as [27]
Cites
Initial sequencing and analysis of the human genome
International Human Genome Sequencing Consortium, Whitehead Institute for Biomedical Research, C. F. G. R., Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., et al. (2001) · Nature · doi:10.1038/35057062 · Cited by 24,216 · see citing works
Self-citationThe sequence of the human genome
Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., et al. (2001) · Science · doi:10.1126/science.1058040 · Cited by 13,909 · see citing works
Self-citationAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana
Initiative, T. A. G. (2000) · Nature · doi:10.1038/35048692 · Cited by 9,301 · see citing works
Ohno, S. (1970) · doi:10.1007/978-3-642-86659-3 · Cited by 7,833 · see citing works
T-Coffee: A novel method for fast and accurate multiple sequence alignment.
Notredame, C., Higgins, D., & Heringa, J. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4042 · Cited by 7,321 · see citing works
A molecular timescale for vertebrate evolution
Kumar, S., & Hedges, S. B. (1998) · Nature · doi:10.1038/31927 · Cited by 1,936 · see citing works
Molecular evidence for an ancient duplication of the entire yeast genome
Wolfe, K. H., & Shields, D. C. (1997) · Nature · doi:10.1038/42711 · Cited by 1,785 · see citing works
Self-citationGene duplications and the origins of vertebrate development
Holland, P. W. H., García‐Fernàndez, J., Williams, N. A., & Sidow, A. (1994) · Development · doi:10.1242/dev.1994.supplement.125 · Cited by 951 · see citing works
Phylogenetic test of the molecular clock and linearized trees.
Takezaki, N., Rzhetsky, A., & Nei, M. (1995) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040259 · Cited by 826 · see citing works
Yesterday's polyploids and the mystery of diploidization
Wolfe, K. H. (2001) · Nature Reviews Genetics · doi:10.1038/35072009 · Cited by 767 · see citing works
Self-citationThornton, J. W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091553298 · Cited by 674 · see citing works
Wang, D. Y.-C., Kumar, S., & Hedges, S. B. (1999) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.1999.0617 · Cited by 493 · see citing works
Comparative Genomics of the MHC
Flajnik, M. F., & Kasahara, M. (2001) · Immunity · doi:10.1016/s1074-7613(01)00198-4 · Cited by 361 · see citing works
Nei, M., Xu, P., & Glazko, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051611498 · Cited by 329 · see citing works
Vertebrate evolution by interspecific hybridisation – are we polyploid?
Spring, J. (1997) · FEBS Letters · doi:10.1016/s0014-5793(96)01351-8 · Cited by 297 · see citing works
Gu, X., Wang, Y., & Gu, J. (2002) · Nature Genetics · doi:10.1038/ng902 · Cited by 257 · see citing works
Pébusque, M., Coulier, F., Birnbaum, D., & Pontarotti, P. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026022 · Cited by 208 · see citing works
Pattern and Timing of Gene Duplication in Animal GenomesPreprint
Friedman, R., & Hughes, A. L. (2001) · Genome Research · doi:10.1101/gr.200601 · Cited by 198 · see citing works
A simple method for estimating the parameter of substitution rate variation among sites
Gu, X., & Zhang, J. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025720 · Cited by 143 · see citing works
Kojima, S., Itoh, Y., Matsumoto, S., Masuho, Y., & Seiki, M. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01919-0 · Cited by 138 · see citing works
Ancient Genome Duplications Did Not Structure the HumanHox-Bearing ChromosomesPreprint
Hughes, A. L., da Silva, J., & Friedman, R. (2001) · Genome Research · doi:10.1101/gr.160001 · Cited by 119 · see citing works
Hughes, A. L. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025990 · Cited by 115 · see citing works
Gene loss and gain in the evolution of the vertebrates
Ruddle, F. H., Bentley, K. L., Murtha, M. T., et al. (1994) · Development · doi:10.1242/dev.1994.supplement.155 · Cited by 111 · see citing works
Ancient Genome Duplications Did Not Structure the Human Hox-Bearing ChromosomesPreprint
Hughes, A., da Silva, J., & Friedman, R. (2001) · Genome Research · doi:10.1101/gr.gr-1600r · Cited by 105 · see citing works
Divergence pattern of animal gene families and relationship with the Cambrian explosion
Miyata, T., & Suga, H. (2001) · BioEssays · doi:10.1002/bies.1147 · Cited by 90 · see citing works
Biochemical Characterization of Copine: A Ubiquitous Ca2+-Dependent, Phospholipid-Binding Protein
Tomsig, J. L., & Creutz, C. E. (2000) · Biochemistry · doi:10.1021/bi0019949 · Cited by 84 · see citing works
Is Tetralogy True? Lack of Support for the “One-to-Four Rule”
Martin, A. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003723 · Cited by 70 · see citing works
Are We Polyploids? A Brief History of One HypothesisPreprint
Makałowski, W. (2001) · Genome Research · doi:10.1101/gr.188801 · Cited by 53 · see citing works
Coparalogy: Physical and Functional Clusterings in the Human Genome
Popovici, C., Leveugle, M., Birnbaum, D., & Coulier, F. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5794 · Cited by 50 · see citing works
Testing the Parsimony Test of Genome Duplications: A CounterexamplePreprint
Gu, X., & Huang, W. (2002) · Genome Research · doi:10.1101/gr.214402 · Cited by 29 · see citing works
Koh, Y.-S., & Moore, D. D. (1999) · Genomics · doi:10.1006/geno.1998.5683 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The protein kinase complement of the human genome
Manning, G., Whyte, D. B., Martinez, R., Hunter, T., & Sudarsanam, S. (2002) · Science · doi:10.1126/science.1075762 · Cited by 8,145 · see citing works
Jaillon, O., Aury, J.-M., Brunet, F., Petit, J.-L., Stange-Thomann, N., Mauceli, E., Bouneau, L., Fischer, C., Ozouf-Costaz, C., Bernot, A., et al. (2004) · Nature · doi:10.1038/nature03025 · Cited by 1,966 · see citing works
Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate
Dehal, P., & Boore, J. L. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030314 · Cited by 1,526 · see citing works
The Genome of the Sea Urchin <i>Strongylocentrotus purpuratus</i>
Sodergren, E., Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., Angerer, L. M., Arnone, M. I., Burgess, D. R., Burke, R. D., et al. (2006) · Science · doi:10.1126/science.1133609 · Cited by 1,132 · see citing works
Bennett, E. P., Mandel, U., Clausen, H., Gerken, T. A., Fritz, T. A., & Tabak, L. A. (2012) · Glycobiology · doi:10.1093/glycob/cwr182 · Cited by 876 · see citing works
A Recent Polyploidy Superimposed on Older Large-Scale Duplications in the <i>Arabidopsis</i> Genome
Blanc, G., Hokamp, K., & Wolfe, K. H. (2003) · Genome Research · doi:10.1101/gr.751803 · Cited by 724 · see citing works
Self-citationMore than the sum of their parts: On the evolution of proteins from peptides
Söding, J., & Lupas, A. N. (2003) · BioEssays · doi:10.1002/bies.10321 · Cited by 252 · see citing works
Gu, X., Wang, Y., & Gu, J. (2002) · Nature Genetics · doi:10.1038/ng902 · Cited by 257 · see citing works
Wenger, Y., & Galliot, B. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt142 · Cited by 26 · see citing works
Extracellular Matrix Evolution: An Overview
Adams, J. C. (2013) · Biology of Extracellular Matrix · doi:10.1007/978-3-642-36002-2_1 · Cited by 16 · see citing works
- Authors
- McLysaght, A., Hokamp, K., & Wolfe, K. H.
- Affiliations
- Trinity College Dublin (IE)
- Corresponding author
- Wolfe, Kenneth H.
- Venue
- Nature Genetics
- Published
- 2002-05-28
- Volume
- 31
- Issue
- 2
- Pages
- 200-204
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W2011889195
- Cited by
- 530
- References
- 32
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 7 · 2023: 9 · 2022: 5 · 2021: 19 · 2020: 11 · 2019: 13 · 2018: 6 · 2017: 10 · 2016: 18 · 2015: 17 · 2014: 23 · 2013: 21 · 2012: 20
- FWCI
- 64.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Health Research Board
- Science Foundation Ireland
- Trinity College Dublin
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- whole-genome duplication, chordate evolution, vertebrate genome evolution, gene family expansion, molecular clock, polyploidy, human genome
- MeSH terms
- Animals, Chordata, Nonvertebrate, Drosophila melanogaster, Humans, Polyploidy, Genome, Human, Genome, Caenorhabditis elegans, Evolution, Molecular, Gene Duplication
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review