Large-Scale Trends in the Evolution of Gene Structures within 11 Animal Genomes

Yandell, Mark; Mungall, Chris J.; Smith, Chris; Prochnik, Simon; Kaminker, Joshua; Hartzell, George; Lewis, Suzanna; Rubin, Gerald M.

doi:10.1371/journal.pcbi.0020015

Large-Scale Trends in the Evolution of Gene Structures within 11 Animal Genomes

Journal Article · Fri Mar 03 00:00:00 EST 2006 · PLoS Computational Biology (Online)

DOI:https://doi.org/10.1371/journal.pcbi.0020015· OSTI ID:1627180

Yandell, Mark ^[1]; Mungall, Chris J. ^[2]; Smith, Chris ^[3]; Prochnik, Simon ^[4]; Kaminker, Joshua ^[3]; Hartzell, George ^[3]; Lewis, Suzanna ^[3]; Rubin, Gerald M. ^[5]

University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); DOE/OSTI
University of California, Berkeley, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Genome Sciences
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

We have used the annotations of six animal genomes (Homo sapiens, Mus musculus, Ciona intestinalis, Drosophila melanogaster, Anopheles gambiae, and Caenorhabditis elegans) together with the sequences of five unannotated Drosophila genomes to survey changes in protein sequence and gene structure over a variety of timescales—from the less than 5 million years since the divergence of D. simulans and D. melanogaster to the more than 500 million years that have elapsed since the Cambrian explosion. To do so, we have developed a new open-source software library called CGL (for ‘‘Comparative Genomics Library’’). Our results demonstrate that change in intron–exon structure is gradual, clock-like, and largely independent of coding-sequence evolution. This means that genome annotations can be used in new ways to inform, corroborate, and test conclusions drawn from comparative genomics analyses that are based upon protein and nucleotide sequence similarities.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Howard Hughes Medical Institute; National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627180

Journal Information:: PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 3 Vol. 2; ISSN 1553-7358

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

Amino acid substitution matrices from an information theoretic perspective Altschul, Stephen F. Journal of Molecular Biology, Vol. 219, Issue 3 https://doi.org/10.1016/0022-2836(91)90193-a	journal	June 1991
Genomic clocks and evolutionary timescales Blair Hedges, S.; Kumar, Sudhir Trends in Genetics, Vol. 19, Issue 4 https://doi.org/10.1016/s0168-9525(03)00053-2	journal	April 2003
The evolution of spliceosomal introns Lynch, M. Current Opinion in Genetics & Development, Vol. 12, Issue 6 https://doi.org/10.1016/s0959-437x(02)00360-x	journal	December 2002
Initial sequencing and analysis of the human genome Lander, Eric S.; Linton, Lauren M. Nature, Vol. 409, Issue 6822, p. 860-921 https://doi.org/10.1038/35057062	journal	February 2001
Evidence for a clade of nematodes, arthropods and other moulting animals Aguinaldo, Anna Marie A.; Turbeville, James M.; Linford, Lawrence S. Nature, Vol. 387, Issue 6632 https://doi.org/10.1038/387489a0	journal	May 1997
Initial sequencing and comparative analysis of the mouse genome Consortium, Mouse Genome Sequencing Nature, Vol. 420, Issue 6915, p. 520-562 https://doi.org/10.1038/nature01262	journal	January 2002
Origins of recently gained introns in Caenorhabditis Coghlan, A.; Wolfe, K. H. Proceedings of the National Academy of Sciences, Vol. 101, Issue 31 https://doi.org/10.1073/pnas.0308192101	journal	July 2004
Resolution of a deep animal divergence by the pattern of intron conservation Roy, S. W.; Gilbert, W. Proceedings of the National Academy of Sciences, Vol. 102, Issue 12 https://doi.org/10.1073/pnas.0409891102	journal	March 2005
More on the sequencing of the human genome Waterston, Robert H.; Lander, Eric S.; Sulston, John E. Proceedings of the National Academy of Sciences, Vol. 100, Issue 6 https://doi.org/10.1073/pnas.0634129100	journal	March 2003
Amino acid substitution matrices from protein blocks. Henikoff, S.; Henikoff, J. G. Proceedings of the National Academy of Sciences, Vol. 89, Issue 22, p. 10915-10919 https://doi.org/10.1073/pnas.89.22.10915	journal	November 1992
Selective Constraints on Intron Evolution in Drosophila Parsch, John Genetics, Vol. 165, Issue 4 https://doi.org/10.1093/genetics/165.4.1843	journal	December 2003
Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks Tamura, K. Molecular Biology and Evolution, Vol. 21, Issue 1 https://doi.org/10.1093/molbev/msg236	journal	October 2003
The Evolutionary Gain of Spliceosomal Introns: Sequence and Phase Preferences Qiu, W. -G. Molecular Biology and Evolution, Vol. 21, Issue 7 https://doi.org/10.1093/molbev/msh120	journal	March 2004
Ensembl 2004 Birney, E. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh038	journal	January 2004
Prevalence of intron gain over intron loss in the evolution of paralogous gene families Babenko, V. N. Nucleic Acids Research, Vol. 32, Issue 12 https://doi.org/10.1093/nar/gkh686	journal	July 2004
FlyBase: genes and gene models Drysdale, R. A. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki046	journal	December 2004
WormBase: a comprehensive data resource for Caenorhabditis biology and genomics Chen, N. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki066	journal	December 2004
Estimating Synonymous and Nonsynonymous Substitution Rates Under Realistic Evolutionary Models Yang, Ziheng; Nielsen, Rasmus Molecular Biology and Evolution, Vol. 17, Issue 1 https://doi.org/10.1093/oxfordjournals.molbev.a026236	journal	January 2000
Conservation, Regulation, Synteny, and Introns in a Large-scale C. briggsae-C. elegans Genomic Alignment Kent, W. J. Genome Research, Vol. 10, Issue 8 https://doi.org/10.1101/gr.10.8.1115	journal	August 2000
Indel-Based Evolutionary Distance and Mouse-Human Divergence Ogurtsov, A. Y. Genome Research, Vol. 14, Issue 8 https://doi.org/10.1101/gr.2450504	journal	August 2004
The Bioperl Toolkit: Perl Modules for the Life Sciences Stajich, J. E. Genome Research, Vol. 12, Issue 10 https://doi.org/10.1101/gr.361602	journal	October 2002
A Computer Program for Aligning a cDNA Sequence with a Genomic DNA Sequence Florea, Liliana; Hartzell, George; Zhang, Zheng Genome Research, Vol. 8, Issue 9 https://doi.org/10.1101/gr.8.9.967	journal	September 1998
The Genome Sequence of the Malaria Mosquito Anopheles gambiae Holt, Robert A.; Subramanian, G. Mani; Halpern, Aaron Science, Vol. 298, Issue 5591 https://doi.org/10.1126/science.1076181	journal	October 2002
Genome Sequence of the Nematode C. elegans: A Platform for Investigating Biology No authors listed Science, Vol. 282, Issue 5396 https://doi.org/10.1126/science.282.5396.2012	journal	December 1998
Comparative Genomics of the Eukaryotes Rubin, G. M. Science, Vol. 287, Issue 5461 https://doi.org/10.1126/science.287.5461.2204	journal	March 2000
Amino acid substitution matrices from an information theoretic perspective Altschul, Stephen F. Journal of Molecular Biology, Vol. 219, Issue 3 https://doi.org/10.1016/0022-2836(91)90193-A	journal	June 1991
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
Genomic clocks and evolutionary timescales Blair Hedges, S.; Kumar, Sudhir Trends in Genetics, Vol. 19, Issue 4 https://doi.org/10.1016/S0168-9525(03)00053-2	journal	April 2003
The evolution of spliceosomal introns Lynch, M. Current Opinion in Genetics & Development, Vol. 12, Issue 6 https://doi.org/10.1016/S0959-437X(02)00360-X	journal	December 2002
Molecular Evolution: Introns Fall into Place Stoltzfus, Arlin Current Biology, Vol. 14, Issue 9 https://doi.org/10.1016/j.cub.2004.04.024	journal	May 2004
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
Nonlinear partial differential equations and applications: The signal of ancient introns is obscured by intron density and homolog number Roy, S. W.; Fedorov, A.; Gilbert, W. Proceedings of the National Academy of Sciences, Vol. 99, Issue 24 https://doi.org/10.1073/pnas.242600199	journal	November 2002
Bootstrap confidence levels for phylogenetic trees Efron, B.; Halloran, E.; Holmes, S. Proceedings of the National Academy of Sciences, Vol. 93, Issue 23 https://doi.org/10.1073/pnas.93.23.13429	journal	November 1996
Toward a resolution of the introns early/late debate: Only phase zero introns are correlated with the structure of ancient proteins de Souza, S. J.; Long, M.; Klein, R. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 9 https://doi.org/10.1073/pnas.95.9.5094	journal	April 1998
Phylogenetic Mapping of Intron Positions: A Case Study of Translation Initiation Factor eIF2γ Krauss, Veiko; Pecyna, Marek; Kurz, Katrin Molecular Biology and Evolution, Vol. 22, Issue 1 https://doi.org/10.1093/molbev/msh255	journal	September 2004
Splicing signals in Drosophila : intron size, information content, and consensus sequences Mount, Stephen M.; Burks, Christian; Herts, Gerald Nucleic Acids Research, Vol. 20, Issue 16 https://doi.org/10.1093/nar/20.16.4255	journal	January 1992
FlyBase: a Drosophila database No authors listed Nucleic Acids Research, Vol. 25, Issue 1, p. 63-66 https://doi.org/10.1093/nar/25.1.63	journal	January 1997
Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution Richards, S. Genome Research, Vol. 15, Issue 1 https://doi.org/10.1101/gr.3059305	journal	January 2005
Retroposed New Genes Out of the X in Drosophila Betran, E. Genome Research, Vol. 12, Issue 12 https://doi.org/10.1101/gr.6049	journal	November 2002
The Sequence of the Human Genome Venter, J. Craig; Adams, Mark D.; Myers, Eugene W. Science, Vol. 291, Issue 5507 https://doi.org/10.1126/science.1058040	journal	February 2001
The Draft Genome of Ciona intestinalis: Insights into Chordate and Vertebrate Origins Dehal, P. Science, Vol. 298, Issue 5601 https://doi.org/10.1126/science.1080049	journal	December 2002
Determining Divergence Times of the Major Kingdoms of Living Organisms with a Protein Clock Doolittle, R. F.; Feng, D. -F.; Tsang, S. Science, Vol. 271, Issue 5248 https://doi.org/10.1126/science.271.5248.470	journal	January 1996
Molecular Evidence for Deep Precambrian Divergences Among Metazoan Phyla Wray, G. A.; Levinton, J. S.; Shapiro, L. H. Science, Vol. 274, Issue 5287 https://doi.org/10.1126/science.274.5287.568	journal	October 1996
Genome-scale evidence of the nematode-arthropod clade Dopazo, Hernán; Dopazo, Joaquín Genome Biology, Vol. 6, Issue 5 https://doi.org/10.1186/gb-2005-6-5-r41	journal	January 2005

Cited By (34)

Comparative genomics approach to detecting split-coding regions in a low-coverage genome: lessons from the chimaera Callorhinchus milii (Holocephali, Chondrichthyes) Dessimoz, C.; Zoller, S.; Manousaki, T. Briefings in Bioinformatics, Vol. 12, Issue 5 https://doi.org/10.1093/bib/bbr038	journal	June 2011
ASGARD: an open-access database of annotated transcriptomes for emerging model arthropod species Zeng, V.; Extavour, C. G. Database, Vol. 2012, Issue 0 https://doi.org/10.1093/database/bas048	journal	January 2012
Comparative Analysis of Teleost Genome Sequences Reveals an Ancient Intron Size Expansion in the Zebrafish Lineage Moss, Stephen P.; Joyce, Domino A.; Humphries, Stuart Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evr090	journal	January 2011
Splice Sites Seldom Slide: Intron Evolution in Oomycetes Sêton Bocco, Steven; Csűrös, Miklós Genome Biology and Evolution, Vol. 8, Issue 8 https://doi.org/10.1093/gbe/evw157	journal	July 2016
Quantitative measures for the management and comparison of annotated genomes Eilbeck, Karen; Moore, Barry; Holt, Carson BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-67	journal	January 2009
The nuclear OXPHOS genes in insecta: a common evolutionary origin, a common cis-regulatory motif, a common destiny for gene duplicates Porcelli, Damiano; Barsanti, Paolo; Pesole, Graziano BMC Evolutionary Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2148-7-215	journal	November 2007
Accumulation of CTCF-binding sites drives expression divergence between tandemly duplicated genes in humans Liao, Ben-Yang; Chang, Andrew BMC Genomics, Vol. 15, Issue Suppl 1 https://doi.org/10.1186/1471-2164-15-s1-s8	journal	January 2014
Huntingtin gene evolution in Chordata and its peculiar features in the ascidian Ciona genus Gissi, Carmela; Pesole, Graziano; Cattaneo, Elena BMC Genomics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2164-7-288	journal	November 2006
A cricket Gene Index: a genomic resource for studying neurobiology, speciation, and molecular evolution Danley, Patrick D.; Mullen, Sean P.; Liu, Fenglong BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-109	journal	January 2007
Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire Lévesque, C. André; Brouwer, Henk; Cano, Liliana Genome Biology, Vol. 11, Issue 7 https://doi.org/10.1186/gb-2010-11-7-r73	journal	January 2010
A standard variation file format for human genome sequences Reese, Martin G.; Moore, Barry; Batchelor, Colin Genome Biology, Vol. 11, Issue 8 https://doi.org/10.1186/gb-2010-11-8-r88	journal	January 2010
Genome-Wide Analysis of Human Disease Alleles Reveals That Their Locations Are Correlated in Paralogous Proteins Yandell, Mark; Moore, Barry; Salas, Fidel PLoS Computational Biology, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pcbi.1000218	journal	November 2008
The Agassiz’s desert tortoise genome provides a resource for the conservation of a threatened species Tollis, Marc; DeNardo, Dale F.; Cornelius, John A. PLOS ONE, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pone.0177708	journal	May 2017
A Novel Model for Development, Organization, and Function of Gonadotropes in Fish Pituitary Golan, Matan; Biran, Jakob; Levavi-Sivan, Berta Frontiers in Endocrinology, Vol. 5 https://doi.org/10.3389/fendo.2014.00182	journal	October 2014
The Fibrillar Collagen Family Exposito, Jean-Yves; Valcourt, Ulrich; Cluzel, Caroline International Journal of Molecular Sciences, Vol. 11, Issue 2 https://doi.org/10.3390/ijms11020407	journal	January 2010
Additional file 1 of Protein length distribution is remarkably uniform across the tree of life Nevers, Yannis; Glover, Natasha M.; Dessimoz, Christophe figshare https://doi.org/10.6084/m9.figshare.23434923	dataset	January 2023
Additional file 3 of Protein length distribution is remarkably uniform across the tree of life Nevers, Yannis; Glover, Natasha M.; Dessimoz, Christophe figshare https://doi.org/10.6084/m9.figshare.23434929.v1	dataset	January 2023
Additional file 4 of Protein length distribution is remarkably uniform across the tree of life Nevers, Yannis; Glover, Natasha M.; Dessimoz, Christophe figshare https://doi.org/10.6084/m9.figshare.23434932.v1	dataset	January 2023
Additional file 5 of Protein length distribution is remarkably uniform across the tree of life Nevers, Yannis; Glover, Natasha M.; Dessimoz, Christophe figshare https://doi.org/10.6084/m9.figshare.23434935.v1	dataset	January 2023
Additional file 6 of Protein length distribution is remarkably uniform across the tree of life Nevers, Yannis; Glover, Natasha M.; Dessimoz, Christophe figshare https://doi.org/10.6084/m9.figshare.23434938.v1	dataset	January 2023
Additional file 7 of Protein length distribution is remarkably uniform across the tree of life Nevers, Yannis; Glover, Natasha M.; Dessimoz, Christophe figshare https://doi.org/10.6084/m9.figshare.23434941.v1	dataset	January 2023
Diversity of animal small RNA pathways and their biological utility: Diversity of animal small RNA pathways Okamura, Katsutomo Wiley Interdisciplinary Reviews: RNA, Vol. 3, Issue 3 https://doi.org/10.1002/wrna.113	journal	November 2011
Accelerated Evolutionary Rate of Housekeeping Genes in Tunicates Tsagkogeorga, Georgia; Turon, Xavier; Galtier, Nicolas Journal of Molecular Evolution, Vol. 71, Issue 2 https://doi.org/10.1007/s00239-010-9372-9	journal	August 2010
Phylogenetic analysis and evolution of aromatic amino acid hydroxylase Cao, Jun; Shi, Feng; Liu, Xiaoguang FEBS Letters, Vol. 584, Issue 23 https://doi.org/10.1016/j.febslet.2010.11.005	journal	November 2010
Intronic microRNA precursors that bypass Drosha processing Ruby, J. Graham; Jan, Calvin H.; Bartel, David P. Nature, Vol. 448, Issue 7149 https://doi.org/10.1038/nature05983	journal	June 2007
Gene length as a biological timer to establish temporal transcriptional regulation Kirkconnell, Killeen S.; Magnuson, Brian; Paulsen, Michelle T. Cell Cycle, Vol. 16, Issue 3 https://doi.org/10.1080/15384101.2016.1234550	journal	January 2017
A Chado case study: an ontology-based modular schema for representing genome-associated biological information Mungall, Christopher J.; Emmert, David B. Bioinformatics, Vol. 23, Issue 13 https://doi.org/10.1093/bioinformatics/btm189	journal	July 2007
Endogenous Mechanisms for the Origins of Spliceosomal Introns Catania, F.; Gao, X.; Scofield, D. G. Journal of Heredity, Vol. 100, Issue 5 https://doi.org/10.1093/jhered/esp062	journal	July 2009
Large-Scale Parsimony Analysis of Metazoan Indels in Protein-Coding Genes Belinky, F.; Cohen, O.; Huchon, D. Molecular Biology and Evolution, Vol. 27, Issue 2 https://doi.org/10.1093/molbev/msp263	journal	October 2009
Evolution of the Nitric Oxide Synthase Family in Metazoans Andreakis, N.; D'Aniello, S.; Albalat, R. Molecular Biology and Evolution, Vol. 28, Issue 1 https://doi.org/10.1093/molbev/msq179	journal	July 2010
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions Merchant, S. S.; Prochnik, S. E.; Vallon, O. Science, Vol. 318, Issue 5848, p. 245-250 https://doi.org/10.1126/science.1143609	journal	October 2007
In with the Old, in with the New: The Promiscuity of the Duplication Process Engenders Diverse Pathways for Novel Gene Creation Katju, Vaishali International Journal of Evolutionary Biology, Vol. 2012 https://doi.org/10.1155/2012/341932	journal	January 2012
COGNATE: comparative gene annotation characterizer Wilbrandt, Jeanne; Misof, Bernhard; Niehuis, Oliver BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-3870-8	journal	July 2017
A General Definition and Nomenclature for Alternative Splicing Events Sammeth, Michael; Foissac, Sylvain; Guigó, Roderic PLoS Computational Biology, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pcbi.1000147	journal	August 2008

Similar Records

Intra-species sequence comparisons for annotating genomes

Journal Article · Thu Jul 15 00:00:00 EDT 2004 · Genome Research · OSTI ID:838983

Unlocking the secrets of the genome

Journal Article · Tue Jun 16 20:00:00 EDT 2009 · Nature (London) · OSTI ID:1815440

A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence

Journal Article · Wed Aug 29 20:00:00 EDT 2012 · Genome Research · OSTI ID:1625619

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
animal genomics
drosophila melanogaster
evolutionary genetics
introns
invertebrate genomics
mammalian genomics
phylogenetic analysis
protein structure

Large-Scale Trends in the Evolution of Gene Structures within 11 Animal Genomes

Citation Formats

References (44)

Cited By (34)

Similar Records

Related Subjects