Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
202878/Z/16/Z
Wellcome Trust - United Kingdom
615584
European Research Council - International
20412
Cancer Research UK - United Kingdom
U41 HG007234
NHGRI NIH HHS - United States
MR/R017565/1
Medical Research Council - United Kingdom
U54 HG007990
NHGRI NIH HHS - United States
Wellcome Trust - United Kingdom
PubMed
29563166
PubMed Central
PMC5880236
DOI
10.1101/gr.234096.117
PII: gr.234096.117
Knihovny.cz E-resources
- MeSH
- CCCTC-Binding Factor genetics MeSH
- Chromosomes genetics MeSH
- Long Interspersed Nucleotide Elements genetics MeSH
- Species Specificity MeSH
- Phylogeny * MeSH
- Genome genetics MeSH
- Karyotyping methods MeSH
- Evolution, Molecular * MeSH
- Muridae genetics MeSH
- Mice MeSH
- Retroelements genetics MeSH
- Binding Sites MeSH
- Animals MeSH
- Check Tag
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- CCCTC-Binding Factor MeSH
- Ctcf protein, mouse MeSH Browser
- Retroelements MeSH
Understanding the mechanisms driving lineage-specific evolution in both primates and rodents has been hindered by the lack of sister clades with a similar phylogenetic structure having high-quality genome assemblies. Here, we have created chromosome-level assemblies of the Mus caroli and Mus pahari genomes. Together with the Mus musculus and Rattus norvegicus genomes, this set of rodent genomes is similar in divergence times to the Hominidae (human-chimpanzee-gorilla-orangutan). By comparing the evolutionary dynamics between the Muridae and Hominidae, we identified punctate events of chromosome reshuffling that shaped the ancestral karyotype of Mus musculus and Mus caroli between 3 and 6 million yr ago, but that are absent in the Hominidae. Hominidae show between four- and sevenfold lower rates of nucleotide change and feature turnover in both neutral and functional sequences, suggesting an underlying coherence to the Muridae acceleration. Our system of matched, high-quality genome assemblies revealed how specific classes of repeats can play lineage-specific roles in related species. Recent LINE activity has remodeled protein-coding loci to a greater extent across the Muridae than the Hominidae, with functional consequences at the species level such as reproductive isolation. Furthermore, we charted a Muridae-specific retrotransposon expansion at unprecedented resolution, revealing how a single nucleotide mutation transformed a specific SINE element into an active CTCF binding site carrier specifically in Mus caroli, which resulted in thousands of novel, species-specific CTCF binding sites. Our results show that the comparison of matched phylogenetic sets of genomes will be an increasingly powerful strategy for understanding mammalian biology.
Bioturing Inc San Diego California 92121 USA
Department of Biomolecular Engineering University of California Santa Cruz California 95064 USA
Department of Medicine College of Medicine University of Arizona Tuscon Arizona 85724 USA
Department of Zoology Faculty of Science Charles University Prague 128 44 Prague Czech Republic
Earlham Institute Norwich Research Park Norwich NR4 7UH United Kingdom
Institute of Mathematics and Computer Science University of Greifswald Greifswald 17487 Germany
Wellcome Sanger Institute Wellcome Genome Campus Hinxton Cambridge CB10 1SA United Kingdom
Wellcome Trust Centre for Human Genetics Oxford OX3 7BN United Kingdom
See more in PubMed
Aken BL, Achuthan P, Akanni W, Amode MR, Bernsdorff F, Bhai J, Billis K, Carvalho-Silva D, Cummins C, Clapham P, et al. 2017. Ensembl 2017. Nucleic Acids Res 45: D635–D642. PubMed PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403–410. PubMed
Ashkenazy H, Penn O, Doron-Faigenboim A, Cohen O, Cannarozzi G, Zomer O, Pupko T. 2012. FastML: a web server for probabilistic reconstruction of ancestral sequences. Nucleic Acids Res 40: W580–W584. PubMed PMC
Atanur SS, Diaz AG, Maratou K, Sarkis A, Rotival M, Game L, Tschannen MR, Kaisaki PJ, Otto GW, Ma MC, et al. 2013. Genome sequencing reveals loci under artificial selection that underlie disease phenotypes in the laboratory rat. Cell 154: 691–703. PubMed PMC
Bailey JA, Baertsch R, Kent WJ, Haussler D, Eichler EE. 2004. Hotspots of mammalian chromosomal evolution. Genome Biol 5: R23. PubMed PMC
Bailey TL, Johnson J, Grant CE, Noble WS. 2015. The MEME suite. Nucleic Acids Res 43: W39–W49. PubMed PMC
Batzer MA, Deininger PL. 2002. Alu repeats and human genomic diversity. Nat Rev Genet 3: 370–379. PubMed
Bimova BV, Macholan M, Baird SJ, Munclinger P, Dufkova P, Laukaitis CM, Karn RC, Luzynski K, Tucker PK, Pialek J. 2011. Reinforcement selection acting on the European house mouse hybrid zone. Mol Ecol 20: 2403–2424. PubMed
Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10: e1003537. PubMed PMC
Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG, Chew JL, Ruan Y, Wei CL, Ng HH, et al. 2008. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18: 1752–1762. PubMed PMC
The Bovine Genome Sequencing and Analysis Consortium. 2009. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324: 522–528. PubMed PMC
Bromham L. 2009. Why do species vary in their rate of molecular evolution? Biol Lett 5: 401–404. PubMed PMC
Capilla L, Sánchez-Guillén RA, Farré M, Paytuví-Gallart A, Malinverni R, Ventura J, Larkin DM, Ruiz-Herrera A. 2016. Mammalian comparative genomics reveals genetic and epigenetic features associated with genome reshuffling in Rodentia. Genome Biol Evol 8: 3703–3717. PubMed PMC
Carbone L, Harris RA, Gnerre S, Veeramah KR, Lorente-Galdos B, Huddleston J, Meyer TJ, Herrero J, Roos C, Aken B, et al. 2014. Gibbon genome and the fast karyotype evolution of small apes. Nature 513: 195–201. PubMed PMC
Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10: 195–205. PubMed
Chevret P, Robinson TJ, Perez J, Veyrunes F, Britton-Davidian J. 2014. A phylogeographic survey of the pygmy mouse Mus minutoides in South Africa: taxonomic and karyotypic inference from cytochrome b sequences of museum specimens. PLoS One 9: e98499. PubMed PMC
The Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69–87. PubMed
Chuong EB, Elde NC, Feschotte C. 2016. Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351: 1083–1087. PubMed PMC
Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S, She X, Bult CJ, Agarwala R, Cherry JL, DiCuccio M, et al. 2009. Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7: e1000112. PubMed PMC
Dobigny G, Britton-Davidian J, Robinson TJ. 2017. Chromosomal polymorphism in mammals: an evolutionary perspective. Biol Rev Camb Philos Soc 92: 1–21. PubMed
Esnault C, Maestre J, Heidmann T. 2000. Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24: 363–367. PubMed
Ferguson-Smith MA, Trifonov V. 2007. Mammalian karyotype evolution. Nat Rev Genet 8: 950–962. PubMed
Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29–W37. PubMed PMC
Foote AD, Liu Y, Thomas GW, Vinar T, Alfoldi J, Deng J, Dugan S, van Elk CE, Hunter ME, Joshi V, et al. 2015. Convergent evolution of the genomes of marine mammals. Nat Genet 47: 272–275. PubMed PMC
Gaffney DJ, Keightley PD. 2006. Genomic selective constraints in murid noncoding DNA. PLoS Genet 2: e204. PubMed PMC
Garagna S, Page J, Fernandez-Donoso R, Zuccotti M, Searle JB. 2014. The Robertsonian phenomenon in the house mouse: mutation, meiosis and speciation. Chromosoma 123: 529–544. PubMed
Gazave E, Darre F, Morcillo-Suarez C, Petit-Marty N, Carreno A, Marigorta UM, Ryder OA, Blancher A, Rocchi M, Bosch E, et al. 2011. Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. Genome Res 21: 1626–1639. PubMed PMC
Geraldes A, Basset P, Smith KL, Nachman MW. 2011. Higher differentiation among subspecies of the house mouse (Mus musculus) in genomic regions with low recombination. Mol Ecol 20: 4722–4736. PubMed PMC
Gnerre S, Maccallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, et al. 2011. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci 108: 1513–1518. PubMed PMC
Goetting-Minesky MP, Makova KD. 2006. Mammalian male mutation bias: impacts of generation time and regional variation in substitution rates. J Mol Evol 63: 537–544. PubMed
Gordon D, Huddleston J, Chaisson MJ, Hill CM, Kronenberg ZN, Munson KM, Malig M, Raja A, Fiddes I, Hillier LW, et al. 2016. Long-read sequence assembly of the gorilla genome. Science 352: aae0344. PubMed PMC
Groenen MA, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, Rogel-Gaillard C, Park C, Milan D, Megens HJ, et al. 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491: 393–398. PubMed PMC
Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S, et al. 2012. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 22: 1760–1774. PubMed PMC
Hedges DJ, Deininger PL. 2007. Inviting instability: transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat Res 616: 46–59. PubMed PMC
Herrero J, Muffato M, Beal K, Fitzgerald S, Gordon L, Pignatelli M, Vilella AJ, Searle SM, Amode R, Brent S, et al. 2016. Ensembl comparative genomics resources. Database (Oxford) 2016: bav096. PubMed PMC
Irie M, Koga A, Kaneko-Ishino T, Ishino F. 2016. An LTR retrotransposon-derived gene displays lineage-specific structural and putative species-specific functional variations in eutherians. Front Chem 4: 26. PubMed PMC
Jacobs L, Flynn L. 2005. Of mice… again: the Siwalik rodent record, murine distribution, and molecular clocks In Interpreting the past: essays on human, primate, and mammal evolution in honor of David Pilbeam (ed. Lieberman D, et al.), pp. 63–80. Brill Academic Publishers, Boston.
Jacques PE, Jeyakani J, Bourque G. 2013. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9: e1003504. PubMed PMC
Janoušek V, Karn RC, Laukaitis CM. 2013. The role of retrotransposons in gene family expansions: insights from the mouse Abp gene family. BMC Evol Biol 13: 107. PubMed PMC
Janoušek V, Laukaitis CM, Yanchukov A, Karn RC. 2016. The role of retrotransposons in gene family expansions in the human and mouse genomes. Genome Biol Evol 8: 2632–2650. PubMed PMC
Johnson DS, Mortazavi A, Myers RM, Wold B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497–1502. PubMed
Kandul NP, Lukhtanov VA, Pierce NE. 2007. Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution 61: 546–559. PubMed
Kass DH, Kim J, Rao A, Deininger PL. 1997. Evolution of B2 repeats: the muroid explosion. Genetica 99: 1–13. PubMed
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772–780. PubMed PMC
Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, Han L, Marino SM, Sun X, Turanov AA, Yang P, et al. 2011. Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479: 223–227. PubMed PMC
Kirkness EF, Bafna V, Halpern AL, Levy S, Remington K, Rusch DB, Delcher AL, Pop M, Wang W, Fraser CM, et al. 2003. The dog genome: survey sequencing and comparative analysis. Science 301: 1898–1903. PubMed
Koepfli KP, Paten B, Genome 10K Community of Scientists, O'Brien SJ. 2015. The Genome 10K Project: a way forward. Annu Rev Anim Biosci 3: 57–111. PubMed PMC
Kolmogorov M, Armstrong J, Raney BJ, Streeter I, Dunn M, Yang F, Odom D, Flicek P, Keane T, Thybert D, et al. 2016. Chromosome assembly of large and complex genomes using multiple references. bioRxiv 10.1101/088435. PubMed DOI PMC
Konig S, Romoth LW, Gerischer L, Stanke M. 2016. Simultaneous gene finding in multiple genomes. Bioinformatics 32: 3388–3395. PubMed PMC
Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, Ng HH, Bourque G. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42: 631–634. PubMed
Lai W, Choudhary V, Park PJ. 2008. CGHweb: a tool for comparing DNA copy number segmentations from multiple algorithms. Bioinformatics 24: 1014–1015. PubMed PMC
Langergraber KE, Prufer K, Rowney C, Boesch C, Crockford C, Fawcett K, Inoue E, Inoue-Muruyama M, Mitani JC, Muller MN, et al. 2012. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci 109: 15716–15721. PubMed PMC
Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359. PubMed PMC
Laukaitis C, Karn RC. 2012. Recognition of subspecies status mediated by androgen-binding protein (ABP) in the evolution of incipient reinforcement on the European house mouse hybrid zone. In Evolution of the house mouse (ed. Macholan M, et al.), pp. 150–190. Cambridge University Press, Cambridge, UK.
Laukaitis CM, Heger A, Blakley TD, Munclinger P, Ponting CP, Karn RC. 2008. Rapid bursts of androgen-binding protein (Abp) gene duplication occurred independently in diverse mammals. BMC Evol Biol 8: 46. PubMed PMC
Li WH, Tanimura M. 1987. The molecular clock runs more slowly in man than in apes and monkeys. Nature 326: 93–96. PubMed
Li WH, Ellsworth DL, Krushkal J, Chang BH, Hewett-Emmett D. 1996. Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis. Mol Phylogenet Evol 5: 182–187. PubMed
Li W, Shang L, Huang K, Li J, Wang Z, Yao H. 2017. Identification of critical base pairs required for CTCF binding in motif M1 and M2. Protein Cell 8: 544–549. PubMed PMC
Lilue J, Doran AG, Fiddes IT, Abrudan M, Armstrong J, Bennet R, Chow W, Collins J, Czechanski A, Danecek P, et al. 2018. Multiple laboratory mouse reference genomes define strain specific haplotypes and novel functional loci. bioRxiv 10.1101/235838. PubMed DOI PMC
Lin L, Shen S, Tye A, Cai JJ, Jiang P, Davidson BL, Xing Y. 2008. Diverse splicing patterns of exonized Alu elements in human tissues. PLoS Genet 4: e1000225. PubMed PMC
Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M, Clamp M, Chang JL, Kulbokas EJ III, Zody MC, et al. 2005. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803–819. PubMed
Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ, Washietl S, Kheradpour P, Ernst J, Jordan G, Mauceli E, et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478: 476–482. PubMed PMC
Liu GE, Alkan C, Jiang L, Zhao S, Eichler EE. 2009. Comparative analysis of Alu repeats in primate genomes. Genome Res 19: 876–885. PubMed PMC
Liu S, Lorenzen ED, Fumagalli M, Li B, Harris K, Xiong Z, Zhou L, Korneliussen TS, Somel M, Babbitt C, et al. 2014. Population genomics reveal recent speciation and rapid evolutionary adaptation in polar bears. Cell 157: 785–794. PubMed PMC
Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV, Muzny DM, Yang SP, Wang Z, Chinwalla AT, Minx P, et al. 2011. Comparative and demographic analysis of orang-utan genomes. Nature 469: 529–533. PubMed PMC
Loytynoja A, Goldman N. 2010. webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11: 579. PubMed PMC
Lynch VJ, Leclerc RD, May G, Wagner GP. 2011. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43: 1154–1159. PubMed
Marques-Bonet T, Kidd JM, Ventura M, Graves TA, Cheng Z, Hillier LW, Jiang Z, Baker C, Malfavon-Borja R, Fulton LA, et al. 2009. A burst of segmental duplications in the genome of the African great ape ancestor. Nature 457: 877–881. PubMed PMC
Mita P, Boeke JD. 2016. How retrotransposons shape genome regulation. Curr Opin Genet Dev 37: 90–100. PubMed PMC
Mortazavi A, Leeper Thompson EC, Garcia ST, Myers RM, Wold B. 2006. Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire. Genome Res 16: 1208–1221. PubMed PMC
Mouse Genome Sequencing Consortium. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520–562. PubMed
Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G, Auvil L, Beever JE, Chowdhary BP, Galibert F, Gatzke L, et al. 2005. Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309: 613–617. PubMed
Navarro FC, Galante PA. 2013. RCPedia: a database of retrocopied genes. Bioinformatics 29: 1235–1237. PubMed PMC
Navarro FC, Galante PA. 2015. A genome-wide landscape of retrocopies in primate genomes. Genome Biol Evol 7: 2265–2275. PubMed PMC
Nellaker C, Keane TM, Yalcin B, Wong K, Agam A, Belgard TG, Flint J, Adams DJ, Frankel WN, Ponting CP. 2012. The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biol 13: R45. PubMed PMC
Pace JK II, Feschotte C. 2007. The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res 17: 422–432. PubMed PMC
Pachkov M, Balwierz PJ, Arnold P, Ozonov E, van Nimwegen E. 2013. SwissRegulon, a database of genome-wide annotations of regulatory sites: recent updates. Nucleic Acids Res 41: D214–D220. PubMed PMC
Park N, Shirley L, Gu Y, Keane T, Swerdlow H, Quail M. 2013. An improved approach to mate-paired library preparation for Illumina sequencing. Methods Next Generation Seq 1: 10–20.
Paten B, Earl D, Nguyen N, Diekhans M, Zerbino D, Haussler D. 2011. Cactus: algorithms for genome multiple sequence alignment. Genome Res 21: 1512–1528. PubMed PMC
Pei B, Sisu C, Frankish A, Howald C, Habegger L, Mu XJ, Harte R, Balasubramanian S, Tanzer A, Diekhans M, et al. 2012. The GENCODE pseudogene resource. Genome Biol 13: R51. PubMed PMC
Phifer-Rixey M, Nachman MW. 2015. Insights into mammalian biology from the wild house mouse Mus musculus. eLife 4 10.7554/eLife.05959.001. PubMed DOI PMC
Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, Pedersen JS, Katzman S, King B, Onodera C, Siepel A, et al. 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443: 167–172. PubMed
Price MN, Dehal PS, Arkin AP. 2010. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490. PubMed PMC
Rat Genome Sequencing Project Consortium. 2004. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428: 493–521. PubMed
Ray DA, Pagan HJ, Thompson ML, Stevens RD. 2007. Bats with hATs: evidence for recent DNA transposon activity in genus Myotis. Mol Biol Evol 24: 632–639. PubMed
Rhesus Macaque Genome Sequencing and Analysis Consortium. 2007. Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222–234. PubMed
Robberecht C, Voet T, Zamani Esteki M, Nowakowska BA, Vermeesch JR. 2013. Nonallelic homologous recombination between retrotransposable elements is a driver of de novo unbalanced translocations. Genome Res 23: 411–418. PubMed PMC
Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, et al. 2012. Insights into hominid evolution from the gorilla genome sequence. Nature 483: 169–175. PubMed PMC
Schmidt D, Wilson MD, Spyrou C, Brown GD, Hadfield J, Odom DT. 2009. ChIP-seq: using high-throughput sequencing to discover protein–DNA interactions. Methods 48: 240–248. PubMed PMC
Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonçalves A, Kutter C, Brown GD, Marshall A, Flicek P, Odom DT. 2012. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148: 335–348. PubMed PMC
Schneider VA, Graves-Lindsay T, Howe K, Bouk N, Chen HC, Kitts PA, Murphy TD, Pruitt KD, Thibaud-Nissen F, Albracht D, et al. 2017. Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly. Genome Res 27: 849–864. PubMed PMC
Schrago CG. 2014. The effective population sizes of the anthropoid ancestors of the human-chimpanzee lineage provide insights on the historical biogeography of the great apes. Mol Biol Evol 31: 37–47. PubMed
Schwalie PC, Ward MC, Cain CE, Faure AJ, Gilad Y, Odom DT, Flicek P. 2013. Co-binding by YY1 identifies the transcriptionally active, highly conserved set of CTCF-bound regions in primate genomes. Genome Biol 14: R148. PubMed PMC
Sisu C, Pei B, Leng J, Frankish A, Zhang Y, Balasubramanian S, Harte R, Wang D, Rutenberg-Schoenberg M, Clark W, et al. 2014. Comparative analysis of pseudogenes across three phyla. Proc Natl Acad Sci 111: 13361–13366. PubMed PMC
Slater GS, Birney E. 2005. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6: 31. PubMed PMC
Smit AFA, Hubley R, Green P. 1996–2010. RepeatMasker Open-3.0. http://www.repeatmasker.org/.
Stanke M, Tzvetkova A, Morgenstern B. 2006. AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol 7(Suppl 1): S11.1–S11.8. PubMed PMC
Stanke M, Diekhans M, Baertsch R, Haussler D. 2008. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637–644. PubMed
Startek M, Szafranski P, Gambin T, Campbell IM, Hixson P, Shaw CA, Stankiewicz P, Gambin A. 2015. Genome-wide analyses of LINE–LINE-mediated nonallelic homologous recombination. Nucleic Acids Res 43: 2188–2198. PubMed PMC
Sultana T, Zamborlini A, Cristofari G, Lesage P. 2017. Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet 18: 292–308. PubMed
Uchimura A, Higuchi M, Minakuchi Y, Ohno M, Toyoda A, Fujiyama A, Miura I, Wakana S, Nishino J, Yagi T. 2015. Germline mutation rates and the long-term phenotypic effects of mutation accumulation in wild-type laboratory mice and mutator mice. Genome Res 25: 1125–1134. PubMed PMC
Veyrunes F, Britton-Davidian J, Robinson TJ, Calvet E, Denys C, Chevret P. 2005. Molecular phylogeny of the African pygmy mice, subgenus Nannomys (Rodentia, Murinae, Mus): implications for chromosomal evolution. Mol Phylogenet Evol 36: 358–369. PubMed
Veyrunes F, Dobigny G, Yang F, O'Brien PC, Catalan J, Robinson TJ, Britton-Davidian J. 2006. Phylogenomics of the genus Mus (Rodentia; Muridae): Extensive genome repatterning is not restricted to the house mouse. Proc Biol Sci 273: 2925–2934. PubMed PMC
Wu H, Guang X, Al-Fageeh MB, Cao J, Pan S, Zhou H, Zhang L, Abutarboush MH, Xing Y, Xie Z, et al. 2014. Camelid genomes reveal evolution and adaptation to desert environments. Nat Commun 5: 5188. PubMed
Zhang Z, Carriero N, Zheng D, Karro J, Harrison PM, Gerstein M. 2006. PseudoPipe: an automated pseudogene identification pipeline. Bioinformatics 22: 1437–1439. PubMed
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137. PubMed PMC
Zhao S, Shetty J, Hou L, Delcher A, Zhu B, Osoegawa K, de Jong P, Nierman WC, Strausberg RL, Fraser CM. 2004. Human, mouse, and rat genome large-scale rearrangements: stability versus speciation. Genome Res 14: 1851–1860. PubMed PMC