A revamped rat reference genome improves the discovery of genetic diversity in laboratory rats
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic
Typ dokumentu preprinty, časopisecké články
Grantová podpora
R01 GM140287
NIGMS NIH HHS - United States
P01 HL149620
NHLBI NIH HHS - United States
U01 DA043098
NIDA NIH HHS - United States
R01 HL064541
NHLBI NIH HHS - United States
R24 AA013162
NIAAA NIH HHS - United States
U24 HG010859
NHGRI NIH HHS - United States
R21 DK089417
NIDDK NIH HHS - United States
R01 HL089895
NHLBI NIH HHS - United States
R01 HG011252
NHGRI NIH HHS - United States
P30 DA044223
NIDA NIH HHS - United States
R24 OD024617
NIH HHS - United States
P50 DA037844
NIDA NIH HHS - United States
Wellcome Trust - United Kingdom
U01 DA051972
NIDA NIH HHS - United States
U01 DA050239
NIDA NIH HHS - United States
R01 DA048017
NIDA NIH HHS - United States
U01 DA047638
NIDA NIH HHS - United States
U01 DA051234
NIDA NIH HHS - United States
PubMed
37214860
PubMed Central
PMC10197727
DOI
10.1101/2023.04.13.536694
PII: 2023.04.13.536694
Knihovny.cz E-zdroje
- Klíčová slova
- Genetic Map, Heterogeneous Stock, Hybrid Rat Diversity Panel, Inbred Strains, Phylogenetic Tree, Rat, Recombinant Inbred, Reference Genome, Rnor_6.0, mRatBN7.2,
- Publikační typ
- časopisecké články MeSH
- preprinty MeSH
The seventh iteration of the reference genome assembly for Rattus norvegicus-mRatBN7.2-corrects numerous misplaced segments and reduces base-level errors by approximately 9-fold and increases contiguity by 290-fold compared to its predecessor. Gene annotations are now more complete, significantly improving the mapping precision of genomic, transcriptomic, and proteomics data sets. We jointly analyzed 163 short-read whole genome sequencing datasets representing 120 laboratory rat strains and substrains using mRatBN7.2. We defined ~20.0 million sequence variations, of which 18.7 thousand are predicted to potentially impact the function of 6,677 genes. We also generated a new rat genetic map from 1,893 heterogeneous stock rats and annotated transcription start sites and alternative polyadenylation sites. The mRatBN7.2 assembly, along with the extensive analysis of genomic variations among rat strains, enhances our understanding of the rat genome, providing researchers with an expanded resource for studies involving rats.
Center for Immunity and Immunotherapies Seattle Children's Research Institute Seattle WA USA
Center for Proteomics and Metabolomics St Jude Children's Research Hospital Memphis TN USA
Department of Animal Sciences Washington State University Pullman WA USA
Department of Human Genetics University of Michigan Ann Arbor MI USA
Department of Integrative Structural and Computational Biology Scripps Research San Diego CA USA
Department of Medicine University of California San Diego San Diego CA USA
Department of Pediatrics University of Washington School of Medicine Seattle WA USA
Department of Physiology Medical College of Wisconsin Milwaukee WI USA
Department of Psychiatry University of California San Diego San Diego CA USA
Genome Structure and Ageing University of Groningen UMC Groningen The Netherlands
Institute for Genomic Medicine University of California San Diego La Jolla CA USA
Institute of Biotechnology University of Helsinki Helsinki Finland
Institute of Genetics and Biophysics National Research Council Naples Italy
Institute of Physiology Czech Academy of Sciences Prague Czechia
Michigan Neuroscience Institute University of Michigan Ann Arbor MI USA
Rat Genome Database Medical College of Wisconsin Milwaukee WI USA
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Richter C.P. (1954). The effects of domestication and selection on the behavior of the Norway rat. J. Natl. Cancer Inst. 15, 727–738. PubMed
Hulme-Beaman A., Orton D., and Cucchi T. (2021). The origins of the domesticate brown rat (Rattus norvegicus) and its pathways to domestication. Anim Front 11, 78–86. PubMed PMC
Modlinska K., and Pisula W. (2020). The Norway rat, from an obnoxious pest to a laboratory pet. Elife 9. 10.7554/eLife.50651. PubMed DOI PMC
Parker C.C., Chen H., Flagel S.B., Geurts A.M., Richards J.B., Robinson T.E., Solberg Woods L.C., and Palmer A.A. (2013). Rats are the smart choice: Rationale for a renewed focus on rats in behavioral genetics. Neuropharmacology 76 Pt B, 250–258. PubMed PMC
Smith J.R., Hayman G.T., Wang S.-J., Laulederkind S.J.F., Hoffman M.J., Kaldunski M.L., Tutaj M., Thota J., Nalabolu H.S., Ellanki S.L.R., et al. (2020). The Year of the Rat: The Rat Genome Database at 20: a multi-species knowledgebase and analysis platform. Nucleic Acids Res. 48, D731–D742. PubMed PMC
RRRC (2021). Rat Resource & Research Center - Rat Models. https://www.rrrc.us/.
Pravenec M., Klír P., Kren V., Zicha J., and Kunes J. (1989). An analysis of spontaneous hypertension in spontaneously hypertensive rats by means of new recombinant inbred strains. J. Hypertens. 7, 217–221. PubMed
Voigt B., Kuramoto T., Mashimo T., Tsurumi T., Sasaki Y., Hokao R., and Serikawa T. (2008). Evaluation of LEXF/FXLE rat recombinant inbred strains for genetic dissection of complex traits. Physiol. Genomics 32, 335–342. PubMed
Tabakoff B., Smith H., Vanderlinden L.A., Hoffman P.L., and Saba L.M. (2019). Rat Genomics book. Methods Mol. Biol. 2018, 213–231. PubMed
Hansen C., and Spuhler K. (1984). Development of the National Institutes of Health genetically heterogeneous rat stock. Alcohol. Clin. Exp. Res. 8, 477–479. PubMed
Baud A., Hermsen R., Guryev V., Stridh P., Graham D., McBride M.W., Foroud T., Calderari S., Diez M., Ockinger J., et al. (2013). Combined sequence-based and genetic mapping analysis of complex traits in outbred rats. Nat. Genet. 45, 767–775. PubMed PMC
Woods L.C.S., and Mott R. (2017). Heterogeneous Stock Populations for Analysis of Complex Traits. Methods Mol. Biol. 1488, 31–44. PubMed PMC
Solberg Woods L.C., and Palmer A.A. (2019). Using Heterogeneous Stocks for Fine-Mapping Genetically Complex Traits. Methods Mol. Biol. 2018, 233–247. PubMed PMC
Chitre A.S., Polesskaya O., Holl K., Gao J., Cheng R., Bimschleger H., Garcia Martinez A., George T., Gileta A.F., Han W., et al. (2020). Genome-Wide Association Study in 3,173 Outbred Rats Identifies Multiple Loci for Body Weight, Adiposity, and Fasting Glucose. Obesity 28, 1964–1973. PubMed PMC
Gunturkun M.H., Wang T., Chitre A.S., Garcia Martinez A., Holl K., St Pierre C., Bimschleger H., Gao J., Cheng R., Polesskaya O., et al. (2022). Genome-Wide Association Study on Three Behaviors Tested in an Open Field in Heterogeneous Stock Rats Identifies Multiple Loci Implicated in Psychiatric Disorders. Front. Psychiatry 13, 790566. PubMed PMC
Kaldunski M.L., Smith J.R., Hayman G.T., Brodie K., De Pons J.L., Demos W.M., Gibson A.C., Hill M.L., Hoffman M.J., Lamers L., et al. (2022). The Rat Genome Database (RGD) facilitates genomic and phenotypic data integration across multiple species for biomedical research. Mamm. Genome 33, 66–80. PubMed PMC
Gibbs R.A., Weinstock G.M., Metzker M.L., Muzny D.M., Sodergren E.J., Scherer S., Scott G., Steffen D., Worley K.C., Burch P.E., et al. (2004). Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428, 493–521. PubMed
Worley K.C., Weinstock G.M., and Gibbs R.A. (2008). Rats in the genomic era. Physiol. Genomics 32, 273–282. PubMed
Twigger S.N., Pruitt K.D., Fernández-Suárez X.M., Karolchik D., Worley K.C., Maglott D.R., Brown G., Weinstock G., Gibbs R.A., Kent J., et al. (2008). What everybody should know about the rat genome and its online resources. Nat. Genet. 40, 523–527. PubMed PMC
van Heesch S., Kloosterman W.P., Lansu N., Ruzius F.-P., Levandowsky E., Lee C.C., Zhou S., Goldstein S., Schwartz D.C., Harkins T.T., et al. (2013). Improving mammalian genome scaffolding using large insert mate-pair next-generation sequencing. BMC Genomics 14, 257. PubMed PMC
Tutaj M., Smith J.R., and Bolton E.R. (2019). Rat Genome Assemblies, Annotation, and Variant Repository. In Rat Genomics, Hayman G. T., Smith J. R., Dwinell M. R., and Shimoyama M., eds. (Springer; New York: ), pp. 43–70. PubMed
Ramdas S., Ozel A.B., Treutelaar M.K., Holl K., Mandel M., Woods L.C.S., and Li J.Z. (2019). Extended regions of suspected mis-assembly in the rat reference genome. Sci Data 6, 39. PubMed PMC
Howe K., Dwinell M., Shimoyama M., Corton C., Betteridge E., Dove A., Quail M.A., Smith M., Saba L., Williams R.W., et al. (2021). The genome sequence of the Norway rat, Rattus norvegicus Berkenhout 1769. Wellcome Open Res. 6, 118. PubMed PMC
Howe K., Chow W., Collins J., Pelan S., Pointon D.-L., Sims Y., Torrance J., Tracey A., and Wood J. (2021). Significantly improving the quality of genome assemblies through curation. Gigascience 10. 10.1093/gigascience/giaa153. PubMed DOI PMC
Poplin R., Chang P.-C., Alexander D., Schwartz S., Colthurst T., Ku A., Newburger D., Dijamco J., Nguyen N., Afshar P.T., et al. (2018). A universal SNP and small-indel variant caller using deep neural networks. Nat. Biotechnol. 10.1038/nbt.4235. PubMed DOI
Yun T., Li H., Chang P.-C., Lin M.F., Carroll A., and McLean C.Y. (2020). Accurate, scalable cohort variant calls using DeepVariant and GLnexus. Cold Spring Harbor Laboratory, 2020.02.10.942086. 10.1101/2020.02.10.942086. PubMed DOI PMC
Manni M., Berkeley M.R., Seppey M., Simão F.A., and Zdobnov E.M. (2021). BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes. Mol. Biol. Evol. 38, 4647–4654. PubMed PMC
Zhou X., Li R., Michal J.J., Wu X.-L., Liu Z., Zhao H., Xia Y., Du W., Wildung M.R., Pouchnik D.J., et al. (2016). Accurate Profiling of Gene Expression and Alternative Polyadenylation with Whole Transcriptome Termini Site Sequencing (WTTS-Seq). Genetics 203, 683–697. PubMed PMC
Munro D., Wang T., Chitre A.S., Polesskaya O., Ehsan N., Gao J., Gusev A., Woods L.C.S., Saba L.M., Chen H., et al. (2022). The regulatory landscape of multiple brain regions in outbred heterogeneous stock rats. Nucleic Acids Res. 10.1093/nar/gkac912. PubMed DOI PMC
Canzian F. (1997). Phylogenetics of the laboratory rat Rattus norvegicus. Genome Res. 7, 262–267. PubMed
Thomas M.A., Chen C.-F., Jensen-Seaman M.I., Tonellato P.J., and Twigger S.N. (2003). Phylogenetics of rat inbred strains. Mamm. Genome 14, 61–64. PubMed
Mashimo T., Voigt B., Tsurumi T., Naoi K., Nakanishi S., Yamasaki K.-I., Kuramoto T., and Serikawa T. (2006). A set of highly informative rat simple sequence length polymorphism (SSLP) markers and genetically defined rat strains. BMC Genet. 7, 19. PubMed PMC
Atanur S.S., Diaz A.G., Maratou K., Sarkis A., Rotival M., Game L., Tschannen M.R., Kaisaki P.J., Otto G.W., Ma M.C.J., et al. (2013). Genome sequencing reveals loci under artificial selection that underlie disease phenotypes in the laboratory rat. Cell 154, 691–703. PubMed PMC
Martín-Gálvez D., Dunoyer de Segonzac D., Ma M.C.J., Kwitek A.E., Thybert D., and Flicek P. (2017). Genome variation and conserved regulation identify genomic regions responsible for strain specific phenotypes in rat. BMC Genomics 18, 986. PubMed PMC
Ma M.C.J., Atanur S.S., Aitman T.J., and Kwitek A.E. (2014). Genomic structure of nucleotide diversity among Lyon rat models of metabolic syndrome. BMC Genomics 15, 197. PubMed PMC
Buniello A., MacArthur J.A.L., Cerezo M., Harris L.W., Hayhurst J., Malangone C., McMahon A., Morales J., Mountjoy E., Sollis E., et al. (2019). The NHGRI-EBI GWAS Catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res. 47, D1005–D1012. PubMed PMC
Walker B.J., Abeel T., Shea T., Priest M., Abouelliel A., Sakthikumar S., Cuomo C.A., Zeng Q., Wortman J., Young S.K., et al. (2014). Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement. PLoS One 9, e112963. PubMed PMC
Mikheenko A., Prjibelski A., Saveliev V., Antipov D., and Gurevich A. (2018). Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 34, i142–i150. PubMed PMC
Rhie A., Walenz B.P., Koren S., and Phillippy A.M. (2020). Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 21, 245. PubMed PMC
Koren S., Phillippy A.M., Simpson J.T., Loman N.J., and Loose M. (2019). Reply to “Errors in long-read assemblies can critically affect protein prediction.” Nat. Biotechnol. 37, 127–128. PubMed
Watson M., and Warr A. (2019). Errors in long-read assemblies can critically affect protein prediction. Nat. Biotechnol. 37, 124–126. PubMed
Sacristán-Horcajada E., González-de la Fuente S., Peiró-Pastor R., Carrasco-Ramiro F., Amils R., Requena J.M., Berenguer J., and Aguado B. (2021). ARAMIS: From systematic errors of NGS long reads to accurate assemblies. Brief. Bioinform. 22. 10.1093/bib/bbab170. PubMed DOI PMC
Rhie A., McCarthy S.A., Fedrigo O., Damas J., Formenti G., Koren S., Uliano-Silva M., Chow W., Fungtammasan A., Kim J., et al. (2021). Towards complete and error-free genome assemblies of all vertebrate species. Nature 592, 737–746. PubMed PMC
Chin C.-S., Peluso P., Sedlazeck F.J., Nattestad M., Concepcion G.T., Clum A., Dunn C., O’Malley R., Figueroa-Balderas R., Morales-Cruz A., et al. (2016). Phased diploid genome assembly with single-molecule real-time sequencing. Nat. Methods 13, 1050–1054. PubMed PMC
de Jong T.V., Chen H., Brashear W.A., Kochan K.J., Hillhouse A.E., Zhu Y., Dhande I.S., Hudson E.A., Sumlut M.H., Smith M.L., et al. (2022). mRatBN7.2: familiar and unfamiliar features of a new rat genome reference assembly. Physiol. Genomics 54, 251–260. PubMed PMC
Nurk S., Koren S., Rhie A., Rautiainen M., Bzikadze A.V., Mikheenko A., Vollger M.R., Altemose N., Uralsky L., Gershman A., et al. (2022). The complete sequence of a human genome. Science 376, 44–53. PubMed PMC
Hermsen R., de Ligt J., Spee W., Blokzijl F., Schäfer S., Adami E., Boymans S., Flink S., van Boxtel R., van der Weide R.H., et al. (2015). Genomic landscape of rat strain and substrain variation. BMC Genomics 16, 357. PubMed PMC
Supernat A., Vidarsson O.V., Steen V.M., and Stokowy T. (2018). Comparison of three variant callers for human whole genome sequencing. Sci. Rep. 8, 17851. PubMed PMC
Ashbrook D.G., Arends D., Prins P., Mulligan M.K., Roy S., Williams E.G., Lutz C.M., Valenzuela A., Bohl C.J., Ingels J.F., et al. (2021). A platform for experimental precision medicine: The extended BXD mouse family. Cell Syst 12, 235–247.e9. PubMed PMC
Ashbrook D.G., Sasani T., Maksimov M., Gunturkun M.H., Ma N., Villani F., Ren Y., Rothschild D., Chen H., Lu L., et al. (2022). Private and sub-family specific mutations of founder haplotypes in the BXD family reveal phenotypic consequences relevant to health and disease. bioRxiv, 2022.04.21.489063. 10.1101/2022.04.21.489063. DOI
Pattee J., Vanderlinden L.A., Mahaffey S., Hoffman P., Tabakoff B., and Saba L.M. (2022). Evaluation and characterization of expression quantitative trait analysis methods in the Hybrid Rat Diversity Panel. Front. Genet. 13, 947423. PubMed PMC
Senko A.N., Overall R.W., Silhavy J., Mlejnek P., Malínská H., Hüttl M., Marková I., Fabel K.S., Lu L., Stuchlik A., et al. (2022). Systems genetics in the rat HXB/BXH family identifies Tti2 as a pleiotropic quantitative trait gene for adult hippocampal neurogenesis and serum glucose. PLoS Genet. 18, e1009638. PubMed PMC
Bryant C.D., Smith D.J., Kantak K.M., Nowak T.S., Williams R.W. Jr, Damaj M.I., Redei E.E., Chen H., and Mulligan M.K. (2020). Facilitating Complex Trait Analysis via Reduced Complexity Crosses. Trends Genet. 36, 549–562. PubMed PMC
Witte F., Ruiz-Orera J., Mattioli C.C., Blachut S., Adami E., Schulz J.F., Schneider-Lunitz V., Hummel O., Patone G., Mücke M.B., et al. (2021). A trans locus causes a ribosomopathy in hypertrophic hearts that affects mRNA translation in a protein length-dependent fashion. Genome Biol. 22, 191. PubMed PMC
Pravenec M., Kožich V., Krijt J., Sokolová J., Zídek V., Landa V., Mlejnek P., Šilhavý J., Šimáková M., Škop V., et al. (2016). Genetic Variation in Renal Expression of Folate Receptor 1 (Folr1) Gene Predisposes Spontaneously Hypertensive Rats to Metabolic Syndrome. Hypertension 67, 335–341. PubMed
Pravenec M., Churchill P.C., Churchill M.C., Viklicky O., Kazdova L., Aitman T.J., Petretto E., Hubner N., Wallace C.A., Zimdahl H., et al. (2008). Identification of renal Cd36 as a determinant of blood pressure and risk for hypertension. Nat. Genet. 40, 952–954. PubMed
Heinig M., Petretto E., Wallace C., Bottolo L., Rotival M., Lu H., Li Y., Sarwar R., Langley S.R., Bauerfeind A., et al. (2010). A trans-acting locus regulates an anti-viral expression network and type 1 diabetes risk. Nature 467, 460–464. PubMed PMC
Lu L.M., Shisa H., Tanuma J., and Hiai H. (1999). Propylnitrosourea-induced T-lymphomas in LEXF RI strains of rats: genetic analysis. Br. J. Cancer 80, 855–861. PubMed PMC
Hubner N., Wallace C.A., Zimdahl H., Petretto E., Schulz H., Maciver F., Mueller M., Hummel O., Monti J., Zidek V., et al. (2005). Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat. Genet. 37, 243–253. PubMed
Holl K., He H., Wedemeyer M., Clopton L., Wert S., Meckes J.K., Cheng R., Kastner A., Palmer A.A., Redei E.E., et al. (2018). Heterogeneous stock rats: a model to study the genetics of despair-like behavior in adolescence. Genes Brain Behav. 17, 139–148. PubMed PMC
Keele G.R., Prokop J.W., He H., Holl K., Littrell J., Deal A., Francic S., Cui L., Gatti D.M., Broman K.W., et al. (2018). Genetic Fine-Mapping and Identification of Candidate Genes and Variants for Adiposity Traits in Outbred Rats. Obesity 26, 213–222. PubMed PMC
Solberg Woods L.C., Holl K.L., Oreper D., Xie Y., Tsaih S.-W., and Valdar W. (2012). Fine-mapping diabetes-related traits, including insulin resistance, in heterogeneous stock rats. Physiol. Genomics 44, 1013–1026. PubMed PMC
Lemen P.M., Hatoum A.S., Dickson P.E., Mittleman G., Agrawal A., Reiner B.C., Berrettini W., Ashbrook D., Gunturkun H., Mulligan M.K., et al. (2022). Opiate responses are controlled by interactions of Oprm1 and Fgf12 loci in the murine BXD family: Correspondence to human GWAS finding. bioRxiv, 2022.03.11.483993. 10.1101/2022.03.11.483993. DOI
Lusis A.J., Seldin M.M., Allayee H., Bennett B.J., Civelek M., Davis R.C., Eskin E., Farber C.R., Hui S., Mehrabian M., et al. (2016). The Hybrid Mouse Diversity Panel: a resource for systems genetics analyses of metabolic and cardiovascular traits. J. Lipid Res. 57, 925–942. PubMed PMC
Ulusoy S., Ozkan G., Alkanat M., Mungan S., Yuluğ E., and Orem A. (2013). Perspective on rhabdomyolysis-induced acute kidney injury and new treatment options. Am. J. Nephrol. 38, 368–378. PubMed
Kang K., Nan C., Fei D., Meng X., Liu W., Zhang W., Jiang L., Zhao M., Pan S., and Zhao M. (2013). Heme oxygenase 1 modulates thrombomodulin and endothelial protein C receptor levels to attenuate septic kidney injury. Shock 40, 136–143. PubMed
Yuan G., Deng J., Wang T., Zhao C., Xu X., Wang P., Voltz J.W., Edin M.L., Xiao X., Chao L., et al. (2007). Tissue kallikrein reverses insulin resistance and attenuates nephropathy in diabetic rats by activation of phosphatidylinositol 3-kinase/protein kinase B and adenosine 5’-monophosphate-activated protein kinase signaling pathways. Endocrinology 148, 2016–2026. PubMed PMC
Osipova E., Barsacchi R., Brown T., Sadanandan K., Gaede A.H., Monte A., Jarrells J., Moebius C., Pippel M., Altshuler D.L., et al. (2023). Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds. Science 379, 185–190. PubMed
Obeidat M. ’en, Zhou G., Li X., Hansel N.N., Rafaels N., Mathias R., Ruczinski I., Beaty T.H., Barnes K.C., Paré P.D., et al. (2018). The genetics of smoking in individuals with chronic obstructive pulmonary disease. Respir. Res. 19, 59. PubMed PMC
Chen N.-C., Solomon B., Mun T., Iyer S., and Langmead B. (2021). Reference flow: reducing reference bias using multiple population genomes. Genome Biol. 22, 8. PubMed PMC
Munger S.C., Raghupathy N., Choi K., Simons A.K., Gatti D.M., Hinerfeld D.A., Svenson K.L., Keller M.P., Attie A.D., Hibbs M.A., et al. (2014). RNA-Seq alignment to individualized genomes improves transcript abundance estimates in multiparent populations. Genetics 198, 59–73. PubMed PMC
Eizenga J.M., Novak A.M., Sibbesen J.A., Heumos S., Ghaffaari A., Hickey G., Chang X., Seaman J.D., Rounthwaite R., Ebler J., et al. (2020). Pangenome Graphs. Annu. Rev. Genomics Hum. Genet. 21, 139–162. PubMed PMC
Kalbfleisch T.S., Hussien AbouEl Ela N.A., Li K., Brashear W.A., Kochan K.J., Hillhouse A.E., Zhu Y., Dhande I.S., Kline E.J., Hudson E.A., et al. (2023). The Assembled Genome of the Stroke-Prone Spontaneously Hypertensive Rat. Hypertension 80, 138–146. PubMed PMC
Rastas P. (2020). Lep-Anchor: automated construction of linkage map anchored haploid genomes. Bioinformatics 36, 2359–2364. PubMed
Kivikoski M., Rastas P., Löytynoja A., and Merilä J. (2021). Automated improvement of stickleback reference genome assemblies with Lep-Anchor software. Mol. Ecol. Resour. 21, 2166–2176. PubMed
ENCODE Project Consortium (2012). An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74. PubMed PMC
Kalikar S., Jain C., Vasimuddin, and Misra S. (2022). Accelerating minimap2 for long-read sequencing applications on modern CPUs. Nature Computational Science 2, 78–83. PubMed
Li H., and Durbin R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595. PubMed PMC
Poplin R., Ruano-Rubio V., DePristo M.A., Fennell T.J., Carneiro M.O., Van der Auwera G.A., Kling D.E., Gauthier L.D., Levy-Moonshine A., Roazen D., et al. (2018). Scaling accurate genetic variant discovery to tens of thousands of samples. bioRxiv, 201178. 10.1101/201178. DOI
Li H. (2018). Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100. PubMed PMC
Jeffares D.C., Jolly C., Hoti M., Speed D., Shaw L., Rallis C., Balloux F., Dessimoz C., Bähler J., and Sedlazeck F.J. (2017). Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast. Nat. Commun. 8, 14061. PubMed PMC
Cingolani P., Platts A., Wang L.L., Coon M., Nguyen T., Wang L., Land S.J., Lu X., and Ruden D.M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92. PubMed PMC
Tarailo-Graovac M., and Chen N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics Chapter 4, Unit 4.10. PubMed
Gunturkun M.H., Flashner E., Wang T., Mulligan M.K., Williams R.W., Prins P., and Chen H. (2022). GeneCup: mining PubMed and GWAS catalog for gene–keyword relationships. G3 Genes|Genomes|Genetics 12, jkac059. PubMed PMC
Hinrichs A.S., Karolchik D., Baertsch R., Barber G.P., Bejerano G., Clawson H., Diekhans M., Furey T.S., Harte R.A., Hsu F., et al. (2006). The UCSC Genome Browser Database: update 2006. Nucleic Acids Res. 34, D590–D598. PubMed PMC
Gileta A.F., Gao J., Chitre A.S., Bimschleger H.V., St Pierre C.L., Gopalakrishnan S., and Palmer A.A. (2020). Adapting Genotyping-by-Sequencing and Variant Calling for Heterogeneous Stock Rats. G3 10, 2195–2205. PubMed PMC
Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A.R., Bender D., Maller J., Sklar P., de Bakker P.I.W., Daly M.J., et al. (2007). PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575. PubMed PMC
Rastas P. (2017). Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data. Bioinformatics 33, 3726–3732. PubMed
Danecek P., Bonfield J.K., Liddle J., Marshall J., Ohan V., Pollard M.O., Whitwham A., Keane T., McCarthy S.A., Davies R.M., et al. (2021). Twelve years of SAMtools and BCFtools. Gigascience 10. 10.1093/gigascience/giab008. PubMed DOI PMC
Tamura K., Stecher G., and Kumar S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 38, 3022–3027. PubMed PMC
Yu G., Smith D.K., Zhu H., Guan Y., and Lam T.T.-Y. (2017). Ggtree : An r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 8, 28–36.
Dobin A., Davis C.A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., and Gingeras T.R. (2012). STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21. PubMed PMC
Duttke S.H., Montilla-Perez P., Chang M.W., Li H., Chen H., Carrette L.L.G., de Guglielmo G., George O., Palmer A.A., Benner C., et al. (2022). Glucocorticoid Receptor-Regulated Enhancers Play a Central Role in the Gene Regulatory Networks Underlying Drug Addiction. Front. Neurosci. 16, 858427. PubMed PMC
Duttke S.H., Chang M.W., Heinz S., and Benner C. (2019). Identification and dynamic quantification of regulatory elements using total RNA. Genome Res. 29, 1836–1846. PubMed PMC
Zhou J.L., de Guglielmo G., Ho A.J., Kallupi M., Li H.-R., Chitre A.S., Carrette L.L.G., George O., Palmer A.A., McVicker G., et al. (2022). Cocaine addiction-like behaviors are associated with long-term changes in gene regulation, energy metabolism, and GABAergic inhibition within the amygdala. bioRxiv, 2022.09.08.506493. 10.1101/2022.09.08.506493. DOI
Delaneau O., Ongen H., Brown A.A., Fort A., Panousis N.I., and Dermitzakis E.T. (2017). A complete tool set for molecular QTL discovery and analysis. Nat. Commun. 8, 15452. PubMed PMC
Jeffs B., Negrin C.D., Graham D., Clark J.S., Anderson N.H., Gauguier D., and Dominiczak A.F. (2000). Applicability of a “speed” congenic strategy to dissect blood pressure quantitative trait loci on rat chromosome 2. Hypertension 35, 179–187. PubMed
Aken B.L., Ayling S., Barrell D., Clarke L., Curwen V., Fairley S., Fernandez Banet J., Billis K., García Girón C., Hourlier T., et al. (2016). The Ensembl gene annotation system. Database 2016. 10.1093/database/baw093. PubMed DOI PMC
Consortium UniProt (2019). UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 47, D506–D515. PubMed PMC
O’Leary N.A., Wright M.W., Brister J.R., Ciufo S., Haddad D., McVeigh R., Rajput B., Robbertse B., Smith-White B., Ako-Adjei D., et al. (2016). Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745. PubMed PMC
Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410. PubMed
Kozomara A., Birgaoanu M., and Griffiths-Jones S. (2019). miRBase: from microRNA sequences to function. Nucleic Acids Res. 47, D155–D162. PubMed PMC
Gruber A.R., Lorenz R., Bernhart S.H., Neuböck R., and Hofacker I.L. (2008). The Vienna RNA websuite. Nucleic Acids Res. 36, W70–W74. PubMed PMC
Kalvari I., Argasinska J., Quinones-Olvera N., Nawrocki E.P., Rivas E., Eddy S.R., Bateman A., Finn R.D., and Petrov A.I. (2018). Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res. 46, D335–D342. PubMed PMC
Nawrocki E.P., and Eddy S.R. (2013). Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935. PubMed PMC
McGarvey K.M., Goldfarb T., Cox E., Farrell C.M., Gupta T., Joardar V.S., Kodali V.K., Murphy M.R., O’Leary N.A., Pujar S., et al. (2015). Mouse genome annotation by the RefSeq project. Mamm. Genome 26, 379–390. PubMed PMC