Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
17 Jan 2024
17 Jan 2024
Historique:
received:
28
10
2021
accepted:
27
10
2023
medline:
18
1
2024
pubmed:
18
1
2024
entrez:
17
1
2024
Statut:
epublish
Résumé
Frogs are an ecologically diverse and phylogenetically ancient group of anuran amphibians that include important vertebrate cell and developmental model systems, notably the genus Xenopus. Here we report a high-quality reference genome sequence for the western clawed frog, Xenopus tropicalis, along with draft chromosome-scale sequences of three distantly related emerging model frog species, Eleutherodactylus coqui, Engystomops pustulosus, and Hymenochirus boettgeri. Frog chromosomes have remained remarkably stable since the Mesozoic Era, with limited Robertsonian (i.e., arm-preserving) translocations and end-to-end fusions found among the smaller chromosomes. Conservation of synteny includes conservation of centromere locations, marked by centromeric tandem repeats associated with Cenp-a binding surrounded by pericentromeric LINE/L1 elements. This work explores the structure of chromosomes across frogs, using a dense meiotic linkage map for X. tropicalis and chromatin conformation capture (Hi-C) data for all species. Abundant satellite repeats occupy the unusually long (~20 megabase) terminal regions of each chromosome that coincide with high rates of recombination. Both embryonic and differentiated cells show reproducible associations of centromeric chromatin and of telomeres, reflecting a Rabl-like configuration. Our comparative analyses reveal 13 conserved ancestral anuran chromosomes from which contemporary frog genomes were constructed.
Identifiants
pubmed: 38233380
doi: 10.1038/s41467-023-43012-9
pii: 10.1038/s41467-023-43012-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
579Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM118183
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
Cannatella, D. C. & de Sá, R. O. Xenopus laevis as a model organism. Syst. Biol. 42, 476–507 (1993).
doi: 10.1093/sysbio/42.4.476
Beetschen, J. C. How did urodele embryos come into prominence as a model system? Int. J. Dev. Biol. 40, 629–636 (1996).
pubmed: 8877434
Brown, D. D. A tribute to the Xenopus laevis oocyte and egg. J. Biol. Chem. 279, 45291–45299 (2004).
pubmed: 15308660
doi: 10.1074/jbc.X400008200
Harland, R. M. & Grainger, R. M. Xenopus research: metamorphosed by genetics and genomics. Trends Genet. 27, 507–515 (2011).
pubmed: 21963197
pmcid: 3601910
doi: 10.1016/j.tig.2011.08.003
Gurdon, J. B. & Hopwood, N. The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int. J. Dev. Biol. 44, 43–50 (2000).
pubmed: 10761846
Blaustein, A. R. & Dobson, A. A message from the frogs. Nature 439, 143–144 (2006).
pubmed: 16407936
doi: 10.1038/439143a
Farrer, R. A. et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc. Natl. Acad. Sci. USA 108, 18732–18736 (2011).
pubmed: 22065772
pmcid: 3219125
doi: 10.1073/pnas.1111915108
Whiles, M. R. et al. Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16, 146–157 (2013).
doi: 10.1007/s10021-012-9602-7
Gomes, A. et al. Bioactive molecules from amphibian skin: their biological activities with reference to therapeutic potentials for possible drug development. Indian J. Exp. Biol. 45, 579–593 (2007).
pubmed: 17821852
McCallum, M. L. Amphibian decline or extinction? Current declines dwarf background extinction rate. hpet 41, 483–491 (2007).
Ryan, M. J., Fox, J. H., Wilczynski, W. & Rand, A. S. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343, 66–67 (1990).
pubmed: 2296291
doi: 10.1038/343066a0
Minsuk, S. B. & Keller, R. E. Surface mesoderm in Xenopus: a revision of the stage 10 fate map. Dev. Genes Evol. 207, 389–401 (1997).
pubmed: 27747438
doi: 10.1007/s004270050128
Daczewska, M. & Saczko, J. Various DNA content in myotube nuclei during myotomal myogenesis in Hymenochirus boettgeri (Anura: Pipidae). Folia Biol. 51, 151–157 (2003).
Romero-Carvajal, A. et al. Embryogenesis and laboratory maintenance of the foam-nesting túngara frogs, genus Engystomops (= Physalaemus). Dev. Dyn. 238, 1444–1454 (2009).
pubmed: 19384855
pmcid: 2934778
doi: 10.1002/dvdy.21952
Ryan, M. J. The brain as a source of selection on the social niche: examples from the psychophysics of mate choice in túngara frogs. Integr. Comp. Biol. 51, 756–770 (2011).
pubmed: 21771854
doi: 10.1093/icb/icr065
Elinson, R. P. Metamorphosis in a frog that does not have a tadpole. Curr. Top. Dev. Biol. 103, 259–276 (2013).
pubmed: 23347522
doi: 10.1016/B978-0-12-385979-2.00009-5
Conlon, J. M. & Mechkarska, M. Host-defense peptides with therapeutic potential from skin secretions of frogs from the family Pipidae. Pharmaceuticals 7, 58–77 (2014).
pubmed: 24434793
pmcid: 3915195
doi: 10.3390/ph7010058
Ryan, M. J. & Guerra, M. A. The mechanism of sound production in túngara frogs and its role in sexual selection and speciation. Curr. Opin. Neurobiol. 28, 54–59 (2014).
pubmed: 25033110
doi: 10.1016/j.conb.2014.06.008
Womble, M., Pickett, M. & Nascone-Yoder, N. Frogs as integrative models for understanding digestive organ development and evolution. Semin. Cell Dev. Biol. 51, 92–105 (2016).
pubmed: 26851628
pmcid: 4798877
doi: 10.1016/j.semcdb.2016.02.001
Burmeister, S. S. Neurobiology of female mate choice in frogs: auditory filtering and valuation. Integr. Comp. Biol. 57, 857–864 (2017).
pubmed: 29048536
doi: 10.1093/icb/icx098
Miller, K. E., Session, A. M. & Heald, R. Kif2a scales meiotic spindle size in Hymenochirus boettgeri. Curr. Biol. 29, 3720–3727.e5 (2019).
pubmed: 31630945
pmcid: 6832855
doi: 10.1016/j.cub.2019.08.073
Ferguson-Smith, M. A. & Trifonov, V. Mammalian karyotype evolution. Nat. Rev. Genet. 8, 950–962 (2007).
pubmed: 18007651
doi: 10.1038/nrg2199
Zhang, G. et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346, 1311–1320 (2014).
pubmed: 25504712
pmcid: 4390078
doi: 10.1126/science.1251385
Kiazim, L. G. et al. Comparative mapping of the macrochromosomes of eight avian species provides further insight into their phylogenetic relationships and avian karyotype evolution. Cells 10, 362 (2021).
pubmed: 33572408
pmcid: 7916199
doi: 10.3390/cells10020362
Mitros, T. et al. A chromosome-scale genome assembly and dense genetic map for Xenopus tropicalis. Dev. Biol. 452, 8–20 (2019).
pubmed: 30980799
doi: 10.1016/j.ydbio.2019.03.015
Niu, L. et al. Three-dimensional folding dynamics of the Xenopus tropicalis genome. Nat. Genet. 53, 1075–1087 (2021).
pubmed: 34099928
pmcid: 8270788
doi: 10.1038/s41588-021-00878-z
Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).
pubmed: 27762356
pmcid: 5313049
doi: 10.1038/nature19840
Denton, R. D., Kudra, R. S., Malcom, J. W., Du Preez, L. & Malone, J. H. The African Bullfrog (Pyxicephalus adspersus) genome unites the two ancestral ingredients for making vertebrate sex chromosomes. Cold Spring Harb. Lab. 329847 https://doi.org/10.1101/329847 (2018).
Li, J. et al. Genomic and transcriptomic insights into molecular basis of sexually dimorphic nuptial spines in Leptobrachium leishanense. Nat. Commun. 10, 5551 (2019).
pubmed: 31804492
pmcid: 6895153
doi: 10.1038/s41467-019-13531-5
Li, Y. et al. Chromosome-level assembly of the mustache toad genome using third-generation DNA sequencing and Hi-C analysis. Gigascience 8, giz114 (2019).
pubmed: 31544214
pmcid: 6755253
doi: 10.1093/gigascience/giz114
Lu, B. et al. A large genome with chromosome-scale assembly sheds light on the evolutionary success of a true toad (Bufo gargarizans). Mol. Ecol. Resour. 21, 1256–1273 (2021).
pubmed: 33426774
doi: 10.1111/1755-0998.13319
Sun, Y.-B., Zhang, Y. & Wang, K. Perspectives on studying molecular adaptations of amphibians in the genomic era. Zool. Res 41, 351–364 (2020).
pubmed: 32390371
pmcid: 7340517
doi: 10.24272/j.issn.2095-8137.2020.046
Wilson, A. C., Sarich, V. M. & Maxson, L. R. The importance of gene rearrangement in evolution: evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proc. Natl. Acad. Sci. USA 71, 3028–3030 (1974).
pubmed: 4528784
pmcid: 388613
doi: 10.1073/pnas.71.8.3028
Gregory, T. R. Animal genome size database. http://www.genomesize.com (2023).
Sotero-Caio, C. G., Challis, R., Kumar, S. & Blaxter, M. Genomes on a Tree (GoaT): a centralized resource for eukaryotic genome sequencing initiatives. BISS 5, e74138 (2021).
doi: 10.3897/biss.5.74138
Morescalchi, A. Evolution and karyology of the amphibians. Boll. Zool. 47, 113–126 (1980).
doi: 10.1080/11250008009438709
Bush, G. L., Case, S. M., Wilson, A. C. & Patton, J. L. Rapid speciation and chromosomal evolution in mammals. Proc. Natl. Acad. Sci. USA 74, 3942–3946 (1977).
pubmed: 269445
pmcid: 431793
doi: 10.1073/pnas.74.9.3942
Nowoshilow, S. et al. The axolotl genome and the evolution of key tissue formation regulators. Nature 554, 50–55 (2018).
pubmed: 29364872
doi: 10.1038/nature25458
Smith, J. J. et al. A chromosome-scale assembly of the axolotl genome. Genome Res. 29, 317–324 (2019).
pubmed: 30679309
pmcid: 6360810
doi: 10.1101/gr.241901.118
Nürnberger, B. et al. A dense linkage map for a large repetitive genome: discovery of the sex-determining region in hybridizing fire-bellied toads (Bombina bombina and Bombina variegata). G3 11, jkab286 (2021).
pubmed: 34849761
pmcid: 8664441
doi: 10.1093/g3journal/jkab286
Deakin, J. E., Graves, J. A. M. & Rens, W. The evolution of marsupial and monotreme chromosomes. Cytogenet. Genome Res. 137, 113–129 (2012).
pubmed: 22777195
doi: 10.1159/000339433
Damas, J. et al. Evolution of the ancestral mammalian karyotype and syntenic regions. Proc. Natl. Acad. Sci. USA 119, e2209139119 (2022).
pubmed: 36161960
pmcid: 9550189
doi: 10.1073/pnas.2209139119
O’Connor, R. E. et al. Reconstruction of the diapsid ancestral genome permits chromosome evolution tracing in avian and non-avian dinosaurs. Nat. Commun. 9, 1883 (2018).
pubmed: 29784931
pmcid: 5962605
doi: 10.1038/s41467-018-04267-9
Bogart, J. P., Balon, E. K. & Bruton, M. N. The chromosomes of the living coelacanth and their remarkable similarity to those of one of the most ancient frogs. J. Hered. 85, 322–325 (1994).
pubmed: 7930502
doi: 10.1093/oxfordjournals.jhered.a111470
Hellsten, U. et al. The genome of the Western clawed frog Xenopus tropicalis. Science 328, 633–636 (2010).
pubmed: 20431018
pmcid: 2994648
doi: 10.1126/science.1183670
Carneiro, M. O. et al. Pacific biosciences sequencing technology for genotyping and variation discovery in human data. BMC Genomics 13, 375 (2012).
pubmed: 22863213
pmcid: 3443046
doi: 10.1186/1471-2164-13-375
Koren, S. et al. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30, 693–700 (2012).
pubmed: 22750884
pmcid: 3707490
doi: 10.1038/nbt.2280
Quail, M. A. et al. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 13, 341 (2012).
pubmed: 22827831
pmcid: 3431227
doi: 10.1186/1471-2164-13-341
Loomis, E. W. et al. Sequencing the unsequenceable: expanded CGG-repeat alleles of the fragile X gene. Genome Res. 23, 121–128 (2013).
pubmed: 23064752
pmcid: 3530672
doi: 10.1101/gr.141705.112
Feng, Y.-J. et al. Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. Proc. Natl. Acad. Sci. USA 114, E5864–E5870 (2017).
pubmed: 28673970
pmcid: 5530686
doi: 10.1073/pnas.1704632114
Schmid, M. et al. The chromosomes of Terraranan frogs. Insights into vertebrate cytogenetics. Cytogenet. Genome Res. 130, 1–14 (2010).
pubmed: 21063086
doi: 10.1159/000301339
Rabello, M. N. Chromosomal studies in Brazilian anurans. Caryologia 23, 45–59 (1970).
doi: 10.1080/00087114.1970.10796362
Scheel, J. J. The chromosomes of some African anuran species. In Genetics and Mutagenesis of Fish (ed Schröder, J. H.) 113–116 (Springer, Berlin, Heidelberg, 1973).
Mezzasalma, M., Glaw, F., Odierna, G., Petraccioli, A. & Guarino, F. M. Karyological analyses of Pseudhymenochirus merlini and Hymenochirus boettgeri provide new insights into the chromosome evolution in the anuran family Pipidae. Zoologischer Anz.—A J. Comp. Zool. 258, 47–53 (2015).
doi: 10.1016/j.jcz.2015.07.001
Temple, G. et al. The completion of the mammalian gene collection (MGC). Genome Res. 19, 2324–2333 (2009).
pubmed: 19767417
pmcid: 2792178
doi: 10.1101/gr.095976.109
Marin, R. et al. Convergent origination of a Drosophila-like dosage compensation mechanism in a reptile lineage. Genome Res. 27, 1974–1987 (2017).
pubmed: 29133310
pmcid: 5741051
doi: 10.1101/gr.223727.117
Owens, N. D. L. et al. Measuring absolute RNA copy numbers at high temporal resolution reveals transcriptome kinetics in development. Cell Rep. 14, 632–647 (2016).
pubmed: 26774488
pmcid: 4731879
doi: 10.1016/j.celrep.2015.12.050
Warren, W. C. et al. A new chicken genome assembly provides insight into avian genome structure. G3 7, 109–117 (2017).
pubmed: 27852011
doi: 10.1534/g3.116.035923
Howe, K. et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498–503 (2013).
pubmed: 23594743
pmcid: 3703927
doi: 10.1038/nature12111
Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562 (2002).
doi: 10.1038/nature01262
Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).
pubmed: 11237011
doi: 10.1038/35057062
Venter, J. C. et al. The sequence of the human genome. Science 291, 1304–1351 (2001).
pubmed: 11181995
doi: 10.1126/science.1058040
Lovell, P. V. et al. Conserved syntenic clusters of protein coding genes are missing in birds. Genome Biol. 15, 565 (2014).
pubmed: 25518852
pmcid: 4290089
doi: 10.1186/s13059-014-0565-1
Xu, L. et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 47, W52–W58 (2019).
pubmed: 31053848
pmcid: 6602458
doi: 10.1093/nar/gkz333
Hartley, G. & O’Neill, R. Centromere repeats: Hidden gems of the genome. Genes 10, 223 (2019).
pubmed: 30884847
pmcid: 6471113
doi: 10.3390/genes10030223
Chueh, A. C., Wong, L. H., Wong, N. & Choo, K. H. A. Variable and hierarchical size distribution of L1-retroelement-enriched CENP-A clusters within a functional human neocentromere. Hum. Mol. Genet. 14, 85–93 (2005).
pubmed: 15537667
doi: 10.1093/hmg/ddi008
Kuznetsova, I. S. et al. LINE-related component of mouse heterochromatin and complex chromocenters’ composition. Chromosome Res. 24, 309–323 (2016).
pubmed: 27116673
doi: 10.1007/s10577-016-9525-9
Suh, A. The specific requirements for CR1 retrotransposition explain the scarcity of retrogenes in birds. J. Mol. Evol. 81, 18–20 (2015).
pubmed: 26223967
doi: 10.1007/s00239-015-9692-x
Benson, G. Tandem Repeats Finder: A program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 (1999).
pubmed: 9862982
pmcid: 148217
doi: 10.1093/nar/27.2.573
Nagylaki, T. Introduction to Theoretical Population Genetics (Springer Berlin Heidelberg, 1992).
Igawa, T. et al. Inbreeding ratio and genetic relationships among strains of the Western clawed frog, Xenopus tropicalis. PLoS ONE 10, e0133963 (2015).
pubmed: 26222540
pmcid: 4519292
doi: 10.1371/journal.pone.0133963
Ford, L. S. & Cannatella, D. C. The major clades of frogs. Herpetol. Monogr. 7, 94–117 (1993).
doi: 10.2307/1466954
Bhutkar, A. et al. Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes. Genetics 179, 1657–1680 (2008).
pubmed: 18622036
pmcid: 2475759
doi: 10.1534/genetics.107.086108
Pyron, R. A. Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Syst. Biol. 60, 466–481 (2011).
pubmed: 21540408
doi: 10.1093/sysbio/syr047
Wright, S. On the probability of fixation of reciprocal translocations. Am. Nat. 75, 513–522 (1941).
doi: 10.1086/280996
Lande, R. The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity 54, 323–332 (1985).
pubmed: 4019220
doi: 10.1038/hdy.1985.43
Schubert, I. & Lysak, M. A. Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet. 27, 207–216 (2011).
pubmed: 21592609
doi: 10.1016/j.tig.2011.03.004
Lysak, M. A. Celebrating Mendel, McClintock, and Darlington: on end-to-end chromosome fusions and nested chromosome fusions. Plant Cell 34, 2475–2491 (2022).
pubmed: 35441689
pmcid: 9252491
doi: 10.1093/plcell/koac116
Griffin, D. K., Robertson, L. B. W., Tempest, H. G. & Skinner, B. M. The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet. Genome Res. 117, 64–77 (2007).
pubmed: 17675846
doi: 10.1159/000103166
Deakin, J. E. & Ezaz, T. Understanding the evolution of reptile chromosomes through applications of combined cytogenetics and genomics approaches. Cytogenet. Genome Res. 157, 7–20 (2019).
pubmed: 30645998
doi: 10.1159/000495974
Maruyama, T. & Imai, H. T. Evolutionary rate of the mammalian karyotype. J. Theor. Biol. 90, 111–121 (1981).
pubmed: 7300369
doi: 10.1016/0022-5193(81)90125-9
Olmo, E. Rate of chromosome changes and speciation in reptiles. Genetica 125, 185–203 (2005).
pubmed: 16247691
doi: 10.1007/s10709-005-8008-2
Duret, L. & Galtier, N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu. Rev. Genomics Hum. Genet. 10, 285–311 (2009).
pubmed: 19630562
doi: 10.1146/annurev-genom-082908-150001
Bogart, J. P. The Influence of Life History on Karyotypic Evolution in Frogs (Academic Press, Inc., 1991).
Bogart, J. P. & Hedges, S. B. Rapid chromosome evolution in Jamaican frogs of the genus Eleutherodactylus (Leptodactylidae). J. Zool. 235, 9–31 (1995).
doi: 10.1111/j.1469-7998.1995.tb05124.x
Jagannathan, M., Cummings, R. & Yamashita, Y. M. A conserved function for pericentromeric satellite DNA. eLife 7, e34122 (2018).
pubmed: 29578410
pmcid: 5957525
doi: 10.7554/eLife.34122
Edwards, N. S. & Murray, A. W. Identification of Xenopus CENP-A and an associated centromeric DNA repeat. Mol. Biol. Cell 16, 1800–1810 (2005).
pubmed: 15673610
pmcid: 1073662
doi: 10.1091/mbc.e04-09-0788
Smith, O. K. et al. Identification and characterization of centromeric sequences in Xenopus laevis. Cold Spring Harb. Lab. https://doi.org/10.1101/2020.06.23.167643 (2020).
Penke, T. J. R., McKay, D. J., Strahl, B. D., Matera, A. G. & Duronio, R. J. Direct interrogation of the role of H3K9 in metazoan heterochromatin function. Genes Dev. 30, 1866–1880 (2016).
pubmed: 27566777
pmcid: 5024684
doi: 10.1101/gad.286278.116
Di Giacomo, M. et al. Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol. Cell 50, 601–608 (2013).
pubmed: 23706823
doi: 10.1016/j.molcel.2013.04.026
Dréau, A., Venu, V., Avdievich, E., Gaspar, L. & Jones, F. C. Genome-wide recombination map construction from single individuals using linked-read sequencing. Nat. Commun. 10, 4309 (2019).
pubmed: 31541091
pmcid: 6754380
doi: 10.1038/s41467-019-12210-9
Backstrom, N. et al. The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res. 20, 485–495 (2010).
pubmed: 20357052
pmcid: 2847751
doi: 10.1101/gr.101410.109
Groenen, M. A. M. et al. A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res. 19, 510–519 (2009).
pubmed: 19088305
pmcid: 2661806
doi: 10.1101/gr.086538.108
Schield, D. R. et al. Snake recombination landscapes are concentrated in functional regions despite PRDM9. Mol. Biol. Evol. 37, 1272–1294 (2020).
pubmed: 31926008
doi: 10.1093/molbev/msaa003
Kong, A. et al. A high-resolution recombination map of the human genome. Nat. Genet. 31, 241–247 (2002).
pubmed: 12053178
doi: 10.1038/ng917
Campbell, C. L., Bhérer, C., Morrow, B. E., Boyko, A. R. & Auton, A. A pedigree-based map of recombination in the domestic dog genome. G3 6, 3517–3524 (2016).
pubmed: 27591755
pmcid: 5100850
doi: 10.1534/g3.116.034678
Tortereau, F. et al. A high density recombination map of the pig reveals a correlation between sex-specific recombination and GC content. BMC Genomics 13, 586 (2012).
pubmed: 23152986
pmcid: 3499283
doi: 10.1186/1471-2164-13-586
Jensen-Seaman, M. I. et al. Comparative recombination rates in the rat, mouse, and human genomes. Genome Res. 14, 528–538 (2004).
pubmed: 15059993
pmcid: 383296
doi: 10.1101/gr.1970304
Baker, Z. et al. Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates. eLife 6, e24133 (2017).
pubmed: 28590247
pmcid: 5519329
doi: 10.7554/eLife.24133
Kuhl, L.-M. & Vader, G. Kinetochores, cohesin, and DNA breaks: Controlling meiotic recombination within pericentromeres. Yeast 36, 121–127 (2019).
pubmed: 30625250
doi: 10.1002/yea.3366
Termolino, P., Cremona, G., Consiglio, M. F. & Conicella, C. Insights into epigenetic landscape of recombination-free regions. Chromosoma 125, 301–308 (2016).
pubmed: 26801812
pmcid: 4830869
doi: 10.1007/s00412-016-0574-9
Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928–932 (2015).
pubmed: 26586757
pmcid: 4864528
doi: 10.1126/science.aad0843
Galtier, N., Piganeau, G., Mouchiroud, D. & Duret, L. GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 159, 907–911 (2001).
pubmed: 11693127
pmcid: 1461818
doi: 10.1093/genetics/159.2.907
Meunier, J. & Duret, L. Recombination drives the evolution of GC-content in the human genome. Mol. Biol. Evol. 21, 984–990 (2004).
pubmed: 14963104
doi: 10.1093/molbev/msh070
Lam, B. S. & Carroll, D. Tandemly repeated DNA sequences from Xenopus laevis. I. Studies on sequence organization and variation in satellite 1 DNA (741 base-pair repeat). J. Mol. Biol. 165, 567–585 (1983).
pubmed: 6189999
doi: 10.1016/S0022-2836(83)80267-8
Cohen, S., Menut, S. & Méchali, M. Regulated formation of extrachromosomal circular DNA molecules during development in Xenopus laevis. Mol. Cell. Biol. 19, 6682–6689 (1999).
pubmed: 10490607
pmcid: 84653
doi: 10.1128/MCB.19.10.6682
Ogiwara, I. V.-S. I. N. Es A new superfamily of vertebrate SINEs that are widespread in vertebrate genomes and retain a strongly conserved segment within each repetitive unit. Genome Res. 12, 316–324 (2002).
pubmed: 11827951
pmcid: 155270
doi: 10.1101/gr.212302
Rao, S. S. P. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
pubmed: 25497547
pmcid: 5635824
doi: 10.1016/j.cell.2014.11.021
Mascher, M. et al. A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427–433 (2017).
pubmed: 28447635
doi: 10.1038/nature22043
Hoencamp, C. et al. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 372, 984–989 (2021).
pubmed: 34045355
pmcid: 8172041
doi: 10.1126/science.abe2218
Rabl, C. Über Zelltheilung. Morphologisches Jahrbuch 10, 214–330 (1885).
Muller, H., Gil, J. Jr & Drinnenberg, I. A. The impact of centromeres on spatial genome architecture. Trends Genet. 35, 565–578 (2019).
pubmed: 31200946
doi: 10.1016/j.tig.2019.05.003
Sperling, K. & Lüdtke, E. K. Arrangement of prematurely condensed chromosomes in cultured cells and lymphocytes of the Indian muntjac. Chromosoma 83, 541–553 (1981).
pubmed: 7273958
doi: 10.1007/BF00328278
Cremer, T. et al. Rabl’s model of the interphase chromosome arrangement tested in Chinese hamster cells by premature chromosome condensation and laser-UV-microbeam experiments. Hum. Genet. 60, 46–56 (1982).
pubmed: 7076247
doi: 10.1007/BF00281263
Mathog, D., Hochstrasser, M., Gruenbaum, Y., Saumweber, H. & Sedat, J. Characteristic folding pattern of polytene chromosomes in Drosophila salivary gland nuclei. Nature 308, 414–421 (1984).
pubmed: 6424026
doi: 10.1038/308414a0
Stevens, T. J. et al. 3D structures of individual mammalian genomes studied by single-cell Hi-C. Nature 544, 59–64 (2017).
pubmed: 28289288
pmcid: 5385134
doi: 10.1038/nature21429
Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92–95 (2017).
pubmed: 28336562
pmcid: 5635820
doi: 10.1126/science.aal3327
Funabiki, H., Hagan, I., Uzawa, S. & Yanagida, M. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121, 961–976 (1993).
pubmed: 8388878
doi: 10.1083/jcb.121.5.961
Duan, Z. et al. A three-dimensional model of the yeast genome. Nature 465, 363–367 (2010).
pubmed: 20436457
pmcid: 2874121
doi: 10.1038/nature08973
Armstrong, S. J., Franklin, F. C. & Jones, G. H. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207–4217 (2001).
pubmed: 11739653
doi: 10.1242/jcs.114.23.4207
Santos, A. P. & Shaw, P. Interphase chromosomes and the Rabl configuration: does genome size matter? J. Microsc. 214, 201–206 (2004).
pubmed: 15102067
doi: 10.1111/j.0022-2720.2004.01324.x
Cowan, C. R., Carlton, P. M. & Cande, W. Z. The polar arrangement of telomeres in interphase and meiosis. Rabl organization and the bouquet. Plant Physiol. 125, 532–538 (2001).
pubmed: 11161011
pmcid: 1539364
doi: 10.1104/pp.125.2.532
Therizols, P., Duong, T., Dujon, B., Zimmer, C. & Fabre, E. Chromosome arm length and nuclear constraints determine the dynamic relationship of yeast subtelomeres. Proc. Natl. Acad. Sci. USA 107, 2025–2030 (2010).
pubmed: 20080699
pmcid: 2836701
doi: 10.1073/pnas.0914187107
Buttrick, G. J. et al. Nsk1 ensures accurate chromosome segregation by promoting association of kinetochores to spindle poles during anaphase B. Mol. Biol. Cell 22, 4486–4502 (2011).
pubmed: 21965289
pmcid: 3226469
doi: 10.1091/mbc.e11-07-0608
Dernburg, A. F. et al. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85, 745–759 (1996).
pubmed: 8646782
doi: 10.1016/S0092-8674(00)81240-4
Hiraoka, Y. et al. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J. Cell Biol. 120, 591–600 (1993).
pubmed: 8425892
doi: 10.1083/jcb.120.3.591
Marshall, W. F., Dernburg, A. F., Harmon, B., Agard, D. A. & Sedat, J. W. Specific interactions of chromatin with the nuclear envelope: positional determination within the nucleus in Drosophila melanogaster. Mol. Biol. Cell 7, 825–842 (1996).
pubmed: 8744953
pmcid: 275932
doi: 10.1091/mbc.7.5.825
Rowley, M. J. & Corces, V. G. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 19, 789–800 (2018).
pubmed: 30367165
doi: 10.1038/s41576-018-0060-8
Lu, J. Y. et al. Homotypic clustering of L1 and B1/Alu repeats compartmentalizes the 3D genome. Cell Res. 31, 613–630 (2021).
pubmed: 33514913
pmcid: 8169921
doi: 10.1038/s41422-020-00466-6
Fishman, V. et al. 3D organization of chicken genome demonstrates evolutionary conservation of topologically associated domains and highlights unique architecture of erythrocytes’ chromatin. Nucleic Acids Res. 47, 648–665 (2019).
pubmed: 30418618
doi: 10.1093/nar/gky1103
Kaaij, L. J. T., van der Weide, R. H., Ketting, R. F. & de Wit, E. Systemic loss and gain of chromatin architecture throughout zebrafish development. Cell Rep. 24, 1–10.e4 (2018).
pubmed: 29972771
pmcid: 6047509
doi: 10.1016/j.celrep.2018.06.003
Eagen, K. P., Aiden, E. L. & Kornberg, R. D. Polycomb-mediated chromatin loops revealed by a subkilobase-resolution chromatin interaction map. Proc. Natl. Acad. Sci. USA 114, 8764–8769 (2017).
pubmed: 28765367
pmcid: 5565414
doi: 10.1073/pnas.1701291114
Dong, P. et al. 3D chromatin architecture of large plant genomes determined by local A/B compartments. Mol. Plant 10, 1497–1509 (2017).
pubmed: 29175436
doi: 10.1016/j.molp.2017.11.005
Francke, U. 2012 William Allan Award: adventures in cytogenetics. Am. J. Hum. Genet. 92, 325–337 (2013).
pubmed: 23472754
pmcid: 3591841
doi: 10.1016/j.ajhg.2013.01.010
Uno, Y. et al. Diversity in the origins of sex chromosomes in anurans inferred from comparative mapping of sexual differentiation genes for three species of the Raninae and Xenopodinae. Chromosome Res. 16, 999–1011 (2008).
pubmed: 18850318
doi: 10.1007/s10577-008-1257-z
Uno, Y. et al. Inference of the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes from comparative gene mapping. PLoS ONE 7, e53027 (2012).
pubmed: 23300852
pmcid: 3534110
doi: 10.1371/journal.pone.0053027
Parada, L. A., McQueen, P. G., Munson, P. J. & Misteli, T. Conservation of relative chromosome positioning in normal and cancer cells. Curr. Biol. 12, 1692–1697 (2002).
pubmed: 12361574
doi: 10.1016/S0960-9822(02)01166-1
Parada, L. A., McQueen, P. G. & Misteli, T. Tissue-specific spatial organization of genomes. Genome Biol. 5, R44 (2004).
pubmed: 15239829
pmcid: 463291
doi: 10.1186/gb-2004-5-7-r44
Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289–293 (2009).
pubmed: 19815776
pmcid: 2858594
doi: 10.1126/science.1181369
Uno, Y., Nishida, C., Takagi, C., Ueno, N. & Matsuda, Y. Homoeologous chromosomes of Xenopus laevis are highly conserved after whole-genome duplication. Heredity 111, 430–436 (2013).
pubmed: 23820579
pmcid: 3806017
doi: 10.1038/hdy.2013.65
Kozubek, S. et al. The topological organization of chromosomes 9 and 22 in cell nuclei has a determinative role in the induction of t(9,22) translocations and in the pathogenesis of t(9,22) leukemias. Chromosoma 108, 426–435 (1999).
pubmed: 10654081
doi: 10.1007/s004120050394
Branco, M. R. & Pombo, A. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol. 4, e138 (2006).
pubmed: 16623600
pmcid: 1440941
doi: 10.1371/journal.pbio.0040138
Rosin, L. F. et al. Chromosome territory formation attenuates the translocation potential of cells. eLife 8, e49553 (2019).
pubmed: 31682226
pmcid: 6855801
doi: 10.7554/eLife.49553
Bright, A. R. et al. Combinatorial transcription factor activities on open chromatin induce embryonic heterogeneity in vertebrates. EMBO J. 40, e104913 (2021).
pubmed: 33555045
pmcid: 8090851
doi: 10.15252/embj.2020104913
Kakebeen, A. D., Chitsazan, A. D., Williams, M. C., Saunders, L. M. & Wills, A. E. Chromatin accessibility dynamics and single cell RNA-Seq reveal new regulators of regeneration in neural progenitors. eLife 9, e52648 (2020).
pubmed: 32338593
pmcid: 7250574
doi: 10.7554/eLife.52648
del Pino, E. M. et al. A comparative analysis of frog early development. Proc. Natl. Acad. Sci. USA 104, 11882–11888 (2007).
pubmed: 17606898
pmcid: 1924569
doi: 10.1073/pnas.0705092104
Vargas, A. & Del Pino, E. M. Analysis of cell size in the gastrula of ten frog species reveals a correlation of egg with cell sizes, and a conserved pattern of small cells in the marginal zone. J. Exp. Zool. B Mol. Dev. Evol. 328, 88–96 (2017).
pubmed: 27381278
doi: 10.1002/jez.b.22685
Oswald, P. et al. Locality, time and heterozygosity affect chytrid infection in yellow-bellied toads. Dis. Aquat. Organ. 142, 225–237 (2020).
pubmed: 33331290
doi: 10.3354/dao03543
Alford, R. A., Dixon, P. M. & Pechmann, J. H. Ecology. Global amphibian population declines. Nature 412, 499–500 (2001).
pubmed: 11484041
doi: 10.1038/35087658
Leung, B. et al. Clustered versus catastrophic global vertebrate declines. Nature 588, 267–271 (2020).
pubmed: 33208939
doi: 10.1038/s41586-020-2920-6
Gvoždík, V., Knytl, M., Zassi-Boulou, A-G, Fornaini, N. R. & Bergelová, B. Tetraploidy in the Boettger’s dwarf clawed frog (Pipidae: Hymenochirus boettgeri) from the Congo indicates non-conspecificity with the captive population, Zoological Journal of the Linnean Society zlad119 https://doi.org/10.1093/zoolinnean/zlad119 (2023).
Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M. & Jaffe, D. B. Direct determination of diploid genome sequences. Genome Res. 27, 757–767 (2017).
pubmed: 28381613
pmcid: 5411770
doi: 10.1101/gr.214874.116
Ye, C., Hill, C. M., Wu, S., Ruan, J. & Ma, Z. S. DBG2OLC: Efficient assembly of large genomes using long erroneous reads of the third generation sequencing technologies. Sci. Rep. 6, 31900 (2016).
pubmed: 27573208
pmcid: 5004134
doi: 10.1038/srep31900
Koren, S. et al. Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).
pubmed: 28298431
pmcid: 5411767
doi: 10.1101/gr.215087.116
Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
pubmed: 14759262
pmcid: 395750
doi: 10.1186/gb-2004-5-2-r12
Chakraborty, M., Baldwin-Brown, J. G., Long, A. D. & Emerson, J. J. Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage. Nucleic Acids Res. 44, e147–e147 (2016).
pubmed: 27458204
pmcid: 5100563
Boetzer, M., Henkel, C. V., Jansen, H. J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27, 578–579 (2011).
pubmed: 21149342
doi: 10.1093/bioinformatics/btq683
Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95–98 (2016).
pubmed: 27467249
pmcid: 5846465
doi: 10.1016/j.cels.2016.07.002
Tange, O. GNU Parallel 2018 (Lulu.com, 2018).
Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3, 99–101 (2016).
pubmed: 27467250
pmcid: 5596920
doi: 10.1016/j.cels.2015.07.012
Dudchenko, O., Shamim, M. S., Batra, S. S. & Durand, N. C. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. Preprint at https://www.biorxiv.org/content/10.1101/254797v1 (2018).
Chin, C.-S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2013).
pubmed: 23644548
doi: 10.1038/nmeth.2474
Walker, B. J. et al. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at https://arxiv.org/abs/1207.3907 (2012).
Shu, S., Rokhsar, D., Goodstein, D., Hayes, D. & Mitros, T. JGI Plant Genomics Gene Annotation Pipeline. https://www.osti.gov/biblio/1241222 (2014).
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 21572440
pmcid: 3571712
doi: 10.1038/nbt.1883
Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).
pubmed: 23845962
doi: 10.1038/nprot.2013.084
Smit, A. F. A. & Hubley, R. RepeatModeler Open-1.0. https://www.repeatmasker.org/RepeatModeler (2008–2015).
Jurka, J. et al. Repbase update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467 (2005).
pubmed: 16093699
doi: 10.1159/000084979
Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0. http://www.repeatmasker.org (2013–2015).
Chapman, J. A. et al. Meraculous: de novo genome assembly with short paired-end reads. PLoS ONE 6, e23501 (2011).
pubmed: 21876754
pmcid: 3158087
doi: 10.1371/journal.pone.0023501
Goltsman, E., Ho, I. & Rokhsar, D. Meraculous-2D: haplotype-sensitive assembly of highly heterozygous genomes. Preprint at https://arxiv.org/ftp/arxiv/papers/1703/1703.09852.pdf (2017).
Putnam, N. H. et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 26, 342–350 (2016).
pubmed: 26848124
pmcid: 4772016
doi: 10.1101/gr.193474.115
English, A. C. et al. Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS ONE 7, e47768 (2012).
pubmed: 23185243
pmcid: 3504050
doi: 10.1371/journal.pone.0047768
Kajitani, R. et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res. 24, 1384–1395 (2014).
pubmed: 24755901
pmcid: 4120091
doi: 10.1101/gr.170720.113
Mudd, A. B., Bredeson, J. V., Baum, R., Hockemeyer, D. & Rokhsar, D. S. Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution. Commun. Biol. 3, 1–10 (2020).
doi: 10.1038/s42003-020-1096-9
Paten, B. et al. Cactus: Algorithms for genome multiple sequence alignment. Genome Res. 21, 1512–1528 (2011).
pubmed: 21665927
pmcid: 3166836
doi: 10.1101/gr.123356.111
Blanchette, M. et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708–715 (2004).
pubmed: 15060014
pmcid: 383317
doi: 10.1101/gr.1933104
Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).
pubmed: 28387841
doi: 10.1093/molbev/msx116
Kiełbasa, S. M., Wan, R., Sato, K., Horton, P. & Frith, M. C. Adaptive seeds tame genomic sequence comparison. Genome Res. 21, 487–493 (2011).
pubmed: 21209072
pmcid: 3044862
doi: 10.1101/gr.113985.110
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).
pubmed: 27004904
pmcid: 8210823
doi: 10.1093/molbev/msw054
Tamura, K. et al. Estimating divergence times in large molecular phylogenies. Proc. Natl. Acad. Sci. USA 109, 19333–19338 (2012).
pubmed: 23129628
pmcid: 3511068
doi: 10.1073/pnas.1213199109
Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).
pubmed: 19541911
pmcid: 2752132
doi: 10.1101/gr.092759.109
Tang, H. et al. Synteny and collinearity in plant genomes. Science 320, 486–488 (2008).
pubmed: 18436778
doi: 10.1126/science.1153917
Dondoshansky, I. & Wolf, Y. Blastclust (NCBI Software Development Toolkit). ScienceOpen https://www.scienceopen.com/document?vid=b654ab9a-231d-410a-832d-37c7c7bc7165 (2002).
Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinforma. 10, 421 (2009).
doi: 10.1186/1471-2105-10-421
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Quinlan, A. R. BEDTools: the Swiss-army tool for genome feature analysis. Curr. Protoc. Bioinforma. 47, 11.12.1–34 (2014).
Bredeson, J. V. et al. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat. Biotechnol. 34, 562–570 (2016).
pubmed: 27088722
doi: 10.1038/nbt.3535
Gorbsky, G. J. et al. Developing immortal cell lines from Xenopus embryos, four novel cell lines derived from Xenopus tropicalis. Open Biol. 12, 1–9 (2022).
doi: 10.1098/rsob.220089
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Li, H. Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242
pmcid: 6137996
doi: 10.1093/bioinformatics/bty191
Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016).
pubmed: 27079975
pmcid: 4987876
doi: 10.1093/nar/gkw257
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982
pmcid: 2592715
doi: 10.1186/gb-2008-9-9-r137
Van Ooijen, J. W. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet. Res. 93, 343–349 (2011).
doi: 10.1017/S0016672311000279
Myers, S., Bottolo, L., Freeman, C., McVean, G. & Donnelly, P. A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321–324 (2005).
pubmed: 16224025
doi: 10.1126/science.1117196
Shifman, S. et al. A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol. 4, e395 (2006).
pubmed: 17105354
pmcid: 1635748
doi: 10.1371/journal.pbio.0040395
Varoquaux, N. et al. Accurate identification of centromere locations in yeast genomes using Hi-C. Nucleic Acids Res. 43, 5331–5339 (2015).
pubmed: 25940625
pmcid: 4477656
doi: 10.1093/nar/gkv424
Knight, P. A. & Ruiz, D. A fast algorithm for matrix balancing. IMA J. Numer. Anal. 33, 1029–1047 (2012).
doi: 10.1093/imanum/drs019
R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Austria http://www.R-project.org/ (2013).
Bredeson, J. V. et al. Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs. https://doi.org/10.5281/zenodo.8393403 (2023).