The little skate genome and the evolutionary emergence of wing-like fins.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
04 2023
Historique:
received: 23 03 2022
accepted: 21 02 2023
medline: 21 4 2023
pubmed: 13 4 2023
entrez: 12 4 2023
Statut: ppublish

Résumé

Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments

Identifiants

pubmed: 37046085
doi: 10.1038/s41586-023-05868-1
pii: 10.1038/s41586-023-05868-1
pmc: PMC10115646
doi:

Substances chimiques

Homeodomain Proteins 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

495-503

Subventions

Organisme : NIDCR NIH HHS
ID : R01 DE028599
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG003143
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG003988
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2023. The Author(s).

Références

Nakamura, T. et al. Molecular mechanisms underlying the exceptional adaptations of batoid fins. Proc. Natl Acad. Sci. USA 112, 15940–15945 (2015).
pubmed: 26644578 pmcid: 4702995 doi: 10.1073/pnas.1521818112
Turner, N. et al. The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids. Proc. Biol. Sci. 286, 20191571 (2019).
pubmed: 31662089 pmcid: 6842844
Shimeld, S. M. & Holland, P. W. Vertebrate innovations. Proc. Natl Acad. Sci. USA 97, 4449–4452 (2000).
pubmed: 10781042 pmcid: 34320 doi: 10.1073/pnas.97.9.4449
Simakov, O. et al. Deeply conserved synteny and the evolution of metazoan chromosomes. Sci. Adv. 8, eabi5884 (2022).
pubmed: 35108053 pmcid: 8809688 doi: 10.1126/sciadv.abi5884
Touceda-Suárez, M. et al. Ancient genomic regulatory blocks are a source for regulatory gene deserts in vertebrates after whole genome duplications. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msaa123 (2020).
Marlétaz, F. et al. Amphioxus functional genomics and the origins of vertebrate gene regulation. Nature 564, 64–70 (2018).
pubmed: 30464347 pmcid: 6292497 doi: 10.1038/s41586-018-0734-6
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).
pubmed: 22495300 pmcid: 3356448 doi: 10.1038/nature11082
Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381–385 (2012).
pubmed: 22495304 pmcid: 3555144 doi: 10.1038/nature11049
Berthelot, C., Muffato, M., Abecassis, J. & Roest Crollius, H. The 3D organization of chromatin explains evolutionary fragile genomic regions. Cell Rep. 10, 1913–1924 (2015).
pubmed: 25801028 doi: 10.1016/j.celrep.2015.02.046
Lupiáñez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012–1025 (2015).
pubmed: 25959774 pmcid: 4791538 doi: 10.1016/j.cell.2015.04.004
Real, F. M. et al. The mole genome reveals regulatory rearrangements associated with adaptive intersexuality. Science https://doi.org/10.1126/science.aaz2582 (2020).
Acemel, R. D. & Gómez-Skarmeta, J. L. Reprogramming nuclear architecture: just a TAD. Cell Stem Cell 24, 679–681 (2019).
pubmed: 31051129 doi: 10.1016/j.stem.2019.04.007
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
Stingo, V. & Rocco, L. Selachian cytogenetics: a review. Genetica 111, 329–347 (2001).
pubmed: 11841178 doi: 10.1023/A:1013747215866
Hirschberger, C., Sleight, V. A., Criswell, K. E., Clark, S. J. & Gillis, J. A. Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw. Mol. Biol. Evol. 38, 4187–4204 (2021).
pubmed: 33905525 pmcid: 8476176 doi: 10.1093/molbev/msab123
Chorostecki, U., Molina, M., Pryszcz, L. P. & Gabaldón, T. MetaPhOrs 2.0: integrative, phylogeny-based inference of orthology and paralogy across the tree of life. Nucleic Acids Res. 48, W553–W557 (2020).
pubmed: 32343307 pmcid: 7319458 doi: 10.1093/nar/gkaa282
Fuentes, D. et al. PhylomeDB V5: an expanding repository for genome-wide catalogues of annotated gene phylogenies. Nucleic Acids Res. 50, D1062–D1068 (2021).
pmcid: 8728271 doi: 10.1093/nar/gkab966
Irisarri, I. et al. Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nat. Ecol. Evol. 1, 1370–1378 (2017).
pubmed: 28890940 pmcid: 5584656 doi: 10.1038/s41559-017-0240-5
Hara, Y. et al. Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates. Nat. Ecol. Evol. 2, 1761–1771 (2018).
pubmed: 30297745 doi: 10.1038/s41559-018-0673-5
Kuraku, S. Shark and ray genomics for disentangling their morphological diversity and vertebrate evolution. Dev. Biol. 477, 262–272 (2021).
pubmed: 34102168 doi: 10.1016/j.ydbio.2021.06.001
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
Perry, B. W., Schield, D. R., Adams, R. H. & Castoe, T. A. Microchromosomes exhibit distinct features of vertebrate chromosome structure and function with underappreciated ramifications for genome evolution. Mol. Biol. Evol. 38, 904–910 (2021).
pubmed: 32986808 doi: 10.1093/molbev/msaa253
Simakov, O. et al. Deeply conserved synteny resolves early events in vertebrate evolution. Nat. Ecol. Evol. 4, 820–830 (2020).
pubmed: 32313176 pmcid: 7269912 doi: 10.1038/s41559-020-1156-z
Nakatani, Y., Takeda, H., Kohara, Y. & Morishita, S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 17, 1254–1265 (2007).
pubmed: 17652425 pmcid: 1950894 doi: 10.1101/gr.6316407
Nakatani, Y. et al. Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution. Nat. Commun. 12, 4489 (2021).
pubmed: 34301952 pmcid: 8302630 doi: 10.1038/s41467-021-24573-z
Thompson, A. W. et al. The bowfin genome illuminates the developmental evolution of ray-finned fishes. Nat. Genet. 53, 1373–1384 (2021).
pubmed: 34462605 pmcid: 8423624 doi: 10.1038/s41588-021-00914-y
Dalloul, R. A. et al. Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis. PLoS Biol. 8, e1000475 (2010).
pubmed: 20838655 pmcid: 2935454 doi: 10.1371/journal.pbio.1000475
Zhang, Y. et al. The white-spotted bamboo shark genome reveals chromosome rearrangements and fast-evolving immune genes of cartilaginous fish. iScience 23, 101754 (2020).
pubmed: 33251490 pmcid: 7677710 doi: 10.1016/j.isci.2020.101754
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
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
Rowley, M. J. et al. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell 67, 837–852 (2017).
pubmed: 28826674 pmcid: 5591081 doi: 10.1016/j.molcel.2017.07.022
Acemel, R. D. et al. A single three-dimensional chromatin compartment in amphioxus indicates a stepwise evolution of vertebrate Hox bimodal regulation. Nat. Genet. 48, 336–341 (2016).
pubmed: 26829752 doi: 10.1038/ng.3497
Gibson-Brown, J. J. et al. Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity. Mech. Dev. 56, 93–101 (1996).
pubmed: 8798150 doi: 10.1016/0925-4773(96)00514-X
Pradeepa, M. M., Sutherland, H. G., Ule, J., Grimes, G. R. & Bickmore, W. A. Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. PLoS Genet. 8, e1002717 (2012).
pubmed: 22615581 pmcid: 3355077 doi: 10.1371/journal.pgen.1002717
Onimaru, K. et al. Developmental hourglass and heterochronic shifts in fin and limb development. eLife 10, e62865 (2021).
pubmed: 33560225 pmcid: 7932699 doi: 10.7554/eLife.62865
Wang, J. S., Infante, C. R., Park, S. & Menke, D. B. PITX1 promotes chondrogenesis and myogenesis in mouse hindlimbs through conserved regulatory targets. Dev. Biol. 434, 186–195 (2018).
pubmed: 29273440 doi: 10.1016/j.ydbio.2017.12.013
DeLaurier, A., Schweitzer, R. & Logan, M. Pitx1 determines the morphology of muscle, tendon, and bones of the hindlimb. Dev. Biol. 299, 22–34 (2006).
pubmed: 16989801 doi: 10.1016/j.ydbio.2006.06.055
Swenson, J. D., Klomp, J., Fisher, R. A. & Crow, K. D. How the devil ray got its horns: the evolution and development of cephalic lobes in myliobatid stingrays (Batoidea: Myliobatidae). Front. Ecol. Evol. 6, 181 (2018).
doi: 10.3389/fevo.2018.00181
Barry, S. N. & Crow, K. D. The role of HoxA11 and HoxA13 in the evolution of novel fin morphologies in a representative batoid (Leucoraja erinacea). Evodevo 8, 24 (2017).
pubmed: 29214009 pmcid: 5709974 doi: 10.1186/s13227-017-0088-4
Lopez-Rios, J. et al. GLI3 constrains digit number by controlling both progenitor proliferation and BMP-dependent exit to chondrogenesis. Dev. Cell 22, 837–848 (2012).
pubmed: 22465667 pmcid: 4486391 doi: 10.1016/j.devcel.2012.01.006
Tanaka, M. Fins into limbs: autopod acquisition and anterior elements reduction by modifying gene networks involving 5′Hox, Gli3, and Shh. Dev. Biol. 413, 1–7 (2016).
pubmed: 26992366 doi: 10.1016/j.ydbio.2016.03.007
Bastida, M. F. et al. The formation of the thumb requires direct modulation of Gli3 transcription by Hoxa13. Proc. Natl Acad. Sci. USA 117, 1090–1096 (2020).
pubmed: 31896583 pmcid: 6969497 doi: 10.1073/pnas.1919470117
Amin, S. et al. Hoxa2 selectively enhances Meis binding to change a branchial arch ground state. Dev. Cell 32, 265–277 (2015).
pubmed: 25640223 pmcid: 4333904 doi: 10.1016/j.devcel.2014.12.024
Fromental-Ramain, C. et al. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997–3011 (1996).
pubmed: 8898214 doi: 10.1242/dev.122.10.2997
Sheth, R. et al. Distal limb patterning requires modulation of cis-regulatory activities by HOX13. Cell Rep. 17, 2913–2926 (2016).
pubmed: 27974206 pmcid: 5697718 doi: 10.1016/j.celrep.2016.11.039
Nakamura, T., Gehrke, A. R., Lemberg, J., Szymaszek, J. & Shubin, N. H. Digits and fin rays share common developmental histories. Nature 537, 225–228 (2016).
pubmed: 27533041 pmcid: 5161576 doi: 10.1038/nature19322
Freitas, R., Gómez-Marín, C., Wilson, J. M., Casares, F. & Gómez-Skarmeta, J. L. Hoxd13 contribution to the evolution of vertebrate appendages. Dev. Cell 23, 1219–1229 (2012).
pubmed: 23237954 doi: 10.1016/j.devcel.2012.10.015
Letelier, J. et al. The Shh/Gli3 gene regulatory network precedes the origin of paired fins and reveals the deep homology between distal fins and digits. Proc. Natl Acad. Sci. USA 118, e2100575118 (2021).
pubmed: 34750251 pmcid: 8673081 doi: 10.1073/pnas.2100575118
Bogdanović, O. et al. Active DNA demethylation at enhancers during the vertebrate phylotypic period. Nat. Genet. 48, 417–426 (2016).
pubmed: 26928226 pmcid: 5912259 doi: 10.1038/ng.3522
Hon, G. C. et al. Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat. Genet. 45, 1198–1206 (2013).
pubmed: 23995138 pmcid: 4095776 doi: 10.1038/ng.2746
Kragesteen, B. K. et al. Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis. Nat. Genet. 50, 1463–1473 (2018).
pubmed: 30262816 doi: 10.1038/s41588-018-0221-x
Venkatesh, B. et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174–179 (2014).
pubmed: 24402279 pmcid: 3964593 doi: 10.1038/nature12826
Krefting, J., Andrade-Navarro, M. A. & Ibn-Salem, J. Evolutionary stability of topologically associating domains is associated with conserved gene regulation. BMC Biol. 16, 87 (2018).
pubmed: 30086749 pmcid: 6091198 doi: 10.1186/s12915-018-0556-x
Schenkelaars, Q., Fierro-Constain, L., Renard, E. & Borchiellini, C. Retracing the path of planar cell polarity. BMC Evol. Biol. 16, 69 (2016).
pubmed: 27039172 pmcid: 4818920 doi: 10.1186/s12862-016-0641-0
Maxwell, E. E., Fröbisch, N. B. & Heppleston, A. C. Variability and conservation in late chondrichthyan development: ontogeny of the winter skate (Leucoraja ocellata). Anat. Rec. 291, 1079–1087 (2008).
doi: 10.1002/ar.20719
Carrier, J. C., Musick, J. A. & Heithaus, M. R. Biology of Sharks and Their Relatives 2nd edn (CRC Press, 2012).
Kvon, E. Z. et al. Progressive loss of function in a limb enhancer during snake evolution. Cell 167, 633–642 (2016).
pubmed: 27768887 pmcid: 5484524 doi: 10.1016/j.cell.2016.09.028
Leal, F. & Cohn, M. J. Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and HOXD enhancers. Curr. Biol. 26, 2966–2973 (2016).
pubmed: 27773569 doi: 10.1016/j.cub.2016.09.020
Lopez-Rios, J. et al. Attenuated sensing of SHH by Ptch1 underlies evolution of bovine limbs. Nature 511, 46–51 (2014).
pubmed: 24990743 doi: 10.1038/nature13289
Enny, A., Flaherty, K., Mori, S., Turner, N. & Nakamura, T. Developmental constraints on fin diversity. Dev. Growth Differ. 62, 311–325 (2020).
pubmed: 32396685 pmcid: 7383993 doi: 10.1111/dgd.12670
Gehrke, A. R. et al. Deep conservation of wrist and digit enhancers in fish. Proc. Natl Acad. Sci. USA 112, 803–808 (2015).
pubmed: 25535365 doi: 10.1073/pnas.1420208112
Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 11, 1432 (2020).
pubmed: 32188846 pmcid: 7080791 doi: 10.1038/s41467-020-14998-3
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
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).
pubmed: 26059717 doi: 10.1093/bioinformatics/btv351
Roach, M. J., Schmidt, S. A. & Borneman, A. R. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinform. 19, 460 (2018).
doi: 10.1186/s12859-018-2485-7
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
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
Kerpedjiev, P. et al. HiGlass: web-based visual exploration and analysis of genome interaction maps. Genome Biol. 19, 125 (2018).
pubmed: 30143029 pmcid: 6109259 doi: 10.1186/s13059-018-1486-1
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
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).
pubmed: 25690850 pmcid: 4643835 doi: 10.1038/nbt.3122
Niknafs, Y. S., Pandian, B., Iyer, H. K., Chinnaiyan, A. M. & Iyer, M. K. TACO produces robust multisample transcriptome assemblies from RNA-seq. Nat. Methods 14, 68–70 (2017).
pubmed: 27869815 doi: 10.1038/nmeth.4078
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
Wu, T. D., Reeder, J., Lawrence, M., Becker, G. & Brauer, M. J. GMAP and GSNAP for genomic sequence alignment: enhancements to speed, accuracy, and functionality. Methods Mol. Biol. 1418, 283–334 (2016).
pubmed: 27008021 doi: 10.1007/978-1-4939-3578-9_15
Venturini, L., Caim, S., Kaithakottil, G. G., Mapleson, D. L. & Swarbreck, D. Leveraging multiple transcriptome assembly methods for improved gene structure annotation. Gigascience 7, giy093 (2018).
pubmed: 30052957 pmcid: 6105091 doi: 10.1093/gigascience/giy093
Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439 (2006).
pubmed: 16845043 pmcid: 1538822 doi: 10.1093/nar/gkl200
Mapleson, D., Venturini, L., Kaithakottil, G. & Swarbreck, D. Efficient and accurate detection of splice junctions from RNA-seq with Portcullis. Gigascience 7, giy131 (2018).
pubmed: 30418570 pmcid: 6302956 doi: 10.1093/gigascience/giy131
Slater, G. S. C. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinform. 6, 31 (2005).
doi: 10.1186/1471-2105-6-31
Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).
pubmed: 18190707 pmcid: 2395244 doi: 10.1186/gb-2008-9-1-r7
Roth, A. C. J., Gonnet, G. H. & Dessimoz, C. Algorithm of OMA for large-scale orthology inference. BMC Bioinform. 9, 518 (2008).
doi: 10.1186/1471-2105-9-518
Marlétaz, F., Peijnenburg, K. T. C. A., Goto, T., Satoh, N. & Rokhsar, D. S. A new spiralian phylogeny places the enigmatic arrow worms among gnathiferans. Curr. Biol. 29, 312–318 (2019).
pubmed: 30639106 doi: 10.1016/j.cub.2018.11.042
Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).
pubmed: 22039361 pmcid: 3197634 doi: 10.1371/journal.pcbi.1002195
Katoh, K., Misawa, K., Kuma, K.-I. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).
pubmed: 12136088 pmcid: 135756 doi: 10.1093/nar/gkf436
Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).
pubmed: 20626897 pmcid: 3017758 doi: 10.1186/1471-2148-10-210
Lartillot, N., Lepage, T. & Blanquart, S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286–2288 (2009).
pubmed: 19535536 doi: 10.1093/bioinformatics/btp368
Benton, M. J., Donoghue, P. C. J. & Asher, R. J. in The Timetree Of Life (ed. Kumar, S. B. H.) 35–86 (Oxford Univ. Press, 2009).
Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017).
pubmed: 29035372 doi: 10.1038/nbt.3988
Derelle, R., Philippe, H. & Colbourne, J. K. Broccoli: combining phylogenetic and network analyses for orthology assignment. Mol. Biol. Evol. 37, 3389–3396 (2020).
pubmed: 32602888 doi: 10.1093/molbev/msaa159
Morel, B., Kozlov, A. M., Stamatakis, A. & Szöllősi, G. J. GeneRax: a tool for species-tree-aware maximum likelihood-based gene family tree inference under gene duplication, transfer, and loss. Mol. Biol. Evol. 37, 2763–2774 (2020).
pubmed: 32502238 pmcid: 8312565 doi: 10.1093/molbev/msaa141
Belaghzal, H., Dekker, J. & Gibcus, J. H. Hi-C 2.0: an optimized Hi-C procedure for high-resolution genome-wide mapping of chromosome conformation. Methods 123, 56–65 (2017).
pubmed: 28435001 pmcid: 5522765 doi: 10.1016/j.ymeth.2017.04.004
Franke, M. et al. CTCF knockout in zebrafish induces alterations in regulatory landscapes and developmental gene expression. Nat. Commun. 12, 5415 (2021).
pubmed: 34518536 pmcid: 8438036 doi: 10.1038/s41467-021-25604-5
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
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
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
Kruse, K., Hug, C. B. & Vaquerizas, J. M. FAN-C: a feature-rich framework for the analysis and visualisation of chromosome conformation capture data. Genome Biol. 21, 303 (2020).
pubmed: 33334380 pmcid: 7745377 doi: 10.1186/s13059-020-02215-9
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033
Crane, E. et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240–244 (2015).
pubmed: 26030525 pmcid: 4498965 doi: 10.1038/nature14450
Frith, M. C. et al. Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res. 32, 1372–1381 (2004).
pubmed: 14988425 pmcid: 390287 doi: 10.1093/nar/gkh299
Grant, C. E., Bailey, T. L. & Noble, W. S. FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018 (2011).
pubmed: 21330290 pmcid: 3065696 doi: 10.1093/bioinformatics/btr064
Barrows, T. C. A. profileplyr (Bioconductor, 2019); https://doi.org/10.18129/B9.BIOC.PROFILEPLYR
Wolff, J., Backofen, R. & Grüning, B. Loop detection using Hi-C data with HiCExplorer. Gigascience 11, giac061 (2022).
pubmed: 35809047 pmcid: 9270730 doi: 10.1093/gigascience/giac061
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308 doi: 10.1093/bioinformatics/btp616
Mumbach, M. R. et al. HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13, 919–922 (2016).
pubmed: 27643841 pmcid: 5501173 doi: 10.1038/nmeth.3999
Serra, F. et al. Automatic analysis and 3D-modelling of Hi-C data using TADbit reveals structural features of the fly chromatin colors. PLoS Comput. Biol. 13, e1005665 (2017).
pubmed: 28723903 pmcid: 5540598 doi: 10.1371/journal.pcbi.1005665
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
Bhattacharyya, S., Chandra, V., Vijayanand, P. & Ay, F. Identification of significant chromatin contacts from HiChIP data by FitHiChIP. Nat. Commun. 10, 4221 (2019).
pubmed: 31530818 pmcid: 6748947 doi: 10.1038/s41467-019-11950-y
Lawrence, M. et al. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 9, e1003118 (2013).
pubmed: 23950696 pmcid: 3738458 doi: 10.1371/journal.pcbi.1003118
Ewels, P. A. et al. The nf-core framework for community-curated bioinformatics pipelines. Nat. Biotechnol. 38, 276–278 (2020).
pubmed: 32055031 doi: 10.1038/s41587-020-0439-x
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281 pmcid: 4302049 doi: 10.1186/s13059-014-0550-8
Alexa, A. & Rahnenfuhrer, J. topGO; https://doi.org/10.18129/B9.BIOC.TOPGO (Bioconductor, 2017).
Fernández-Miñán, A., Bessa, J., Tena, J. J. & Gómez-Skarmeta, J. L. Assay for transposase-accessible chromatin and circularized chromosome conformation capture, two methods to explore the regulatory landscapes of genes in zebrafish. Methods Cell. Biol. 135, 413–430 (2016).
pubmed: 27443938 doi: 10.1016/bs.mcb.2016.02.008
Di Tommaso, P. et al. Nextflow enables reproducible computational workflows. Nat. Biotechnol. 35, 316–319 (2017).
pubmed: 28398311 doi: 10.1038/nbt.3820
Irimia, M. et al. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res. 22, 2356–2367 (2012).
pubmed: 22722344 pmcid: 3514665 doi: 10.1101/gr.139725.112
Harris, R. S. Improved Pairwise Alignment of Genomic DNA. PhD thesis, Pennsylvania State Univ. (2007).
Hiller, M. et al. Computational methods to detect conserved non-genic elements in phylogenetically isolated genomes: application to zebrafish. Nucleic Acids Res. 41, e151 (2013).
pubmed: 23814184 pmcid: 3753653 doi: 10.1093/nar/gkt557
Kent, W. J., Baertsch, R., Hinrichs, A., Miller, W. & Haussler, D. Evolution’s cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl Acad. Sci. USA 100, 11484–11489 (2003).
pubmed: 14500911 pmcid: 208784 doi: 10.1073/pnas.1932072100
Suarez, H. G., Langer, B. E., Ladde, P. & Hiller, M. chainCleaner improves genome alignment specificity and sensitivity. Bioinformatics 33, 1596–1603 (2017).
pubmed: 28108446 doi: 10.1093/bioinformatics/btx024
Yu, G. & He, Q.-Y. ReactomePA: an R/Bioconductor package for reactome pathway analysis and visualization. Mol. Biosyst. 12, 477–479 (2016).
pubmed: 26661513 doi: 10.1039/C5MB00663E
Yu, G., Wang, L.-G., Han, Y. & He, Q.-Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16, 284–287 (2012).
pubmed: 22455463 pmcid: 3339379 doi: 10.1089/omi.2011.0118
Dahn, R. D., Davis, M. C., Pappano, W. N. & Shubin, N. H. Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning. Nature 445, 311–314 (2006).
pubmed: 17187056 doi: 10.1038/nature05436
Olsen, A. M. & Westneat, M. W. StereoMorph: an R package for the collection of 3D landmarks and curves using a stereo camera set‐up. Methods Ecol. Evol. 6, 351–356 (2015).
doi: 10.1111/2041-210X.12326
Baken, E. K., Collyer, M. L., Kaliontzopoulou, A. & Adams, D. C. geomorph v4.0 and gmShiny: Enhanced analytics and a new graphical interface for a comprehensive morphometric experience. Methods Ecol. Evol. 12, 2355–2363 (2021).
Adams, D., Collyer, M., Kaliontzopoulou, A. & Baken, E. geomorph: geometric morphometric analyses of 2D/3D landmark data. R package version 4.0.1 (2021).
Suster, M. L., Abe, G., Schouw, A. & Kawakami, K. Transposon-mediated BAC transgenesis in zebrafish. Nat. Protoc. 6, 1998–2021 (2011).
pubmed: 22134125 doi: 10.1038/nprot.2011.416
Huerta-Cepas, J., Capella-Gutierrez, S., Pryszcz, L. P., Marcet-Houben, M. & Gabaldon, T. PhylomeDB v4: zooming into the plurality of evolutionary histories of a genome. Nucleic Acids Res. 42, D897–D902 (2014).
pubmed: 24275491 doi: 10.1093/nar/gkt1177
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147 pmcid: 390337 doi: 10.1093/nar/gkh340
Katoh, K., Kuma, K., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005).
pubmed: 15661851 pmcid: 548345 doi: 10.1093/nar/gki198
Lassmann, T. & Sonnhammer, E. L. Kalign—an accurate and fast multiple sequence alignment algorithm. BMC Bioinform. 6, 298 (2005).
doi: 10.1186/1471-2105-6-298
Wallace, I. M., O’Sullivan, O., Higgins, D. G. & Notredame, C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res. 34, 1692–1699 (2006).
pubmed: 16556910 pmcid: 1410914 doi: 10.1093/nar/gkl091
Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
pubmed: 19505945 pmcid: 2712344 doi: 10.1093/bioinformatics/btp348
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430 doi: 10.1093/molbev/msu300
Wehe, A., Bansal, M. S., Burleigh, J. G. & Eulenstein, O. DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony. Bioinformatics 24, 1540–1541 (2008).
pubmed: 18474508 doi: 10.1093/bioinformatics/btn230
Urich, M. A., Nery, J. R., Lister, R., Schmitz, R. J. & Ecker, J. R. MethylC-seq library preparation for base-resolution whole-genome bisulfite sequencing. Nat. Protoc. 10, 475–483 (2015).
pubmed: 25692984 pmcid: 4465251 doi: 10.1038/nprot.2014.114
Peat, J. R., Ortega-Recalde, O., Kardailsky, O. & Hore, T. A. The elephant shark methylome reveals conservation of epigenetic regulation across jawed vertebrates. F1000Research 6, 526 (2017).
pubmed: 28580133 pmcid: 5437953 doi: 10.12688/f1000research.11281.1
Skvortsova, K. et al. Retention of paternal DNA methylome in the developing zebrafish germline. Nat. Commun. 10, 3054 (2019).
pubmed: 31296860 pmcid: 6624265 doi: 10.1038/s41467-019-10895-6
Chen, H., Smith, A. D. & Chen, T. WALT: fast and accurate read mapping for bisulfite sequencing. Bioinformatics 32, 3507–3509 (2016).
pubmed: 27466624 pmcid: 5181568 doi: 10.1093/bioinformatics/btw490
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
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187–W191 (2014).
pubmed: 24799436 pmcid: 4086134 doi: 10.1093/nar/gku365

Auteurs

Ferdinand Marlétaz (F)

Centre for Life's Origin and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK. ferdinand.marletaz@gmail.com.
Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Japan. ferdinand.marletaz@gmail.com.

Elisa de la Calle-Mustienes (E)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Rafael D Acemel (RD)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.
Epigenetics and Sex Development Group, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany.

Christina Paliou (C)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Silvia Naranjo (S)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Pedro Manuel Martínez-García (PM)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Ildefonso Cases (I)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Victoria A Sleight (VA)

Department of Zoology, University of Cambridge, Cambridge, UK.
School of Biological Sciences, University of Aberdeen, Aberdeen, UK.

Christine Hirschberger (C)

Department of Zoology, University of Cambridge, Cambridge, UK.

Marina Marcet-Houben (M)

Barcelona Supercomputing Centre (BCS-CNS), Barcelona, Spain.
Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain.

Dina Navon (D)

Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, USA.

Ali Andrescavage (A)

Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, USA.

Ksenia Skvortsova (K)

Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
Faculty of Medicine, St Vincent's Clinical School, University of New South Wales, Sydney, New South Wales, Australia.

Paul Edward Duckett (PE)

Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.

Álvaro González-Rajal (Á)

Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
Faculty of Medicine, St Vincent's Clinical School, University of New South Wales, Sydney, New South Wales, Australia.

Ozren Bogdanovic (O)

Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia.

Johan H Gibcus (JH)

Department of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA, USA.

Liyan Yang (L)

Department of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA, USA.

Lourdes Gallardo-Fuentes (L)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Ismael Sospedra (I)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Javier Lopez-Rios (J)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Fabrice Darbellay (F)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Department of Genetic Medicine and Development, Faculty of Medicine, University of Geneva, Geneva, Switzerland.

Axel Visel (A)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
US Department of Energy Joint Genome Institute, Berkeley, CA, USA.
School of Natural Sciences, University of California, Merced, CA, USA.

Job Dekker (J)

Department of Systems Biology, University of Massachusetts Chan Medical School, Worcester, MA, USA.
Howard Hughes Medical Institute, Chevy Chase, MD, USA.

Neil Shubin (N)

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.

Toni Gabaldón (T)

Barcelona Supercomputing Centre (BCS-CNS), Barcelona, Spain.
Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain.
Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain.
CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, Madrid, Spain.

Tetsuya Nakamura (T)

Department of Genetics, Rutgers the State University of New Jersey, Piscataway, NJ, USA. nakamura@dls.rutgers.edu.

Juan J Tena (JJ)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain. jjtenagu@upo.es.

Darío G Lupiáñez (DG)

Epigenetics and Sex Development Group, Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany. Dario.Lupianez@mdc-berlin.de.

Daniel S Rokhsar (DS)

Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Japan. dsrokhsar@gmail.com.
Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA. dsrokhsar@gmail.com.
Chan-Zuckerberg Biohub, San Francisco, CA, USA. dsrokhsar@gmail.com.

José Luis Gómez-Skarmeta (JL)

Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide/Junta de Andalucía, Seville, Spain.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH