The bowfin genome illuminates the developmental evolution of ray-finned fishes.
Journal
Nature genetics
ISSN: 1546-1718
Titre abrégé: Nat Genet
Pays: United States
ID NLM: 9216904
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
received:
13
10
2020
accepted:
13
07
2021
pubmed:
1
9
2021
medline:
15
10
2021
entrez:
31
8
2021
Statut:
ppublish
Résumé
The bowfin (Amia calva) is a ray-finned fish that possesses a unique suite of ancestral and derived phenotypes, which are key to understanding vertebrate evolution. The phylogenetic position of bowfin as a representative of neopterygian fishes, its archetypical body plan and its unduplicated and slowly evolving genome make bowfin a central species for the genomic exploration of ray-finned fishes. Here we present a chromosome-level genome assembly for bowfin that enables gene-order analyses, settling long-debated neopterygian phylogenetic relationships. We examine chromatin accessibility and gene expression through bowfin development to investigate the evolution of immune, scale, respiratory and fin skeletal systems and identify hundreds of gene-regulatory loci conserved across vertebrates. These resources connect developmental evolution among bony fishes, further highlighting the bowfin's importance for illuminating vertebrate biology and diversity in the genomic era.
Identifiants
pubmed: 34462605
doi: 10.1038/s41588-021-00914-y
pii: 10.1038/s41588-021-00914-y
pmc: PMC8423624
doi:
Substances chimiques
Chromatin
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1373-1384Subventions
Organisme : NIH HHS
ID : R01 OD011116
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021. The Author(s).
Références
Jarvik, J. Basic Structure and Evolution of Vertebrates Vol. 1 (Academic Press, 1980).
Burr, B. M. & Bennett, M. G. in Freshwater Fishes of North America 1 (eds Warren, M. L. & Burr, M. G.) (John Hopkins University Press, 2014).
Nelson, J. S. Fishes of the World 4th edn (John Wiley, 2006).
Near, T. J. et al. Resolution of ray-finned fish phylogeny and timing of diversification. Proc. Natl Acad. Sci. USA 109, 13698–13703 (2012).
pubmed: 22869754
pmcid: 3427055
doi: 10.1073/pnas.1206625109
Betancur, R. R. et al. The tree of life and a new classification of bony fishes. PLoS Curr. 5, ecurrents.tol.53ba26640df0ccaee75bb165c8c26288 (2013).
Faircloth, B. C., Sorenson, L., Santini, F. & Alfaro, M. E. A phylogenomic perspective on the radiation of ray-finned fishes based upon targeted sequencing of ultraconserved elements (UCEs). PLoS ONE 8, e65923 (2013).
pubmed: 23824177
pmcid: 3688804
doi: 10.1371/journal.pone.0065923
Braasch, I. et al. The spotted gar genome illuminates vertebrate evolution and facilitates human–teleost comparisons. Nat. Genet. 48, 427–437 (2016).
pubmed: 26950095
pmcid: 4817229
doi: 10.1038/ng.3526
Hughes, L. C. et al. Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data. Proc. Natl Acad. Sci. USA 115, 6249–6254 (2018).
pubmed: 29760103
pmcid: 6004478
doi: 10.1073/pnas.1719358115
Clarke, J. T., Lloyd, G. T. & Friedman, M. Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group. Proc. Natl Acad. Sci. USA 113, 11531–11536 (2016).
pubmed: 27671652
pmcid: 5068283
doi: 10.1073/pnas.1607237113
Braasch, I. et al. A new model army: emerging fish models to study the genomics of vertebrate Evo-Devo. J. Exp. Zool. B Mol. Dev. Evol. 324, 316–341 (2015).
pubmed: 25111899
doi: 10.1002/jez.b.22589
Du, K. et al. The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization. Nat. Ecol. Evol. 4, 841–852 (2020).
pubmed: 32231327
pmcid: 7269910
doi: 10.1038/s41559-020-1166-x
Bi, X. et al. Tracing the genetic footprints of vertebrate landing in non-teleost ray-finned fishes. Cell 184, 1377–1391 (2021).
pubmed: 33545088
doi: 10.1016/j.cell.2021.01.046
Cheng, P. et al. The American paddlefish genome provides novel insights into chromosomal evolution and bone mineralization in early vertebrates. Mol. Biol. Evol. 38, 1595–1607 (2020).
pmcid: 8042750
doi: 10.1093/molbev/msaa326
Braasch, I. & Postlethwait, J. H. in Polyploidy and Genome Evolution (eds Soltis, P. S. & Soltis, D. E.) Ch. 17, 341–383 (Springer, 2012).
Ravi, V. & Venkatesh, B. The divergent genomes of teleosts. Annu. Rev. Anim. Biosci. 6, 47–68 (2018).
pubmed: 29447475
doi: 10.1146/annurev-animal-030117-014821
Takezaki, N. Global rate variation in bony vertebrates. Genome Biol. Evol. 10, 1803–1815 (2018).
pubmed: 29931060
pmcid: 6055543
doi: 10.1093/gbe/evy125
Patterson, C. in Interrelationships of Fishes Vol. Supplement 1 (eds Greenwood, P. H., Miles, R. S. & Patterson, C.) 233–305 (Academic Press, 1973).
Grande, L. An Empirical Synthetic Pattern Study of Gars (Lepisosteiformes) and Closely Related Species, Based Mostly on Skeletal Anatomy. The Resurrection of Holostei 1–863 (American Society of Ichthyologists and Herpetologists, 2010).
Sallan, L. C. Major issues in the origins of ray-finned fish (Actinopterygii) biodiversity. Biol. Rev. Camb. Philos. Soc. 89, 950–971 (2014).
pubmed: 24612207
doi: 10.1111/brv.12086
Grande, L. & Bemis, W. E. A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history. J. Vertebr. Paleontol. 18, 1–696 (1998).
doi: 10.1080/02724634.1998.10011114
Majtanova, Z., Symonova, R., Arias-Rodriguez, L., Sallan, L. & Rab, P. “Holostei versus Halecostomi” problem: insight from cytogenetics of ancient nonteleost actinopterygian fish, bowfin Amia calva. J. Exp. Zool. B Mol. Dev. Evol. 328, 620–628 (2017).
pubmed: 28074622
doi: 10.1002/jez.b.22720
Litman, G. W., Frommel, D., Finstad, J. & Good, R. A. The evolution of the immune reponse. IX. Immunoglobulins of the bowfin: purification and characterization. J. Immunol. 106, 747–754 (1971).
pubmed: 4100690
doi: 10.4049/jimmunol.106.3.747
Sire, J. Y., Donoghue, P. C. & Vickaryous, M. K. Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. J. Anat. 214, 409–440 (2009).
pubmed: 19422423
pmcid: 2736117
doi: 10.1111/j.1469-7580.2009.01046.x
Funk, E., Lencer, E. & McCune, A. Dorsoventral inversion of the air-filled organ (lungs, gas bladder) in vertebrates: RNAsequencing of laser capture microdissected embryonic tissue. J. Exp. Zool. B Mol. Dev. Evol. 334, 325–338 (2020).
pubmed: 32864827
pmcid: 8094346
doi: 10.1002/jez.b.22998
Funk, E. C., Breen, C., Sanketi, B. D., Kurpios, N. & McCune, A. Changes in Nkx2.1, Sox2, Bmp4 and Bmp16 expression underlying the lung-to-gas bladder evolutionary transition in ray-finned fishes. Evol. Dev. 22, 384–402 (2020).
pubmed: 33463017
pmcid: 8013215
doi: 10.1111/ede.12354
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
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
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
Ohno, S. et al. Microchromosomes in holocephalian, chondrostean and holostean fishes. Chromosoma 26, 35–40 (1969).
pubmed: 5799423
doi: 10.1007/BF00319498
Pasquier, J. et al. Gene evolution and gene expression after whole genome duplication in fish: the PhyloFish database. BMC Genomics 17, 368 (2016).
pubmed: 27189481
pmcid: 4870732
doi: 10.1186/s12864-016-2709-z
Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12, 491 (2011).
pubmed: 22192575
pmcid: 3280279
doi: 10.1186/1471-2105-12-491
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).
pubmed: 31727128
pmcid: 6857279
doi: 10.1186/s13059-019-1832-y
Feron, R. et al. RADSex: a computational workflow to study sex determination using restriction site-associated DNA sequencing data. Mol. Ecol. Resour. 21, 1715–1731 (2021).
pubmed: 33590960
doi: 10.1111/1755-0998.13360
Sacerdot, C., Louis, A., Bon, C., Berthelot, C. & Roest Crollius, H. Chromosome evolution at the origin of the ancestral vertebrate genome. Genome Biol. 19, 166 (2018).
pubmed: 30333059
pmcid: 6193309
doi: 10.1186/s13059-018-1559-1
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
Moret, B. M. E., Tang, J., Wang, L.-S. & Warnow, T. Steps toward accurate reconstructions of phylogenies from gene-order data. J. Comput. Syst. Sci. 65, 508–525 (2002).
doi: 10.1016/S0022-0000(02)00007-7
Lin, Y., Hu, F., Tang, J. & Moret, B. M. Maximum likelihood phylogenetic reconstruction from high-resolution whole-genome data and a tree of 68 eukaryotes. Pac. Symp. Biocomput. 2013, 285–296 (2013).
Emms, D. M. & Kelly, S. STAG: species tree inference from all genes. Preprint at bioRxiv https://doi.org/10.1101/267914 (2018).
Wcisel, D. J., Ota, T., Litman, G. W. & Yoder, J. A. Spotted gar and the evolution of innate immune receptors. J. Exp. Zool. B Mol. Dev. Evol. 328, 666–684 (2017).
pubmed: 28544607
pmcid: 6876127
doi: 10.1002/jez.b.22738
Trowsdale, J. The MHC, disease and selection. Immunol. Lett. 137, 1–8 (2011).
pubmed: 21262263
doi: 10.1016/j.imlet.2011.01.002
Ohta, Y. et al. Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc. Natl Acad. Sci. USA 97, 4712–4717 (2000).
pubmed: 10781076
pmcid: 18298
doi: 10.1073/pnas.97.9.4712
Grimholt, U. MHC and evolution in teleosts. Biology 5, 6 (2016).
pmcid: 4810163
doi: 10.3390/biology5010006
Flajnik, M. F. A cold-blooded view of adaptive immunity. Nat. Rev. Immunol. 18, 438–453 (2018).
pubmed: 29556016
pmcid: 6084782
doi: 10.1038/s41577-018-0003-9
Fillatreau, S. et al. The astonishing diversity of Ig classes and B cell repertoires in teleost fish. Front. Immunol. 4, 28 (2013).
pubmed: 23408183
pmcid: 3570791
doi: 10.3389/fimmu.2013.00028
Mirete-Bachiller, S., Olivieri, D. N. & Gambon-Deza, F. Immunoglobulin T genes in Actinopterygii. Fish Shellfish Immunol. 108, 86–93 (2021).
pubmed: 33279606
doi: 10.1016/j.fsi.2020.11.027
Aderem, A. & Ulevitch, R. J. Toll-like receptors in the induction of the innate immune response. Nature 406, 782–787 (2000).
pubmed: 10963608
doi: 10.1038/35021228
Fitzgerald, K. A. & Kagan, J. C. Toll-like receptors and the control of immunity. Cell 180, 1044–1066 (2020).
pubmed: 32164908
doi: 10.1016/j.cell.2020.02.041
Aoki, T., Hikima, J., Hwang, S. D. & Jung, T. S. Innate immunity of finfish: primordial conservation and function of viral RNA sensors in teleosts. Fish Shellfish Immunol. 35, 1689–1702 (2013).
pubmed: 23462146
doi: 10.1016/j.fsi.2013.02.005
Kawasaki, K. et al. SCPP genes and their relatives in gar: rapid expansion of mineralization genes in Osteichthyans. J. Exp. Zool. B Mol. Dev. Evol. 328, 645–665 (2017).
pubmed: 28643450
doi: 10.1002/jez.b.22755
Qu, Q., Haitina, T., Zhu, M. & Ahlberg, P. E. New genomic and fossil data illuminate the origin of enamel. Nature 526, 108–111 (2015).
pubmed: 26416752
doi: 10.1038/nature15259
Kawasaki, K. et al. Coevolution of enamel, ganoin, enameloid, and their matrix SCPP genes in osteichthyans. iScience 24, 102023 (2021).
pubmed: 33506188
pmcid: 7814152
doi: 10.1016/j.isci.2020.102023
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
pubmed: 24097267
pmcid: 3959825
doi: 10.1038/nmeth.2688
Ballard, W. W. Stages and rates of normal development in the holostean fish, Amia calva. J. Exp. Zool. 238, 337–354 (1986).
doi: 10.1002/jez.1402380308
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
pubmed: 20513432
pmcid: 2898526
doi: 10.1016/j.molcel.2010.05.004
Armstrong, J. et al. Progressive Cactus is a multiple-genome aligner for the thousand-genome era. Nature 587, 246–251 (2020).
pubmed: 33177663
pmcid: 7673649
doi: 10.1038/s41586-020-2871-y
Visel, A., Minovitsky, S., Dubchak, I. & Pennacchio, L. A. VISTA Enhancer Browser—a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88–D92 (2007).
pubmed: 17130149
doi: 10.1093/nar/gkl822
Yuan, X. et al. Heart enhancers with deeply conserved regulatory activity are established early in zebrafish development. Nat. Commun. 9, 4977 (2018).
pubmed: 30478328
pmcid: 6255839
doi: 10.1038/s41467-018-07451-z
Abbasi, A. A. et al. Human intronic enhancers control distinct sub-domains of Gli3 expression during mouse CNS and limb development. BMC Dev. Biol. 10, 44 (2010).
pubmed: 20426846
pmcid: 2875213
doi: 10.1186/1471-213X-10-44
Adachi, N., Robinson, M., Goolsbee, A. & Shubin, N. H. Regulatory evolution of Tbx5 and the origin of paired appendages. Proc. Natl Acad. Sci. USA 113, 10115–10120 (2016).
pubmed: 27503876
pmcid: 5018757
doi: 10.1073/pnas.1609997113
Menke, D. B., Guenther, C. & Kingsley, D. M. Dual hindlimb control elements in the Tbx4 gene and region-specific control of bone size in vertebrate limbs. Development 135, 2543–2553 (2008).
pubmed: 18579682
doi: 10.1242/dev.017384
Zhang, W. et al. Spatial–temporal targeting of lung-specific mesenchyme by a Tbx4 enhancer. BMC Biol. 11, 111 (2013).
pubmed: 24225400
pmcid: 3907025
doi: 10.1186/1741-7007-11-111
Vernimmen, D. Uncovering enhancer functions using the α-globin locus. PLoS Genet. 10, e1004668 (2014).
pubmed: 25330308
pmcid: 4199490
doi: 10.1371/journal.pgen.1004668
Huang, P. et al. Comparative analysis of three-dimensional chromosomal architecture identifies a novel fetal hemoglobin regulatory element. Genes Dev. 31, 1704–1713 (2017).
pubmed: 28916711
pmcid: 5647940
doi: 10.1101/gad.303461.117
Ulianov, S. V. et al. Activation of the α-globin gene expression correlates with dramatic upregulation of nearby non-globin genes and changes in local and large-scale chromatin spatial structure. Epigenetics Chromatin 10, 35 (2017).
pubmed: 28693562
pmcid: 5504709
doi: 10.1186/s13072-017-0142-4
Pijuan-Sala, B. et al. Single-cell chromatin accessibility maps reveal regulatory programs driving early mouse organogenesis. Nat. Cell Biol. 22, 487–497 (2020).
pubmed: 32231307
pmcid: 7145456
doi: 10.1038/s41556-020-0489-9
Tena, J. J. et al. Comparative epigenomics in distantly related teleost species identifies conserved cis-regulatory nodes active during the vertebrate phylotypic period. Genome Res. 24, 1075–1085 (2014).
pubmed: 24709821
pmcid: 4079964
doi: 10.1101/gr.163915.113
Li, Y. et al. Dynamic transcriptional and chromatin accessibility landscape of medaka embryogenesis. Genome Res. 30, 924–937 (2020).
pubmed: 32591361
pmcid: 7370878
doi: 10.1101/gr.258871.119
Graham, J. B. Air-Breathing Fishes (Academic Press, 1997).
Meyer, A. et al. Giant lungfish genome elucidates the conquest of land by vertebrates. Nature 590, 284–289 (2021).
pubmed: 33461212
pmcid: 7875771
doi: 10.1038/s41586-021-03198-8
Wang, K. et al. African lungfish genome sheds light on the vertebrate water-to-land transition. Cell 184, 1362–1376 (2021).
pubmed: 33545087
doi: 10.1016/j.cell.2021.01.047
Kuraku, S. et al. Noncanonical role of Hox14 revealed by its expression patterns in lamprey and shark. Proc. Natl Acad. Sci. USA 105, 6679–6683 (2008).
pubmed: 18448683
pmcid: 2373320
doi: 10.1073/pnas.0710947105
Powers, T. P. & Amemiya, C. T. Evidence for a Hox14 paralog group in vertebrates. Curr. Biol. 14, R183–R184 (2004).
pubmed: 15028231
doi: 10.1016/j.cub.2004.02.015
Tulenko, F. J. et al. HoxD expression in the fin-fold compartment of basal gnathostomes and implications for paired appendage evolution. Sci. Rep. 6, 22720 (2016).
pubmed: 26940624
pmcid: 4778128
doi: 10.1038/srep22720
Zhang, J. et al. Loss of fish actinotrichia proteins and the fin-to-limb transition. Nature 466, 234–237 (2010).
pubmed: 20574421
doi: 10.1038/nature09137
Duran, I. et al. Collagen duplicate genes of bone and cartilage participate during regeneration of zebrafish fin skeleton. Gene Expr. Patterns 19, 60–69 (2015).
pubmed: 26256560
doi: 10.1016/j.gep.2015.07.004
Wade, C., Brinas, I., Welfare, M., Wicking, C. & Farlie, P. G. Twist2 contributes to termination of limb bud outgrowth and patterning through direct regulation of Grem1. Dev. Biol. 370, 145–153 (2012).
pubmed: 22884497
doi: 10.1016/j.ydbio.2012.07.025
Yashiro, K. et al. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell 6, 411–422 (2004).
pubmed: 15030763
doi: 10.1016/S1534-5807(04)00062-0
Kawakami, Y. et al. Sp8 and Sp9, two closely related buttonhead-like transcription factors, regulate Fgf8 expression and limb outgrowth in vertebrate embryos. Development 131, 4763–4774 (2004).
pubmed: 15358670
doi: 10.1242/dev.01331
Gillis, J. A., Dahn, R. D. & Shubin, N. H. Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. Proc. Natl Acad. Sci. USA 106, 5720–5724 (2009).
pubmed: 19321424
pmcid: 2667079
doi: 10.1073/pnas.0810959106
Tulenko, F. J. et al. Fin-fold development in paddlefish and catshark and implications for the evolution of the autopod. Proc. Biol. Sci. 284, 20162780 (2017).
pubmed: 28539509
pmcid: 5454254
Hodgkinson, V. S., Ericsson, R., Johanson, Z. & Joss, J. M. P. The apical ectodermal ridge in the pectoral fin of the Australian lungfish (Neoceratodus forsteri): keeping the fin to limb transition in the fold. Acta Zool. 90, 253–263 (2009).
doi: 10.1111/j.1463-6395.2008.00349.x
Gehrke, A. R. & Shubin, N. H. Cis-regulatory programs in the development and evolution of vertebrate paired appendages. Semin. Cell Dev. Biol. 57, 31–39 (2016).
pubmed: 26783722
pmcid: 5360378
doi: 10.1016/j.semcdb.2016.01.015
Doroba, C. K. & Sears, K. E. The divergent development of the apical ectodermal ridge in the marsupial Monodelphis domestica. Anat. Rec. 293, 1325–1332 (2010).
doi: 10.1002/ar.21183
Purushothaman, S., Elewa, A. & Seifert, A. W. Fgf-signaling is compartmentalized within the mesenchyme and controls proliferation during salamander limb development. eLife 8, e48507 (2019).
pubmed: 31538936
pmcid: 6754229
doi: 10.7554/eLife.48507
Negrisolo, E. et al. Different phylogenomic approaches to resolve the evolutionary relationships among model fish species. Mol. Biol. Evol. 27, 2757–2774 (2010).
pubmed: 20591844
doi: 10.1093/molbev/msq165
Nikaido, M. et al. Coelacanth genomes reveal signatures for evolutionary transition from water to land. Genome Res. 23, 1740–1748 (2013).
pubmed: 23878157
pmcid: 3787270
doi: 10.1101/gr.158105.113
Frazer, K. A., Pachter, L., Poliakov, A., Rubin, E. M. & Dubchak, I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 32, W273–W279 (2004).
pubmed: 15215394
pmcid: 441596
doi: 10.1093/nar/gkh458
Brudno, M. et al. Glocal alignment: finding rearrangements during alignment. Bioinformatics 19, i54–i62 (2003).
pubmed: 12855437
doi: 10.1093/bioinformatics/btg1005
Braasch, I. et al. Connectivity of vertebrate genomes: paired-related homeobox (Prrx) genes in spotted gar, basal teleosts, and tetrapods. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 163, 24–36 (2014).
pubmed: 24486528
pmcid: 4032612
doi: 10.1016/j.cbpc.2014.01.005
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. & 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
Ramirez, F. et al. High-resolution TADs reveal DNA sequences underlying genome organization in flies. Nat. Commun. 9, 189 (2018).
pubmed: 29335486
pmcid: 5768762
doi: 10.1038/s41467-017-02525-w
Lopez-Delisle, L. et al. pyGenomeTracks: reproducible plots for multivariate genomic data sets. Bioinformatics 37, 422–423 (2020).
pmcid: 8058774
doi: 10.1093/bioinformatics/btaa692
Smit, A. F. A. & Hubley, R. RepeatModeler Open-1.0 http://www.repeatmasker.org (Institute for Systems Biology) (2008).
Jurka, J. Repbase update: a database and an electronic journal of repetitive elements. Trends Genet. 16, 418–420 (2000).
pubmed: 10973072
doi: 10.1016/S0168-9525(00)02093-X
Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0 http://www.repeatmasker.org (Institute for Systems Biology) (2013).
Smith, C. D. et al. Improved repeat identification and masking in Dipterans. Gene 389, 1–9 (2007).
pubmed: 17137733
doi: 10.1016/j.gene.2006.09.011
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Slater, G. S. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005).
pubmed: 15713233
pmcid: 553969
doi: 10.1186/1471-2105-6-31
Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).
pubmed: 15144565
pmcid: 421630
doi: 10.1186/1471-2105-5-59
Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19, ii215–ii225 (2003).
pubmed: 14534192
doi: 10.1093/bioinformatics/btg1080
Bowman, M. J., Pulman, J. A., Liu, T. L. & Childs, K. L. A modified GC-specific MAKER gene annotation method reveals improved and novel gene predictions of high and low GC content in Oryza sativa. BMC Bioinformatics 18, 522 (2017).
pubmed: 29178822
pmcid: 5702205
doi: 10.1186/s12859-017-1942-z
Bateman, A. et al. The Pfam Protein Families Database http://www.sanger.ac.uk/Software/Pfam/ (2000).
Eddy, S. R. Multiple alignment using hidden Markov models. Proc. Int. Conf. Intell. Syst. Mol. Biol. 3, 114–120 (1995).
pubmed: 7584426
Campbell, M. S., Holt, C., Moore, B. & Yandell, M. Genome annotation and curation using MAKER and MAKER-P. Curr. Protoc. Bioinformatics 48, 4.11.1–4.11.39 (2014).
doi: 10.1002/0471250953.bi0411s48
Vilella, A. J. et al. EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res. 19, 327–335 (2009).
pubmed: 19029536
pmcid: 2652215
doi: 10.1101/gr.073585.107
Ruan, J. et al. TreeFam: 2008 update. Nucleic Acids Res. 36, D735–D740 (2008).
pubmed: 18056084
doi: 10.1093/nar/gkm1005
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
Sankoff, D., Deneault, M., Bryant, D., Lemieux, C. & Turmel, M. in Comparative Genomics. Computational Biology Vol. 1 (eds Sankoff, D. & Nadeau, J. H.) (Springer, 2000).
Sawa, G., Dicks, J. & Roberts, I. N. Current approaches to whole genome phylogenetic analysis. Brief. Bioinform. 4, 63–74 (2003).
pubmed: 12715835
doi: 10.1093/bib/4.1.63
Farris, J. S. Phylogenetic analysis under Dollo’s law. Syst. Biol. 26, 77–88 (1977).
doi: 10.1093/sysbio/26.1.77
Felsenstein, J. PHYLIP—phylogeny inference package (ver. 3.2). Cladistics 5, 164–166 (1989).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
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
Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178–192 (2013).
pubmed: 22517427
doi: 10.1093/bib/bbs017
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
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
Kopylova, E., Noé, L. & Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217 (2012).
pubmed: 23071270
doi: 10.1093/bioinformatics/bts611
Fernandez-Minan, A., Bessa, J., Tena, J. J. & Gomez-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
Gaspar, J. M. Improved peak-calling with MACS2. Preprint at bioRxiv https://doi.org/10.1101/496521 (2018).
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
Babicki, S. et al. Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res. 44, W147–W153 (2016).
pubmed: 27190236
pmcid: 4987948
doi: 10.1093/nar/gkw419
Wickham, H. ggplot2: Elegant Graphics for Data Analysis 2nd edn (Springer Verlag, 2016).
Lufkin, T. In situ hybridization of whole-mount mouse embryos with RNA probes: preparation of embryos and probes. CSH Protoc. 2007, pdb.prot4822 (2007).
pubmed: 21356975
Lufkin, T. In situ hybridization of whole-mount mouse embryos with RNA probes: hybridization, washes, and histochemistry. CSH Protoc. 2007, pdb.prot4823 (2007).
pubmed: 21356976
Tatsumi, N. et al. Molecular developmental mechanism in polypterid fish provides insight into the origin of vertebrate lungs. Sci. Rep. 6, 30580 (2016).
pubmed: 27466206
pmcid: 4964569
doi: 10.1038/srep30580
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
Komisarczuk, A. Z., Kawakami, K. & Becker, T. S. Cis-regulation and chromosomal rearrangement of the fgf8 locus after the teleost/tetrapod split. Dev. Biol. 336, 301–312 (2009).
pubmed: 19782672
doi: 10.1016/j.ydbio.2009.09.029
Marinic, M., Aktas, T., Ruf, S. & Spitz, F. An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev. Cell 24, 530–542 (2013).
pubmed: 23453598
doi: 10.1016/j.devcel.2013.01.025
Hornblad, A., Bastide, S., Langenfeld, K., Langa, F. & Spitz, F. Dissection of the Fgf8 regulatory landscape by in vivo CRISPR-editing reveals extensive intra- and inter-enhancer redundancy. Nat. Commun. 12, 439 (2021).
pubmed: 33469032
pmcid: 7815712
doi: 10.1038/s41467-020-20714-y