Tracing the genetic footprints of vertebrate landing in non-teleost ray-finned fishes

نویسندگان

چکیده

•De novo reference genome assemblies of four non-teleost ray-finned fishes•Basal fishes have key limb development regulatory elements•Lung-related genes in early hold the for lung origin•Cardio-respiratory systems’ co-evolution during air breathing evolution Rich fossil evidence suggests that many traits and functions related to terrestrial were present long before ancestor lobe- fishes. Here, we sequences bichir, paddlefish, bowfin, alligator gar, covering all major divergent lineages Our analyses show these species exhibit mosaic genomic features In particular, elements are fishes, supporting hypothesis relevant ancestral regulation networks emerged origin tetrapods. Transcriptome confirm homology between swim bladder reveal presence functional lung-related Furthermore, functionally validate essential role a jawed vertebrate highly conserved element cardiovascular development. results imply ancestors vertebrates already had potential gene cardio-respiratory systems breathing. The water-to-land transition Devonian is one most prominent events evolution. During this transition, various organs underwent adaptive changes, particularly those locomotion respiration (Hinchliffe, 1994Hinchliffe J.R. Evolutionary developmental biology tetrapod limb.Dev. Suppl. 1994; 1994: 163-168Google Scholar; Long Gordon, 2004Long J.A. Gordon M.S. greatest step history: paleobiological review fish-tetrapod transition.Physiol. Biochem. Zool. 2004; 77: 700-719Crossref PubMed Scopus (0) Google Scholar). Study changes occurred tetrapods challenging because animals involved transitional extinct. However, it has been postulated innovations evolved bony (ray-finned lobe-finned tetrapods) thus still some living basal groups actinopterygians fishes) (Graham et al., 2014Graham J.B. Wegner N.C. Miller L.A. Jew C.J. Lai Berquist R.M. Frank L.R. Spiracular polypterid its implications aerial stem tetrapods.Nat. Commun. 2014; 5: 3022Crossref (26) Takeuchi 2009Takeuchi M. 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Silurian placoderm osteichthyan-like marginal bones.Nature. 502: 188-193Crossref (148) Yu, 2009Zhu Stem sarcopterygians polybasal fin articulation.Palaeontology. 372-375Google place phylogenetic position crucial comparative studies aim transitions vertebrates. elucidate diverging produced chromosome level assembly senegalus) draft American paddlefish (Polyodon spathula), bowfin (Amia calva), gar (Atractosteus spatula), together cover outgroup lineages. showed relating We then undertook transcriptomic-based exploration revealed Finally, performed experiments (gnathostome) generated 250 Gb reads using Nanopore Technology used produce assembly. was polished Illumina short improved chromosome-level Hi-C data. final contig N50 size 4.53 Mb scaffold 189.69 Mb, 94.3% anchored onto 18 chromosomes. sequenced assembled 135–242x coverage libraries inserted sizes ranging bp 40 kb (Table S1). From 89%–96% 2,586 core sets Benchmarking Universal Single-Copy Orthologs (BUSCO) completely annotated (Simão 2015Simão F.A. Waterhouse Ioannidis P. Kriventseva E.V. Zdobnov E.M. BUSCO: assessing annotation completeness single-copy orthologs.Bioinformatics. 31: 3210-3212Crossref (3219) transcriptome nine tissues each assist annotation, resulted 18,839–23,374 protein coding studied date vary considerably, 0.95 3.67 Gb, implies happened structures divergence Some variation differences proportions repeat content, range 14% 44% Interestingly, TcMar-Tc1 seems abundant type transposon (Figure S1A), accordance previous findings transposons active freshwater (Yuan 2018Yuan Liu Zhou Tian Bao Dunham Comparative analysis 52 differential associations repetitive aquatic environments.BMC 2018; 19: 141Crossref addition, similar contain LINE/CR1 repeats, might S1B). Despite extensive both extinct since late nineteenth century (Allen, 1876Allen bisons, extinct.Vol. 10. 1876Crossref Cope, 1878Cope E.D. 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Iwabe Miyata inferred multiple nuclear DNA-coded genes.BMC 2: 3Crossref (90) identified 359 one-to-one orthologs across 27 chordates (allowing up missing) derived same chromosomes two rounds whole-genome duplications (WGDs) base (Sacerdot 2018Sacerdot Louis Bon Berthelot Crollius Chromosome genome.Genome 1-15Crossref (29) S1C). Phylogenetic orthologous confirmed Polypteriformes (bichirs) form resolved 1). This topology supported (Gardiner 2005Gardiner B.G. Schaeffer Masserie lower phylogeny.Zoological Journal Linnean Society. 2005; 511-525Crossref (84) trees 23 genome-wide 319 single copy 14 selected (Figures S1D S1E). dating calibrated records S1) split 453 million years ago (Mya, 95% confidence interval: 445.8–459.8 Mya), close estimate (422 Mya) based (Lalu 2010Lalu X.C. Kosen J.D. Tjakrawidjaja A.H. Kusumah R.V. Sadhotomo Pouyaud Slembrouck Paradis E. 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Remarkably, higher synteny chicken than whose undergone more fusions, fissions, rearrangements following teleost-specific 2B S2B). example, found 51% genome. When expanding include vertebrates, share 9%–36% humans, shared any teleosts (6%–7%) examined humans S2). clearly indicate largely preserved structure duplication. overall conservation genome, 22 fusion appear lineage, micro-chromosomes merged macro-chromosomes. rearrangement accompanied elevated activity, increases species.Figure S2The WGD 2Show caption(A) reconstruction procedure.(B) bichir-spotted gar-chicken gar-zebrafish-medaka.(C) HOX clusters vertebrates.(D) 4DTv determine 3R time sterlet.(E) Construction 1935 among (g), (p) (s). green represents independent sterlet. orange WGD. purple cannot prove whether independently not. pie chart proportion topologies.View Large Image ViewerDownload Hi-res image Download (PPT) (A) procedure. (B) gar-zebrafish-medaka. (C) (D) (E) topologies. Recent shown third round (3R WGD) (Acipenser ruthenus) (Du closely paddlefish. detected seven Hox indicating S2C). To investigate event lineages, analyzed distributions synonymous substitution rates (Ks) 4-fold degenerative third-codon transversions (4dTv) 3,743 8,297 paralogs. Ks age different ranges, suggesting 2C). pattern distribution 4dTv values, S2D S2E). Based (135 1), 121 Mya 51 Mya, respectively. Although our estimated much study, prior sterlet-Atlantic 166 earlier (74 (Rabosky 2013Rabosky D.L. Santini F. Eastman S.A. Sidlauskas Chang Alfaro M.E. Rates correlated largest radiation.Nat. 1958Crossref whole offers excellent model studying fate duplicate after Unlike retained eight clusters, lost HoxC cluster loss fugu (Takifugu rubripes) medaka (Oryzias latipes) At global level, 8,377 singletons paralogous retention around 31%, considerably (70%), indications corresponding (15%–20%) (Hrbek 2007Hrbek Seckinger biogeographic poeciliid fishes.Molecular Phylogenetics Evolution. 43: 986-998Crossref (138) Notably, duplicated turnover, signal transduction, cell proliferation, preferably maintained but enriched biosynthetic process, expression, metabolic process suggest substantially selection pressures acted locomotion, evolution, appearance appendicular (Carroll Holmes, 2007Carroll Holmes skeleton amphibians.in: Hall B.K. Fins Limbs: Evolution, Development, Transformation. Chicago 2007: 185-224Google Neyt 2000Neyt Jagla Thisse Haines Currie P.D. muscle.Nature. 2000; 408: 82-86Crossref (139) anatomical (Clack, 2009Clack transition: data, interpretations, hypotheses paleontology biology.Annual Review Earth Planetary Sciences. 37: 163-179Crossref humerus proximal sarcopterygian forelimb, metapterygium putatively appeared (Davis 2004Davis Shubin N.H. Force Pectoral girdle Polyodon spathula Acipenser transmontanus.J. Morphol. 262: 608-628Crossref (54) Tanaka, 2016Tanaka limbs: Autopod acquisition anterior reduction modifying involving 5’Hox, Gli3, Shh.Dev. 413: 1-7Crossref (13) Wagner Chiu, 2001Wagner G.P. Chiu C.H. limb: origin.J. Exp. 291: 226-240Crossref 2020Woltering Irisarri Ericsson Joss J.M.P. Sordino Sarcopterygian ontogeny elucidates hands digits.Sci. Adv. 6: eabc3510Crossref (7) study fleshy fins movable elbow joint connects ulna crisscrossed ligaments (Miyake 2016Miyake Kumamoto Iwata Sato Koie Kumai Fujii Matsuzaki Nakamura muscles Latimeria chalumnae: Functional fin-to-limb subsequent tetrapods.Anat. Rec. (Hoboken). 299: 1203-1223Crossref Meanwhile, preaxial postaxial pelvic resemble Neoceratodus (Molnar 2017Molnar J.L. Johnston Esteve-Altava Diogo Musculoskeletal Polypterus: pre- muscles.J. Anat. 230: 532-541Crossref reason movement connections crown teleosts. test hypothesis, first searched presences homologs 264 morphogenesis development, bud formation, did detect difference numbers when comparing nor specific flexibility significant change protein-coding S3). Therefore, next screened enhancer validated mice. Among investigated, lowest enhancers mice tissue types, partially turnover group. there number

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ژورنال

عنوان ژورنال: Cell

سال: 2021

ISSN: ['0092-8674', '1097-4172']

DOI: https://doi.org/10.1016/j.cell.2021.01.046