The brittle star genome illuminates the genetic basis of animal appendage regeneration.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
19 Jul 2024
19 Jul 2024
Historique:
received:
06
11
2023
accepted:
29
05
2024
medline:
20
7
2024
pubmed:
20
7
2024
entrez:
19
7
2024
Statut:
aheadofprint
Résumé
Species within nearly all extant animal lineages are capable of regenerating body parts. However, it remains unclear whether the gene expression programme controlling regeneration is evolutionarily conserved. Brittle stars are a species-rich class of echinoderms with outstanding regenerative abilities, but investigations into the genetic bases of regeneration in this group have been hindered by the limited genomic resources. Here we report a chromosome-scale genome assembly for the brittle star Amphiura filiformis. We show that the brittle star genome is the most rearranged among echinoderms sequenced so far, featuring a reorganized Hox cluster reminiscent of the rearrangements observed in sea urchins. In addition, we performed an extensive profiling of gene expression during brittle star adult arm regeneration and identified sequential waves of gene expression governing wound healing, proliferation and differentiation. We conducted comparative transcriptomic analyses with other invertebrate and vertebrate models for appendage regeneration and uncovered hundreds of genes with conserved expression dynamics, particularly during the proliferative phase of regeneration. Our findings emphasize the crucial importance of echinoderms to detect long-range expression conservation between vertebrates and classical invertebrate regeneration model systems.
Identifiants
pubmed: 39030276
doi: 10.1038/s41559-024-02456-y
pii: 10.1038/s41559-024-02456-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Royal Society
ID : URF\R1\191161
Organisme : Royal Society
ID : NIF\R1\222125
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/V01109X/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/V01109X/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/W017865/1
Organisme : Leverhulme Trust
ID : RPG-2021-436
Organisme : Japan Society for the Promotion of Science London (JSPS London)
ID : JP 19K06620
Organisme : Vetenskapsrådet (Swedish Research Council)
ID : 253016979
Organisme : Vetenskapsrådet (Swedish Research Council)
ID : 253016979
Organisme : Fonds De La Recherche Scientifique - FNRS (Belgian National Fund for Scientific Research)
ID : 40013965
Organisme : Fonds De La Recherche Scientifique - FNRS (Belgian National Fund for Scientific Research)
ID : T.0169.20
Organisme : National Science Foundation (NSF)
ID : 2131297
Organisme : EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020)
ID : MARISTEM
Organisme : EC | EC Seventh Framework Programm | FP7 Research infrastructures (FP7-INFRASTRUCTURES - Specific Programme "Capacities": Research Infrastructures)
ID : ASSEMBLE (227799)
Informations de copyright
© 2024. The Author(s).
Références
Stöhr, S., O’Hara, T. D. & Thuy, B. Global diversity of brittle stars (Echinodermata: Ophiuroidea). PLoS ONE 7, e31940 (2012).
pubmed: 22396744
pmcid: 3292557
doi: 10.1371/journal.pone.0031940
O’Hara, T. D., Hugall, A. F., Woolley, S. N. C., Bribiesca-Contreras, G. & Bax, N. J. Contrasting processes drive ophiuroid phylodiversity across shallow and deep seafloors. Nature 565, 636–639 (2019).
pubmed: 30675065
doi: 10.1038/s41586-019-0886-z
Vistisen, B. & Vismann, B. Tolerance to low oxygen and sulfide in Amphiura filiformis and Ophiura albida (Echinodermata: Ophiuroidea). Mar. Biol. 128, 241–246 (1997).
doi: 10.1007/s002270050088
Vopel, K., Thistle, D. & Rosenberg, R. Effect of the brittle star Amphiura filiformis (Amphiuridae, Echinodermata) on oxygen flux into the sediment. Limnol. Oceanogr. 48, 2034–2045 (2003).
doi: 10.4319/lo.2003.48.5.2034
Dupont, S. & Thorndyke, M. Bridging the regeneration gap: insights from echinoderm models. Nat. Rev. Genet. 8, 320 (2007).
doi: 10.1038/nrg1923-c1
Mosher, C. V. & Watling, L. Partners for life: a brittle star and its octocoral host. Mar. Ecol. Prog. Ser. 397, 81–88 (2009).
doi: 10.3354/meps08113
Thuy, B. et al. Ancient origin of the modern deep-sea fauna. PLoS ONE 7, e46913 (2012).
pubmed: 23071660
pmcid: 3468611
doi: 10.1371/journal.pone.0046913
Delroisse, J. et al. A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence. Open Biol. 7, 160300 (2017).
pubmed: 28381628
pmcid: 5413902
doi: 10.1098/rsob.160300
Dylus, D. V., Czarkwiani, A., Blowes, L. M., Elphick, M. R. & Oliveri, P. Developmental transcriptomics of the brittle star Amphiura filiformis reveals gene regulatory network rewiring in echinoderm larval skeleton evolution. Genome Biol. 19, 26 (2018).
pubmed: 29490679
pmcid: 5831733
doi: 10.1186/s13059-018-1402-8
Telford, M. J. et al. Phylogenomic analysis of echinoderm class relationships supports Asterozoa. Proc. R. Soc. B 281, 20140479 (2014).
pubmed: 24850925
pmcid: 4046411
doi: 10.1098/rspb.2014.0479
O’Hara, T. D., Hugall, A. F., Thuy, B. & Moussalli, A. Phylogenomic resolution of the class Ophiuroidea unlocks a global microfossil record. Curr. Biol. 24, 1874–1879 (2014).
pubmed: 25065752
doi: 10.1016/j.cub.2014.06.060
Cannon, J. T. et al. Phylogenomic resolution of the hemichordate and echinoderm clade. Curr. Biol. 24, 2827–2832 (2014).
pubmed: 25454590
doi: 10.1016/j.cub.2014.10.016
Mongiardino Koch, N. et al. Phylogenomic analyses of echinoid diversification prompt a re-evaluation of their fossil record. Elife 11, e72460 (2022).
pubmed: 35315317
pmcid: 8940180
doi: 10.7554/eLife.72460
Sea Urchin Genome Sequencing Consortium. The genome of the sea urchin Strongylocentrotus purpuratus. Science 314, 941–952 (2006).
pmcid: 3159423
doi: 10.1126/science.1133609
Raible, F. et al. Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Dev. Biol. 300, 461–475 (2006).
pubmed: 17067569
doi: 10.1016/j.ydbio.2006.08.070
Livingston, B. T. et al. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 300, 335–348 (2006).
pubmed: 16987510
doi: 10.1016/j.ydbio.2006.07.047
Rast, J. P., Smith, L. C., Loza-Coll, M., Hibino, T. & Litman, G. W. Genomic insights into the immune system of the sea urchin. Science 314, 952–956 (2006).
pubmed: 17095692
pmcid: 3707132
doi: 10.1126/science.1134301
Hall, M. R. et al. The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest. Nature 544, 231–234 (2017).
pubmed: 28379940
doi: 10.1038/nature22033
Chen, T. et al. The Holothuria leucospilota genome elucidates sacrificial organ expulsion and bioadhesive trap enriched with amyloid-patterned proteins. Proc. Natl Acad. Sci. USA 120, e2213512120 (2023).
pubmed: 37036994
pmcid: 10120082
doi: 10.1073/pnas.2213512120
Davidson, P. L. et al. Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins. Nat. Ecol. Evol. 6, 1907–1920 (2022).
pubmed: 36266460
doi: 10.1038/s41559-022-01906-9
Davidson, P. L. et al. Chromosomal-level genome assembly of the sea urchin Lytechinus variegatus substantially improves functional genomic analyses. Genome Biol. Evol. 12, 1080–1086 (2020).
pubmed: 32433766
pmcid: 7455304
doi: 10.1093/gbe/evaa101
Zhang, X. et al. The sea cucumber genome provides insights into morphological evolution and visceral regeneration. PLoS Biol. 15, e2003790 (2017).
pubmed: 29023486
pmcid: 5638244
doi: 10.1371/journal.pbio.2003790
Marlétaz, F. et al. Analysis of the P. lividus sea urchin genome highlights contrasting trends of genomic and regulatory evolution in deuterostomes. Cell Genom. 3, 100295 (2023).
pubmed: 37082140
pmcid: 10112332
doi: 10.1016/j.xgen.2023.100295
Lawniczak, M. K. N. et al. The genome sequence of the spiny starfish, Marthasterias glacialis (Linnaeus, 1758). Wellcome Open Res. 6, 295 (2021).
pubmed: 36936045
pmcid: 10015122
doi: 10.12688/wellcomeopenres.17344.1
Smith, A. B. Deuterostomes in a twist: the origins of a radical new body plan. Evol. Dev. 10, 493–503 (2008).
pubmed: 18638326
doi: 10.1111/j.1525-142X.2008.00260.x
Cameron, R. A. et al. Unusual gene order and organization of the sea urchin hox cluster. J. Exp. Zool. B 306, 45–58 (2006).
doi: 10.1002/jez.b.21070
David, B. & Mooi, R. How Hox genes can shed light on the place of echinoderms among the deuterostomes. Evodevo 5, 22 (2014).
pubmed: 24959343
pmcid: 4066700
doi: 10.1186/2041-9139-5-22
Mooi, R. & David, B. Radial symmetry, the anterior/posterior axis, and echinoderm Hox genes. Annu. Rev. Ecol. Evol. Syst. 39, 43–62 (2008).
doi: 10.1146/annurev.ecolsys.39.110707.173521
Lowe, C. J. & Wray, G. A. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389, 718–721 (1997).
pubmed: 9338781
doi: 10.1038/39580
Baughman, K. W. et al. Genomic organization of Hox and ParaHox clusters in the echinoderm, Acanthaster planci. Genesis 52, 952–958 (2014).
pubmed: 25394327
doi: 10.1002/dvg.22840
Byrne, M., Martinez, P. & Morris, V. Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited. Evol. Dev. 18, 137–143 (2016).
pubmed: 26763653
doi: 10.1111/ede.12172
Medina-Feliciano, J. G. & García-Arrarás, J. E. Regeneration in echinoderms: molecular advancements. Front. Cell Dev. Biol. 9, 768641 (2021).
pubmed: 34977019
pmcid: 8718600
doi: 10.3389/fcell.2021.768641
Srivastava, M. Beyond casual resemblance: rigorous frameworks for comparing regeneration across species. Annu. Rev. Cell Dev. Biol. 37, 415–440 (2021).
pubmed: 34288710
doi: 10.1146/annurev-cellbio-120319-114716
Lai, A. G. & Aboobaker, A. A. EvoRegen in animals: time to uncover deep conservation or convergence of adult stem cell evolution and regenerative processes. Dev. Biol. 433, 118–131 (2018).
pubmed: 29198565
doi: 10.1016/j.ydbio.2017.10.010
Bely, A. E. & Nyberg, K. G. Evolution of animal regeneration: re-emergence of a field. Trends Ecol. Evol. 25, 161–170 (2010).
pubmed: 19800144
doi: 10.1016/j.tree.2009.08.005
Cary, G. A., Wolff, A., Zueva, O., Pattinato, J. & Hinman, V. F. Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa. BMC Biol. 17, 16 (2019).
pubmed: 30795750
pmcid: 6385403
doi: 10.1186/s12915-019-0633-9
Goldman, J. A. & Poss, K. D. Gene regulatory programmes of tissue regeneration. Nat. Rev. Genet. 21, 511–525 (2020).
pubmed: 32504079
pmcid: 7448550
doi: 10.1038/s41576-020-0239-7
Bideau, L., Kerner, P., Hui, J., Vervoort, M. & Gazave, E. Animal regeneration in the era of transcriptomics. Cell. Mol. Life Sci. 78, 3941–3956 (2021).
pubmed: 33515282
pmcid: 11072743
doi: 10.1007/s00018-021-03760-7
Sköld, M. & Rosenberg, R. Arm regeneration frequency in eight species of Ophiuroidea (Echinodermata) from European sea areas. J. Sea Res. 35, 353–362 (1996).
doi: 10.1016/S1385-1101(96)90762-5
Duineveld, G. C. A. & Van Noort, G. J. Observations on the population dynamics of Amphiura filiformis (Ophiuroidea: Echinodermata) in the southern North Sea and its exploitation by the dab, Limanda limanda. Neth. J. Sea Res. 20, 85–94 (1986).
doi: 10.1016/0077-7579(86)90064-5
Czarkwiani, A., Dylus, D. V. & Oliveri, P. Expression of skeletogenic genes during arm regeneration in the brittle star Amphiura filiformis. Gene Expr. Patterns 13, 464–472 (2013).
pubmed: 24051028
pmcid: 3838619
doi: 10.1016/j.gep.2013.09.002
Czarkwiani, A., Ferrario, C., Dylus, D. V., Sugni, M. & Oliveri, P. Skeletal regeneration in the brittle star Amphiura filiformis. Front. Zool. 13, 18 (2016).
pubmed: 27110269
pmcid: 4841056
doi: 10.1186/s12983-016-0149-x
Piovani, L., Czarkwiani, A., Ferrario, C., Sugni, M. & Oliveri, P. Ultrastructural and molecular analysis of the origin and differentiation of cells mediating brittle star skeletal regeneration. BMC Biol. 19, 9 (2021).
pubmed: 33461552
pmcid: 7814545
doi: 10.1186/s12915-020-00937-7
Czarkwiani, A., Taylor, J. & Oliveri, P. Neurogenesis during brittle star arm regeneration is characterised by a conserved set of key developmental genes. Biology 11, 1360 (2022).
pubmed: 36138839
pmcid: 9495562
doi: 10.3390/biology11091360
Hu, M. Y., Casties, I., Stumpp, M., Ortega-Martinez, O. & Dupont, S. Energy metabolism and regeneration are impaired by seawater acidification in the infaunal brittlestar Amphiura filiformis. J. Exp. Biol. 217, 2411–2421 (2014).
pubmed: 24737772
Purushothaman, S. et al. Transcriptomic and proteomic analyses of Amphiura filiformis arm tissue–undergoing regeneration. J. Proteom. 112, 113–124 (2015).
doi: 10.1016/j.jprot.2014.08.011
Dupont, S. & Thorndyke, M. C. Growth or differentiation? Adaptive regeneration in the brittlestar Amphiura filiformis. J. Exp. Biol. 209, 3873–3881 (2006).
pubmed: 16985203
doi: 10.1242/jeb.02445
Sinigaglia, C. et al. Distinct gene expression dynamics in developing and regenerating crustacean limbs. Proc. Natl Acad. Sci. USA 119, e2119297119 (2022).
pubmed: 35776546
pmcid: 9271199
doi: 10.1073/pnas.2119297119
Stewart, R. et al. Comparative RNA-seq analysis in the unsequenced axolotl: the oncogene burst highlights early gene expression in the blastema. PLoS Comput. Biol. 9, e1002936 (2013).
pubmed: 23505351
pmcid: 3591270
doi: 10.1371/journal.pcbi.1002936
Li, Y. et al. Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms. Commun. Biol. 3, 371 (2020).
pubmed: 32651448
pmcid: 7351957
doi: 10.1038/s42003-020-1091-1
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
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
Liu, J., Zhou, Y., Pu, Y. & Zhang, H. A chromosome-level genome assembly of a deep-sea starfish (Zoroaster cf. ophiactis). Sci. Data 10, 506 (2023).
pubmed: 37528102
pmcid: 10394057
doi: 10.1038/s41597-023-02397-4
Davidson, P. L., Lessios, H. A., Wray, G. A., McMillan, W. O. & Prada, C. Near-chromosomal-level genome assembly of the sea urchin Echinometra lucunter, a model for speciation in the sea. Genome Biol. Evol. 15, evad093 (2023).
pubmed: 37280750
pmcid: 10244470
doi: 10.1093/gbe/evad093
Schiebelhut, L. M., Puritz, J. B. & Dawson, M. N. Decimation by sea star wasting disease and rapid genetic change in a keystone species, Pisaster ochraceus. Proc. Natl Acad. Sci. USA 115, 7069–7074 (2018).
pubmed: 29915091
pmcid: 6142263
doi: 10.1073/pnas.1800285115
Lee, Y. et al. Chromosome-level genome assembly of Plazaster borealis sheds light on the morphogenesis of multiarmed starfish and its regenerative capacity. Gigascience 11, giac063c (2022).
doi: 10.1093/gigascience/giac063
Ketchum, R. N. et al. A chromosome-level genome assembly of the highly heterozygous sea urchin Echinometra sp. EZ reveals adaptation in the regulatory regions of stress response genes. Genome Biol. Evol. 14, evac144 (2022).
pubmed: 36161313
pmcid: 9557091
doi: 10.1093/gbe/evac144
Belyayev, A. Bursts of transposable elements as an evolutionary driving force. J. Evol. Biol. 27, 2573–2584 (2014).
pubmed: 25290698
doi: 10.1111/jeb.12513
Annunziata, R., Martinez, P. & Arnone, M. I. Intact cluster and chordate-like expression of ParaHox genes in a sea star. BMC Biol. 11, 68 (2013).
pubmed: 23803323
pmcid: 3710244
doi: 10.1186/1741-7007-11-68
Arenas-Mena, C., Martinez, P., Cameron, R. A. & Davidson, E. H. Expression of the Hox gene complex in the indirect development of a sea urchin. Proc. Natl Acad. Sci. USA 95, 13062–13067 (1998).
pubmed: 9789041
pmcid: 23710
doi: 10.1073/pnas.95.22.13062
Dylus, D. V. et al. Large-scale gene expression study in the ophiuroid Amphiura filiformis provides insights into evolution of gene regulatory networks. Evodevo 7, 2 (2016).
pubmed: 26759711
pmcid: 4709884
doi: 10.1186/s13227-015-0039-x
Delroisse, J. et al. High opsin diversity in a non-visual infaunal brittle star. BMC Genomics 15, 1035 (2014).
pubmed: 25429842
pmcid: 4289182
doi: 10.1186/1471-2164-15-1035
Delroisse, J., Ortega-Martinez, O., Dupont, S., Mallefet, J. & Flammang, P. De novo transcriptome of the European brittle star Amphiura filiformis pluteus larvae. Mar. Genomics 23, 109–121 (2015).
pubmed: 26044617
doi: 10.1016/j.margen.2015.05.014
Tu, Q., Cameron, R. A. & Davidson, E. H. Quantitative developmental transcriptomes of the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 385, 160–167 (2014).
pubmed: 24291147
doi: 10.1016/j.ydbio.2013.11.019
Arnone, M. I. et al. Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: insights into the relationship between clustering and colinearity. Dev. Biol. 300, 63–73 (2006).
pubmed: 16959236
doi: 10.1016/j.ydbio.2006.07.037
Kikuchi, M., Omori, A., Kurokawa, D. & Akasaka, K. Patterning of anteroposterior body axis displayed in the expression of Hox genes in sea cucumber Apostichopus japonicus. Dev. Genes Evol. 225, 275–286 (2015).
pubmed: 26250612
doi: 10.1007/s00427-015-0510-7
Hara, Y. et al. Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus. Dev. Genes Evol. 216, 797–809 (2006).
pubmed: 17013610
doi: 10.1007/s00427-006-0108-1
Li, Y. et al. Sea cucumber genome provides insights into saponin biosynthesis and aestivation regulation. Cell Discov. 4, 29 (2018).
pubmed: 29951224
pmcid: 6018497
doi: 10.1038/s41421-018-0030-5
Arenas-Mena, C., Cameron, R. A. & Davidson, E. H. Hindgut specification and cell-adhesion functions of Sphox11/13b in the endoderm of the sea urchin embryo. Dev. Growth Differ. 48, 463–472 (2006).
pubmed: 16961593
doi: 10.1111/j.1440-169X.2006.00883.x
Yamazaki, A., Yamakawa, S., Morino, Y., Sasakura, Y. & Wada, H. Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option. Sci. Rep. 11, 20111 (2021).
pubmed: 34635691
pmcid: 8505446
doi: 10.1038/s41598-021-99521-4
Seo, H. C. et al. Miniature genome in the marine chordate Oikopleura dioica. Science 294, 2506 (2001).
pubmed: 11752568
doi: 10.1126/science.294.5551.2506
Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064–1071 (2008).
pubmed: 18563158
doi: 10.1038/nature06967
Leulier, F. & Lemaitre, B. Toll-like receptors—taking an evolutionary approach. Nat. Rev. Genet. 9, 165–178 (2008).
pubmed: 18227810
doi: 10.1038/nrg2303
Nei, M., Gu, X. & Sitnikova, T. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc. Natl Acad. Sci. USA 94, 7799–7806 (1997).
pubmed: 9223266
pmcid: 33709
doi: 10.1073/pnas.94.15.7799
Saco, A., Novoa, B., Greco, S., Gerdol, M. & Figueras, A. Bivalves present the largest and most diversified repertoire of toll-like receptors in the animal kingdom, suggesting broad-spectrum pathogen recognition in marine waters. Mol. Biol. Evol. 40, msad133 (2023).
pubmed: 37279919
pmcid: 10279657
doi: 10.1093/molbev/msad133
Pryzdial, E. L. G., Leatherdale, A. & Conway, E. M. Coagulation and complement: key innate defense participants in a seamless web. Front. Immunol. 13, 918775 (2022).
pubmed: 36016942
pmcid: 9398469
doi: 10.3389/fimmu.2022.918775
Loof, T. G., Schmidt, O., Herwald, H. & Theopold, U. Coagulation systems of invertebrates and vertebrates and their roles in innate immunity: the same side of two coins? J. Innate Immun. 3, 34–40 (2011).
pubmed: 21051879
doi: 10.1159/000321641
Hanington, P. C. & Zhang, S.-M. The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J. Innate Immun. 3, 17–27 (2011).
pubmed: 21063081
doi: 10.1159/000321882
Arenas Gómez, C. M., Sabin, K. Z. & Echeverri, K. Wound healing across the animal kingdom: crosstalk between the immune system and the extracellular matrix. Dev. Dyn. 249, 834–846 (2020).
pubmed: 32314465
pmcid: 7383677
doi: 10.1002/dvdy.178
Ferrario, C. et al. Fundamental aspects of arm repair phase in two echinoderm models. Dev. Biol. 433, 297–309 (2018).
pubmed: 29291979
doi: 10.1016/j.ydbio.2017.09.035
Suárez-Álvarez, B., Liapis, H. & Anders, H.-J. Links between coagulation, inflammation, regeneration, and fibrosis in kidney pathology. Lab Invest. 96, 378–390 (2016).
pubmed: 26752746
doi: 10.1038/labinvest.2015.164
Ramachandra, R. et al. A potential role for chondroitin sulfate/dermatan sulfate in arm regeneration in Amphiura filiformis. Glycobiology 27, 438–449 (2017).
pubmed: 28130266
Karra, R., Knecht, A. K., Kikuchi, K. & Poss, K. D. Myocardial NF-κB activation is essential for zebrafish heart regeneration. Proc. Natl Acad. Sci. USA 112, 13255–13260 (2015).
pubmed: 26472034
pmcid: 4629358
doi: 10.1073/pnas.1511209112
Straughn, A. R., Hindi, S. M., Xiong, G. & Kumar, A. Canonical NF-κB signaling regulates satellite stem cell homeostasis and function during regenerative myogenesis. J. Mol. Cell. Biol. 11, 53–66 (2019).
pubmed: 30239789
doi: 10.1093/jmcb/mjy053
Wenger, Y., Buzgariu, W., Reiter, S. & Galliot, B. Injury-induced immune responses in Hydra. Semin. Immunol. 26, 277–294 (2014).
pubmed: 25086685
doi: 10.1016/j.smim.2014.06.004
Cui, M. et al. Nrf1 promotes heart regeneration and repair by regulating proteostasis and redox balance. Nat. Commun. 12, 5270 (2021).
pubmed: 34489413
pmcid: 8421386
doi: 10.1038/s41467-021-25653-w
Ayaz, G., Yan, H., Malik, N. & Huang, J. An updated view of the roles of p53 in embryonic stem cells. Stem Cells 40, 883–891 (2022).
pubmed: 35904997
pmcid: 9585900
doi: 10.1093/stmcls/sxac051
Kawaguchi, M. et al. Co-option of the PRDM14-CBFA2T complex from motor neurons to pluripotent cells during vertebrate evolution. Development 146, dev168633 (2019).
pubmed: 30630825
doi: 10.1242/dev.168633
Dong, X. et al. YY1 safeguard multidimensional epigenetic landscape associated with extended pluripotency. Nucleic Acids Res. 50, 12019–12038 (2022).
pubmed: 35425987
pmcid: 9756953
doi: 10.1093/nar/gkac230
Oh, S. K. et al. RORα is crucial for attenuated inflammatory response to maintain intestinal homeostasis. Proc. Natl Acad. Sci. USA 116, 21140–21149 (2019).
pubmed: 31570593
pmcid: 6800319
doi: 10.1073/pnas.1907595116
Villot, R. et al. ZNF768: controlling cellular senescence and proliferation with ten fingers. Mol. Cell Oncol. 8, 1985930 (2021).
pubmed: 35419475
pmcid: 8997246
doi: 10.1080/23723556.2021.1985930
Han, D. et al. ZBTB12 is a molecular barrier to dedifferentiation in human pluripotent stem cells. Nat. Commun. 14, 632 (2023).
pubmed: 36759523
pmcid: 9911396
doi: 10.1038/s41467-023-36178-9
Huat, T. J. et al. IGF-1 enhances cell proliferation and survival during early differentiation of mesenchymal stem cells to neural progenitor-like cells. BMC Neurosci. 15, 91 (2014).
pubmed: 25047045
pmcid: 4117972
doi: 10.1186/1471-2202-15-91
Herrera, S. C. & Bach, E. A. JAK/STAT signaling in stem cells and regeneration: from Drosophila to vertebrates. Development 146, dev167643 (2019).
pubmed: 30696713
pmcid: 6361132
doi: 10.1242/dev.167643
Xu, N., Lao, Y., Zhang, Y. & Gillespie, D. A. Akt: a double-edged sword in cell proliferation and genome stability. J. Oncol. 2012, 951724 (2012).
pubmed: 22481935
pmcid: 3317191
doi: 10.1155/2012/951724
Apte, R. S., Chen, D. S. & Ferrara, N. VEGF in signaling and disease: beyond discovery and development. Cell 176, 1248–1264 (2019).
pubmed: 30849371
pmcid: 6410740
doi: 10.1016/j.cell.2019.01.021
Gross, J. M., Peterson, R. E., Wu, S.-Y. & McClay, D. R. LvTbx2/3: a T-box family transcription factor involved in formation of the oral/aboral axis of the sea urchin embryo. Development 130, 1989–1999 (2003).
pubmed: 12642501
doi: 10.1242/dev.00409
Slota, L. A. & McClay, D. R. Identification of neural transcription factors required for the differentiation of three neuronal subtypes in the sea urchin embryo. Dev. Biol. 435, 138–149 (2018).
pubmed: 29331498
pmcid: 5837949
doi: 10.1016/j.ydbio.2017.12.015
Slota, L. A., Miranda, E. M. & McClay, D. R. Spatial and temporal patterns of gene expression during neurogenesis in the sea urchin Lytechinus variegatus. Evodevo 10, 2 (2019).
pubmed: 30792836
pmcid: 6371548
doi: 10.1186/s13227-019-0115-8
Barrera-Redondo, J., Lotharukpong, J. S., Drost, H.-G. & Coelho, S. M. Uncovering gene-family founder events during major evolutionary transitions in animals, plants and fungi using GenEra. Genome Biol. 24, 54 (2023).
pubmed: 36964572
pmcid: 10037820
doi: 10.1186/s13059-023-02895-z
Kiyokawa, H. et al. Airway basal stem cells reutilize the embryonic proliferation regulator, Tgfβ-Id2 axis, for tissue regeneration. Dev. Cell 56, 1917–1929.e9 (2021).
pubmed: 34129836
doi: 10.1016/j.devcel.2021.05.016
Zhou, Y. & Chen, J. J. STAT3 plays an important role in DNA replication by turning on WDHD1. Cell Biosci. 11, 10 (2021).
pubmed: 33413624
pmcid: 7792067
doi: 10.1186/s13578-020-00524-x
Angileri, K. M., Bagia, N. A. & Feschotte, C. Transposon control as a checkpoint for tissue regeneration. Development 149, dev191957 (2022).
pubmed: 36440631
pmcid: 10655923
doi: 10.1242/dev.191957
Hoch, W. Formation of the neuromuscular junction. Agrin and its unusual receptors. Eur. J. Biochem. 265, 1–10 (1999).
pubmed: 10491152
doi: 10.1046/j.1432-1327.1999.00765.x
Novinec, M., Kordis, D., Turk, V. & Lenarcic, B. Diversity and evolution of the thyroglobulin type-1 domain superfamily. Mol. Biol. Evol. 23, 744–755 (2006).
pubmed: 16368776
doi: 10.1093/molbev/msj082
Yan, A. et al. Identification and functional characterization of a novel antistasin/WAP-like serine protease inhibitor from the tropical sea cucumber, Stichopus monotuberculatus. Fish. Shellfish Immunol. 59, 203–212 (2016).
pubmed: 27989867
doi: 10.1016/j.fsi.2016.10.038
Elkasrawy, M. N. & Hamrick, M. W. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J. Musculoskelet. Neuronal Interact. 10, 56–63 (2010).
pubmed: 20190380
McCroskery, S. et al. Improved muscle healing through enhanced regeneration and reduced fibrosis in myostatin-null mice. J. Cell Sci. 118, 3531–3541 (2005).
pubmed: 16079293
doi: 10.1242/jcs.02482
Schiffer, P. H. et al. The slow evolving genome of the xenacoelomorph worm Xenoturbella bocki. Preprint at bioRxiv https://doi.org/10.1101/2022.06.24.497508 (2022).
Philippe, H. et al. Mitigating anticipated effects of systematic errors supports sister-group relationship between Xenacoelomorpha and Ambulacraria. Curr. Biol. 29, 1818–1826.e6 (2019).
pubmed: 31104936
doi: 10.1016/j.cub.2019.04.009
Arenas-Mena, C., Cameron, A. R. & Davidson, E. H. Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. Development 127, 4631–4643 (2000).
pubmed: 11023866
doi: 10.1242/dev.127.21.4631
Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764–770 (2011).
pubmed: 21217122
pmcid: 3051319
doi: 10.1093/bioinformatics/btr011
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
Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540–546 (2019).
pubmed: 30936562
doi: 10.1038/s41587-019-0072-8
Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 27, 737–746 (2017).
pubmed: 28100585
pmcid: 5411768
doi: 10.1101/gr.214270.116
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242
pmcid: 6137996
doi: 10.1093/bioinformatics/bty191
Rhie, A., Walenz, B. P., Koren, S. & Phillippy, A. M. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 21, 245 (2020).
pubmed: 32928274
pmcid: 7488777
doi: 10.1186/s13059-020-02134-9
Chen, Y., Zhang, Y., Wang, A. Y., Gao, M. & Chong, Z. Accurate long-read de novo assembly evaluation with Inspector. Genome Biol. 22, 312 (2021).
pubmed: 34775997
pmcid: 8590762
doi: 10.1186/s13059-021-02527-4
Guan, D. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896–2898 (2020).
pubmed: 31971576
pmcid: 7203741
doi: 10.1093/bioinformatics/btaa025
Open2C et al. Pairtools: from sequencing data to chromosome contacts. Preprint at bioRxiv https://doi.org/10.1101/2023.02.13.528389 (2023).
Zhou, C., McCarthy, S. A. & Durbin, R. YaHS: yet another Hi-C scaffolding tool. Bioinformatics 39, btac808 (2023).
pubmed: 36525368
doi: 10.1093/bioinformatics/btac808
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
Flynn, J. M. et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl Acad. Sci. USA 117, 9451–9457 (2020).
pubmed: 32300014
pmcid: 7196820
doi: 10.1073/pnas.1921046117
Yan, H., Bombarely, A. & Li, S. DeepTE: a computational method for de novo classification of transposons with convolutional neural network. Bioinformatics 36, 4269–4275 (2020).
pubmed: 32415954
doi: 10.1093/bioinformatics/btaa519
Bao, W., Kojima, K. K. & Kohany, O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob. DNA 6, 11 (2015).
pubmed: 26045719
pmcid: 4455052
doi: 10.1186/s13100-015-0041-9
Hubley, R. et al. The Dfam database of repetitive DNA families. Nucleic Acids Res. 44, D81–D89 (2016).
pubmed: 26612867
doi: 10.1093/nar/gkv1272
Parey, E. et al. Supplemental datasets for the brittle star A. filiformis genome. Zenodo https://doi.org/10.5281/zenodo.10785182 (2024).
Hubisz, M. J., Pollard, K. S. & Siepel, A. PHAST and RPHAST: phylogenetic analysis with space/time models. Brief. Bioinform. 12, 41–51 (2011).
pubmed: 21278375
doi: 10.1093/bib/bbq072
Parey, E. & Marlétaz, F. eparey/AnnotateSnakeMake: Genome Annotation Workflow v1.0.0. Zenodo https://doi.org/10.5281/zenodo.11084023 (2024).
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
Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res. 42, D222–D230 (2014).
pubmed: 24288371
doi: 10.1093/nar/gkt1223
Levy Karin, E., Mirdita, M. & Söding, J. MetaEuk-sensitive, high-throughput gene discovery, and annotation for large-scale eukaryotic metagenomics. Microbiome 8, 48 (2020).
pubmed: 32245390
pmcid: 7126354
doi: 10.1186/s40168-020-00808-x
Buchfink, B., Reuter, K. & Drost, H.-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368 (2021).
pubmed: 33828273
pmcid: 8026399
doi: 10.1038/s41592-021-01101-x
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
Hao, Z. et al. RIdeogram: drawing SVG graphics to visualize and map genome-wide data on the idiograms. PeerJ Comput Sci. 6, e251 (2020).
pubmed: 33816903
pmcid: 7924719
doi: 10.7717/peerj-cs.251
Kozlov, A. M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455 (2019).
pubmed: 31070718
pmcid: 6821337
doi: 10.1093/bioinformatics/btz305
Comte, N. et al. Treerecs: an integrated phylogenetic tool, from sequences to reconciliations. Bioinformatics 36, 4822–4824 (2020).
pubmed: 33085745
doi: 10.1093/bioinformatics/btaa615
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
Mendes, F. K., Vanderpool, D., Fulton, B. & Hahn, M. W. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 36, 5516–5518 (2020).
doi: 10.1093/bioinformatics/btaa1022
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 (eds Hedges, S. B. & Kumar, S.) 35–86 (Oxford Univ. Press, 2009).
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825–5829 (2021).
pubmed: 34597405
pmcid: 8662613
doi: 10.1093/molbev/msab293
Wu, T. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2, 100141 (2021).
pubmed: 34557778
pmcid: 8454663
Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800 (2011).
pubmed: 21789182
pmcid: 3138752
doi: 10.1371/journal.pone.0021800
Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
pubmed: 27043002
doi: 10.1038/nbt.3519
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
Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).
pubmed: 20196867
pmcid: 2864565
doi: 10.1186/gb-2010-11-3-r25
Kumar, L. & Futschik, M. E. Mfuzz: a software package for soft clustering of microarray data. Bioinformation 2, 5–7 (2007).
pubmed: 18084642
pmcid: 2139991
doi: 10.6026/97320630002005
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
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).
doi: 10.14806/ej.17.1.200
Schloissnig, S. et al. The giant axolotl genome uncovers the evolution, scaling, and transcriptional control of complex gene loci. Proc. Natl Acad. Sci. USA 118, e2017176118 (2021).
pubmed: 33827918
pmcid: 8053990
doi: 10.1073/pnas.2017176118
Boutet, E., Lieberherr, D., Tognolli, M., Schneider, M. & Bairoch, A. UniProtKB/Swiss-Prot. Methods Mol. Biol. 406, 89–112 (2007).
pubmed: 18287689
Jeong, H.-H., Yalamanchili, H. K., Guo, C., Shulman, J. M. & Liu, Z. An ultra-fast and scalable quantification pipeline for transposable elements from next generation sequencing data. Pac. Symp. Biocomput. 23, 168–179 (2018).
pubmed: 29218879
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
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
Freeman, R. et al. Identical genomic organization of two hemichordate hox clusters. Curr. Biol. 22, 2053–2058 (2012).
pubmed: 23063438
pmcid: 4524734
doi: 10.1016/j.cub.2012.08.052