Bichir external gills arise via heterochronic shift that accelerates hyoid arch development
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
1448514
Charles University Grant Agency - International
640016
Charles University Grant Agency - International
220213
Charles University Grant Agency - International
16-23836S
Czech Science Foundation - International
726516
Charles University Grant Agency - International
Grant SVV 260434/2019
Charles University - International
Research Centre program 204069
Charles University - International
1/0415/17
Vedecká Grantová Agentúra MŠVVaŠ SR a SAV - International
751066
H2020 Marie Skłodowska-Curie Actions - International
260434/2019
The Charles University grant SVV - International
204069
The Charles University Research Centre program - International
1/0415/17
The grant of the Scientific Grant Agency of Slovak Republic VEGA - International
751066
The European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant - International
PubMed
30910008
PubMed Central
PMC6440740
DOI
10.7554/elife.43531
PII: 43531
Knihovny.cz E-zdroje
- Klíčová slova
- bichir, breathing, developmental biology, evolutionary biology, external gills, head, pharynx,
- MeSH
- branchiální krajina embryologie MeSH
- rozvržení tělního plánu MeSH
- ryby embryologie MeSH
- vývojová regulace genové exprese MeSH
- žábry embryologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
In most vertebrates, pharyngeal arches form in a stereotypic anterior-to-posterior progression. To gain insight into the mechanisms underlying evolutionary changes in pharyngeal arch development, here we investigate embryos and larvae of bichirs. Bichirs represent the earliest diverged living group of ray-finned fishes, and possess intriguing traits otherwise typical for lobe-finned fishes such as ventral paired lungs and larval external gills. In bichir embryos, we find that the anteroposterior way of formation of cranial segments is modified by the unique acceleration of the entire hyoid arch segment, with earlier and orchestrated development of the endodermal, mesodermal, and neural crest tissues. This major heterochronic shift in the anteroposterior developmental sequence enables early appearance of the external gills that represent key breathing organs of bichir free-living embryos and early larvae. Bichirs thus stay as unique models for understanding developmental mechanisms facilitating increased breathing capacity.
Department of Theoretical Biology University of Vienna Vienna Austria
Department of Zoology Faculty of Science Charles University Prague Prague Czech Republic
Zobrazit více v PubMed
Abu-Issa R, Smyth G, Smoak I, Yamamura K, Meyers EN. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development. 2002;129:4613–4625. doi: 10.1242/dev.02408. PubMed DOI
Baltzinger M, Ori M, Pasqualetti M, Nardi I, Rijli FM. Hoxa2 knockdown in xenopus results in hyoid to mandibular homeosis. Developmental Dynamics : An Official Publication of the American Association of Anatomists. 2005;234:858–867. doi: 10.1002/dvdy.20567. PubMed DOI
Brand M, Granato M, Nusslein-Volhard C. Keeping and raising zebrafish. In: Nusslein-Volhard C, Dahm R, editors. In Zebrafish: A Practical Approach. Oxford University Press; 2002. pp. 7–37.
Cerny R, Meulemans D, Berger J, Wilsch-Bräuninger M, Kurth T, Bronner-Fraser M, Epperlein HH. Combined intrinsic and extrinsic influences pattern cranial neural crest migration and pharyngeal arch morphogenesis in axolotl. Developmental Biology. 2004;266:252–269. doi: 10.1016/j.ydbio.2003.09.039. PubMed DOI
Cheung M, Briscoe J. Neural crest development is regulated by the transcription factor Sox9. Development. 2003;130:5681–5693. doi: 10.1242/dev.00808. PubMed DOI
Choe CP, Crump JG. Dynamic epithelia of the developing vertebrate face. Current Opinion in Genetics & Development. 2015;32:66–72. doi: 10.1016/j.gde.2015.02.003. PubMed DOI PMC
Clack JA. Devonian climate change, breathing, and the origin of the tetrapod stem group. Integrative and Comparative Biology. 2007;47:510–523. doi: 10.1093/icb/icm055. PubMed DOI
Coates MI, Clack JA. Fish-like gills and breathing in the earliest known tetrapod. Nature. 1991;352:234–236. doi: 10.1038/352234a0. DOI
Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development. 2002;129:1061–1073. PubMed
Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development. 2004;131:5703–5716. doi: 10.1242/dev.01444. PubMed DOI
Diedhiou S, Bartsch P. Staging of the early development of Polypterus (Cladistia: Actinopterygii) In: Kunz-Ramsay Y. W, Luer C. A, Kapoor B. G, editors. Development of Non-Teleost Fishes. Enfield: Science Publishers; 2009. pp. 104–109. DOI
Duellman WE, Trueb L. Biology of Amphibians. New York: McGraw-Hill; 1994.
Ericsson R, Cerny R, Falck P, Olsson L. Role of cranial neural crest cells in visceral arch muscle positioning and morphogenesis in the mexican axolotl, ambystoma mexicanum. Developmental Dynamics. 2004;231:237–247. doi: 10.1002/dvdy.20127. PubMed DOI
Giles S, Xu GH, Near TJ, Friedman M. Early members of 'living fossil' lineage imply later origin of modern ray-finned fishes. Nature. 2017;549:265–268. doi: 10.1038/nature23654. PubMed DOI
Gillis JA, Fritzenwanker JH, Lowe CJ. A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proceedings of the Royal Society B: Biological Sciences. 2012;279:237–246. doi: 10.1098/rspb.2011.0599. PubMed DOI PMC
Gillis JA, Tidswell OR. The origin of vertebrate gills. Current Biology. 2017;27:729–732. doi: 10.1016/j.cub.2017.01.022. PubMed DOI PMC
Goodrich ES. Vertebrata Craniata (first fascicle: cyclostomes and fishes) In: Lankester R, editor. Treatise on Zoology. Part 9. London: Adam and Charles Black; 1909.
Graham A. Deconstructing the pharyngeal metamere. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2008;310:336–344. doi: 10.1002/jez.b.21182. PubMed DOI
Graham JB, Wegner NC, Miller LA, Jew CJ, Lai NC, Berquist RM, Frank LR, Long JA. Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods. Nature Communications. 2014;5:3022. doi: 10.1038/ncomms4022. PubMed DOI
Graham A, Smith A. Patterning the pharyngeal arches. BioEssays. 2001;23:54–61. doi: 10.1002/1521-1878(200101)23:1<54::AID-BIES1007>3.0.CO;2-5. PubMed DOI
Grevellec A, Tucker AS. The pharyngeal pouches and clefts: development, evolution, structure and derivatives. Seminars in Cell & Developmental Biology. 2010;21:325–332. doi: 10.1016/j.semcdb.2010.01.022. PubMed DOI
Hughes LC, Ortí G, Huang Y, Sun Y, Baldwin CC, Thompson AW, Arcila D, Betancur-R R, Li C, Becker L, Bellora N, Zhao X, Li X, Wang M, Fang C, Xie B, Zhou Z, Huang H, Chen S, Venkatesh B, Shi Q. Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data. PNAS. 2018;115:6249–6254. doi: 10.1073/pnas.1719358115. PubMed DOI PMC
Hunter MP, Prince VE. Zebrafish hox paralogue group 2 genes function redundantly as selector genes to pattern the second pharyngeal arch. Developmental Biology. 2002;247:367–389. doi: 10.1006/dbio.2002.0701. PubMed DOI
Jandzik D, Hawkins MB, Cattell MV, Cerny R, Square TA, Medeiros DM. Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head. Development. 2014;141:629–638. doi: 10.1242/dev.097261. PubMed DOI
Kerr JG. The development of Polypterus senegalus Cuvier. In: Kerr J. G, editor. Budget Memorial Volume. Cambridge: Cambridge University Press; 1907.
Köntges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996;122:3229–3242. PubMed
Koop D, Chen J, Theodosiou M, Carvalho JE, Alvarez S, de Lera AR, Holland LZ, Schubert M. Roles of retinoic acid and Tbx1/10 in pharyngeal segmentation: amphioxus and the ancestral chordate condition. EvoDevo. 2014;5:36. doi: 10.1186/2041-9139-5-36. PubMed DOI PMC
Lumsden A, Sprawson N, Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development. 1991;113:1281–1291. PubMed
Metscher BD. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Developmental Dynamics. 2009;238:632–640. doi: 10.1002/dvdy.21857. PubMed DOI
Minarik M, Stundl J, Fabian P, Jandzik D, Metscher BD, Psenicka M, Gela D, Osorio-Pérez A, Arias-Rodriguez L, Horácek I, Cerny R. Pre-oral gut contributes to facial structures in non-teleost fishes. Nature. 2017;547:209–212. doi: 10.1038/nature23008. PubMed DOI
Minoux M, Rijli FM. Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development. 2010;137:2605–2621. doi: 10.1242/dev.040048. PubMed DOI
Mitgutsch C, Piekarski N, Olsson L, Haas A. Heterochronic shifts during early cranial neural crest cell migration in two ranid frogs. Acta Zoologica. 2008;89:69–78. doi: 10.1111/j.1463-6395.2007.00295.x. DOI
Mori-Akiyama Y, Akiyama H, Rowitch DH, de Crombrugghe B. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. PNAS. 2003;100:9360–9365. doi: 10.1073/pnas.1631288100. PubMed DOI PMC
Noda M, Miyake T, Okabe M. Development of cranial muscles in the actinopterygian fish Senegal bichir, Polypterus senegalus Cuvier, 1829. Journal of Morphology. 2017;278:450–463. doi: 10.1002/jmor.20636. PubMed DOI
Nokhbatolfoghahai M, Downie JR. The external gills of anuran amphibians: comparative morphology and ultrastructure. Journal of Morphology. 2008;269:1197–1213. doi: 10.1002/jmor.10655. PubMed DOI
Piotrowski T, Nüsslein-Volhard C. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio) Developmental Biology. 2000;225:339–356. doi: 10.1006/dbio.2000.9842. PubMed DOI
Quinlan R, Martin P, Graham A. The role of actin cables in directing the morphogenesis of the pharyngeal pouches. Development. 2004;131:593–599. doi: 10.1242/dev.00950. PubMed DOI
Richardson J, Shono T, Okabe M, Graham A. The presence of an embryonic opercular flap in amniotes. Proceedings of the Royal Society B: Biological Sciences. 2012;279:224–229. doi: 10.1098/rspb.2011.0740. PubMed DOI PMC
Rijli FM, Mark M, Lakkaraju S, Dierich A, Dollé P, Chambon P. A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell. 1993;75:1333–1349. doi: 10.1016/0092-8674(93)90620-6. PubMed DOI
Santagati F, Rijli FM. Cranial neural crest and the building of the vertebrate head. Nature Reviews Neuroscience. 2003;4:806–818. doi: 10.1038/nrn1221. PubMed DOI
Schilling TF. Anterior-posterior patterning and segmentation of the vertebrate head. Integrative and Comparative Biology. 2008;48:658–667. doi: 10.1093/icb/icn081. PubMed DOI PMC
Schoch RR, Witzmann F. Bystrow’s Paradox - gills, fossils, and the fish-to-tetrapod transition. Acta Zoologica. 2011;92:251–265. doi: 10.1111/j.1463-6395.2010.00456.x. DOI
Shone V, Graham A. Endodermal/ectodermal interfaces during pharyngeal segmentation in vertebrates. Journal of Anatomy. 2014;225:479–491. doi: 10.1111/joa.12234. PubMed DOI PMC
Square T, Jandzik D, Romášek M, Cerny R, Medeiros DM. The origin and diversification of the developmental mechanisms that pattern the vertebrate head skeleton. Developmental Biology. 2017;427:219–229. doi: 10.1016/j.ydbio.2016.11.014. PubMed DOI
Standen EM, Du TY, Larsson HC. Developmental plasticity and the origin of tetrapods. Nature. 2014;513:54–58. doi: 10.1038/nature13708. PubMed DOI
Takeuchi M, Okabe M, Aizawa S. The genus polypterus (Bichirs): A fish group diverged at the stem of Ray-Finned fishes (Actinopterygii) Cold Spring Harbor Protocols. 2009;2009:emo117. doi: 10.1101/pdb.emo117. PubMed DOI
Tatsumi N, Kobayashi R, Yano T, Noda M, Fujimura K, Okada N, Okabe M. Molecular developmental mechanism in polypterid fish provides insight into the origin of vertebrate lungs. Scientific Reports. 2016;6:30580. doi: 10.1038/srep30580. PubMed DOI PMC
Theveneau E, Mayor R. Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Developmental Biology. 2012;366:34–54. doi: 10.1016/j.ydbio.2011.12.041. PubMed DOI
Tokita M, Schneider RA. Developmental origins of species-specific muscle pattern. Developmental Biology. 2009;331:311–325. doi: 10.1016/j.ydbio.2009.05.548. PubMed DOI PMC
Walshe J, Mason I. Fgf signalling is required for formation of cartilage in the head. Developmental Biology. 2003;264:522–536. doi: 10.1016/j.ydbio.2003.08.010. PubMed DOI
Warga RM, Nüsslein-Volhard C. Origin and development of the zebrafish endoderm. Development. 1999;126:827–838. PubMed
Willey A. The later larval development of amphioxus. The Quarterly Journal of Microscopical Science. 1891;32:183–234.
Witzmann F. The external gills of paleozoic amphibians. Neues Jahrbuch Für Geologie Und Paläontologie Abhandlungen. 2004;232:375–401.
Sturgeon gut development: a unique yolk utilization strategy among vertebrates
Pre-mandibular pharyngeal pouches in early non-teleost fish embryos
Evolution of the nitric oxide synthase family in vertebrates and novel insights in gill development
The conundrum of pharyngeal teeth origin: the role of germ layers, pouches, and gill slits
Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes