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Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes

Stundl, Jan and Pospisilova, Anna and Matějková, Tereza and Psenicka, Martin and Bronner, Marianne E. and Cerny, Robert (2020) Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes. Developmental Biology, 467 (1-2). pp. 14-29. ISSN 0012-1606. https://resolver.caltech.edu/CaltechAUTHORS:20200831-143448217

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Abstract

The cranial neural crest (CNC) arises within the developing central nervous system, but then migrates away from the neural tube in three consecutive streams termed mandibular, hyoid and branchial, respectively, according to the order along the anteroposterior axis. While the process of neural crest emigration generally follows a conserved anterior to posterior sequence across vertebrates, we find that ray-finned fishes (bichir, sterlet, gar, and pike) exhibit several heterochronies in the timing and order of CNC emergence that influences their subsequent migratory patterns. First, emigration of the cranial neural crest in these fishes occurs prematurely compared to other vertebrates, already initiating during early neurulation and well before neural tube closure. Second, delamination of the hyoid stream occurs prior to the more anterior mandibular stream; this is associated with early morphogenesis of key hyoid structures like external gills (bichir), a large opercular flap (gar) or first forming cartilage (pike). In sterlet, the hyoid and branchial CNC cells form a single hyobranchial sheet, which later segregates in concert with second pharyngeal pouch morphogenesis. Taken together, the results show that despite generally conserved migratory patterns, heterochronic alterations in the timing of emigration and pattern of migration of CNC cells accompanies morphological diversity of ray-finned fishes.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.ydbio.2020.08.007DOIArticle
ORCID:
AuthorORCID
Psenicka, Martin0000-0002-3808-7856
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2020 Elsevier Inc. Received 27 April 2020, Revised 13 August 2020, Accepted 14 August 2020, Available online 21 August 2020. We thank Vojtěch Miller and Karel Kodejš for the bichir colony care and logistic support; Roman Franěk, Michaela Fučíková, David Gela, Martin Kahanec and Marek Rodina for the sterlet spawns; Lenin Arias-Rodriguez and Adriana Osorio-Pérez for the gar spawns; Radek Holcman for the northern pike spawns; Peter Fabian (ISH), and Brian D. Metscher (microCT) for technical assistance; Martin Minařík for the pharyngeal endoderm reconstructions of the sterlet David Jandzik for the generous gift of primer sequences of Hand2_Ps; Vladimir Soukup and Jana Štundlová for critical reading of the manuscript. Special thanks are due to Radek Šanda for the support and continuous interest in our work. This study was supported by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 897949 (to JS), the Charles University grant GAUK 1448514 (to JS), NIH R35NS111564 (to MEB), the Czech Science Foundation GACR 19-18634S (to RC), and the Ministry of Education, Youth and Sports of the Czech Republic—project CENAKVA LM2018099 and Biodiversity CZ.02.1.01/0.0/0.0/16_025/0007370) (to MP).
Funders:
Funding AgencyGrant Number
Marie Curie Fellowship897949
Charles University1448514
NIHR35NS111564
Czech Science Foundation19-18634S
Ministry of Education, Youth and Sports (Czech Republic)CENAKVA LM2018099
Ministry of Education, Youth and Sports (Czech Republic)CZ.02.1.01/0.0/0.0/16_025/0007370
Subject Keywords:Neural crest; Vertebrates; Craniofacial; Evolution; Neurulation
Issue or Number:1-2
Record Number:CaltechAUTHORS:20200831-143448217
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200831-143448217
Official Citation:Jan Stundl, Anna Pospisilova, Tereza Matějková, Martin Psenicka, Marianne E. Bronner, Robert Cerny, Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes, Developmental Biology, Volume 467, Issues 1–2, 2020, Pages 14-29, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2020.08.007. (http://www.sciencedirect.com/science/article/pii/S0012160620302281)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105180
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:08 Sep 2020 19:07
Last Modified:10 Sep 2020 19:49

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