Cargando…

An Updated Staging System for Cephalochordate Development: One Table Suits Them All

Chordates are divided into three subphyla: Vertebrata, Tunicata, and Cephalochordata. Phylogenetically, the Cephalochordata, more commonly known as lancelets or amphioxus, constitute the sister group of Vertebrata and Tunicata. Lancelets are small, benthic, marine filter feeders, and their roughly t...

Descripción completa

Detalles Bibliográficos
Autores principales: Carvalho, João E., Lahaye, François, Yong, Luok Wen, Croce, Jenifer C., Escrivá, Hector, Yu, Jr-Kai, Schubert, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8174843/
https://www.ncbi.nlm.nih.gov/pubmed/34095136
http://dx.doi.org/10.3389/fcell.2021.668006
_version_ 1783702975382814720
author Carvalho, João E.
Lahaye, François
Yong, Luok Wen
Croce, Jenifer C.
Escrivá, Hector
Yu, Jr-Kai
Schubert, Michael
author_facet Carvalho, João E.
Lahaye, François
Yong, Luok Wen
Croce, Jenifer C.
Escrivá, Hector
Yu, Jr-Kai
Schubert, Michael
author_sort Carvalho, João E.
collection PubMed
description Chordates are divided into three subphyla: Vertebrata, Tunicata, and Cephalochordata. Phylogenetically, the Cephalochordata, more commonly known as lancelets or amphioxus, constitute the sister group of Vertebrata and Tunicata. Lancelets are small, benthic, marine filter feeders, and their roughly three dozen described species are divided into three genera: Branchiostoma, Epigonichthys, and Asymmetron. Due to their phylogenetic position and their stereotypical chordate morphology and genome architecture, lancelets are key models for understanding the evolutionary history of chordates. Lancelets have thus been studied by generations of scientists, with the first descriptions of adult anatomy and developmental morphology dating back to the 19th century. Today, several different lancelet species are used as laboratory models, predominantly for developmental, molecular and genomic studies. Surprisingly, however, a universal staging system and an unambiguous nomenclature for developing lancelets have not yet been adopted by the scientific community. In this work, we characterized the development of the European lancelet (Branchiostoma lanceolatum) using confocal microscopy and compiled a streamlined developmental staging system, from fertilization through larval life, including an unambiguous stage nomenclature. By tracing growth curves of the European lancelet reared at different temperatures, we were able to show that our staging system permitted an easy conversion of any developmental time into a specific stage name. Furthermore, comparisons of embryos and larvae from the European lancelet (B. lanceolatum), the Florida lancelet (Branchiostoma floridae), two Asian lancelets (Branchiostoma belcheri and Branchiostoma japonicum), and the Bahamas lancelet (Asymmetron lucayanum) demonstrated that our staging system could readily be applied to other lancelet species. Although the detailed staging description was carried out on developing B. lanceolatum, the comparisons with other lancelet species thus strongly suggested that both staging and nomenclature are applicable to all extant lancelets. We conclude that this description of embryonic and larval development will be of great use for the scientific community and that it should be adopted as the new standard for defining and naming developing lancelets. More generally, we anticipate that this work will facilitate future studies comparing representatives from different chordate lineages.
format Online
Article
Text
id pubmed-8174843
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-81748432021-06-04 An Updated Staging System for Cephalochordate Development: One Table Suits Them All Carvalho, João E. Lahaye, François Yong, Luok Wen Croce, Jenifer C. Escrivá, Hector Yu, Jr-Kai Schubert, Michael Front Cell Dev Biol Cell and Developmental Biology Chordates are divided into three subphyla: Vertebrata, Tunicata, and Cephalochordata. Phylogenetically, the Cephalochordata, more commonly known as lancelets or amphioxus, constitute the sister group of Vertebrata and Tunicata. Lancelets are small, benthic, marine filter feeders, and their roughly three dozen described species are divided into three genera: Branchiostoma, Epigonichthys, and Asymmetron. Due to their phylogenetic position and their stereotypical chordate morphology and genome architecture, lancelets are key models for understanding the evolutionary history of chordates. Lancelets have thus been studied by generations of scientists, with the first descriptions of adult anatomy and developmental morphology dating back to the 19th century. Today, several different lancelet species are used as laboratory models, predominantly for developmental, molecular and genomic studies. Surprisingly, however, a universal staging system and an unambiguous nomenclature for developing lancelets have not yet been adopted by the scientific community. In this work, we characterized the development of the European lancelet (Branchiostoma lanceolatum) using confocal microscopy and compiled a streamlined developmental staging system, from fertilization through larval life, including an unambiguous stage nomenclature. By tracing growth curves of the European lancelet reared at different temperatures, we were able to show that our staging system permitted an easy conversion of any developmental time into a specific stage name. Furthermore, comparisons of embryos and larvae from the European lancelet (B. lanceolatum), the Florida lancelet (Branchiostoma floridae), two Asian lancelets (Branchiostoma belcheri and Branchiostoma japonicum), and the Bahamas lancelet (Asymmetron lucayanum) demonstrated that our staging system could readily be applied to other lancelet species. Although the detailed staging description was carried out on developing B. lanceolatum, the comparisons with other lancelet species thus strongly suggested that both staging and nomenclature are applicable to all extant lancelets. We conclude that this description of embryonic and larval development will be of great use for the scientific community and that it should be adopted as the new standard for defining and naming developing lancelets. More generally, we anticipate that this work will facilitate future studies comparing representatives from different chordate lineages. Frontiers Media S.A. 2021-05-20 /pmc/articles/PMC8174843/ /pubmed/34095136 http://dx.doi.org/10.3389/fcell.2021.668006 Text en Copyright © 2021 Carvalho, Lahaye, Yong, Croce, Escrivá, Yu and Schubert. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Carvalho, João E.
Lahaye, François
Yong, Luok Wen
Croce, Jenifer C.
Escrivá, Hector
Yu, Jr-Kai
Schubert, Michael
An Updated Staging System for Cephalochordate Development: One Table Suits Them All
title An Updated Staging System for Cephalochordate Development: One Table Suits Them All
title_full An Updated Staging System for Cephalochordate Development: One Table Suits Them All
title_fullStr An Updated Staging System for Cephalochordate Development: One Table Suits Them All
title_full_unstemmed An Updated Staging System for Cephalochordate Development: One Table Suits Them All
title_short An Updated Staging System for Cephalochordate Development: One Table Suits Them All
title_sort updated staging system for cephalochordate development: one table suits them all
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8174843/
https://www.ncbi.nlm.nih.gov/pubmed/34095136
http://dx.doi.org/10.3389/fcell.2021.668006
work_keys_str_mv AT carvalhojoaoe anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT lahayefrancois anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT yongluokwen anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT crocejeniferc anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT escrivahector anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT yujrkai anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT schubertmichael anupdatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT carvalhojoaoe updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT lahayefrancois updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT yongluokwen updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT crocejeniferc updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT escrivahector updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT yujrkai updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall
AT schubertmichael updatedstagingsystemforcephalochordatedevelopmentonetablesuitsthemall