Post-metamorphic skeletal growth in the sea urchin Paracentrotus lividus and implications for body plan evolution.

Development Echinoid Skeleton

Journal

EvoDevo
ISSN: 2041-9139
Titre abrégé: Evodevo
Pays: England
ID NLM: 101525836

Informations de publication

Date de publication:
16 Mar 2021
Historique:
received: 08 12 2020
accepted: 02 03 2021
entrez: 17 3 2021
pubmed: 18 3 2021
medline: 18 3 2021
Statut: epublish

Résumé

Understanding the molecular and cellular processes that underpin animal development are crucial for understanding the diversity of body plans found on the planet today. Because of their abundance in the fossil record, and tractability as a model system in the lab, skeletons provide an ideal experimental model to understand the origins of animal diversity. We herein use molecular and cellular markers to understand the growth and development of the juvenile sea urchin (echinoid) skeleton. We developed a detailed staging scheme based off of the first ~ 4 weeks of post-metamorphic life of the regular echinoid Paracentrotus lividus. We paired this scheme with immunohistochemical staining for neuronal, muscular, and skeletal tissues, and fluorescent assays of skeletal growth and cell proliferation to understand the molecular and cellular mechanisms underlying skeletal growth and development of the sea urchin body plan. Our experiments highlight the role of skeletogenic proteins in accretionary skeletal growth and cell proliferation in the addition of new metameric tissues. Furthermore, this work provides a framework for understanding the developmental evolution of sea urchin body plans on macroevolutionary timescales.

Sections du résumé

BACKGROUND BACKGROUND
Understanding the molecular and cellular processes that underpin animal development are crucial for understanding the diversity of body plans found on the planet today. Because of their abundance in the fossil record, and tractability as a model system in the lab, skeletons provide an ideal experimental model to understand the origins of animal diversity. We herein use molecular and cellular markers to understand the growth and development of the juvenile sea urchin (echinoid) skeleton.
RESULTS RESULTS
We developed a detailed staging scheme based off of the first ~ 4 weeks of post-metamorphic life of the regular echinoid Paracentrotus lividus. We paired this scheme with immunohistochemical staining for neuronal, muscular, and skeletal tissues, and fluorescent assays of skeletal growth and cell proliferation to understand the molecular and cellular mechanisms underlying skeletal growth and development of the sea urchin body plan.
CONCLUSIONS CONCLUSIONS
Our experiments highlight the role of skeletogenic proteins in accretionary skeletal growth and cell proliferation in the addition of new metameric tissues. Furthermore, this work provides a framework for understanding the developmental evolution of sea urchin body plans on macroevolutionary timescales.

Identifiants

pubmed: 33726833
doi: 10.1186/s13227-021-00174-1
pii: 10.1186/s13227-021-00174-1
pmc: PMC7968366
doi:

Types de publication

Journal Article

Langues

eng

Pagination

3

Références

Nature. 2016 Mar 31;531(7596):637-641
pubmed: 26886793
Dev Genes Evol. 2009 Mar;219(3):159-66
pubmed: 19238430
Front Zool. 2016 Apr 22;13:18
pubmed: 27110269
J Comp Neurol. 2006 May 10;496(2):244-51
pubmed: 16538680
Development. 2012 Feb;139(3):579-90
pubmed: 22190640
Proc Biol Sci. 2009 Apr 7;276(1660):1277-84
pubmed: 19129140
J Struct Biol. 2013 Aug;183(2):199-204
pubmed: 23583702
Dev Biol. 2015 Apr 1;400(1):148-58
pubmed: 25641694
J Histochem Cytochem. 1999 Sep;47(9):1189-200
pubmed: 10449540
J Comp Neurol. 2021 Apr 15;529(6):1135-1156
pubmed: 32841380
Science. 2006 Feb 10;311(5762):796-800
pubmed: 16469913
J Exp Zool B Mol Dev Evol. 2005 Sep 15;304(5):456-67
pubmed: 16075458
Development. 2017 May 15;144(10):1896-1905
pubmed: 28432218
BMC Evol Biol. 2018 Dec 13;18(1):189
pubmed: 30545284
Dev Genes Evol. 2009 Dec;219(11-12):597-608
pubmed: 20229180
Evol Dev. 2011 Jul-Aug;13(4):370-81
pubmed: 21740510
Genesis. 2014 Mar;52(3):251-68
pubmed: 24376127
Proteome Sci. 2010 Jun 17;8:33
pubmed: 20565753
Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8403-8408
pubmed: 30967509
Syst Biol. 2020 Sep 03;:
pubmed: 32882040
Proteome Sci. 2008 Dec 09;6:33
pubmed: 19068105
Biol Rev Camb Philos Soc. 2020 Oct;95(5):1372-1392
pubmed: 32447836
Gene Expr Patterns. 2014 Nov;16(2):93-103
pubmed: 25460514
Proteome Sci. 2008 Aug 11;6:22
pubmed: 18694502
Development. 2016 Jan 15;143(2):286-97
pubmed: 26511925
Nature. 2003 May 15;423(6937):332-6
pubmed: 12748651
Sci Rep. 2015 Oct 21;5:15541
pubmed: 26486232
Proc Natl Acad Sci U S A. 2015 Mar 24;112(12):3758-63
pubmed: 25713369
Dev Genes Evol. 2012 Nov;222(6):313-23
pubmed: 23001286
Development. 1997 May;124(10):1899-908
pubmed: 9169837
Sci Rep. 2020 Feb 6;10(1):1973
pubmed: 32029769
Dev Biol. 1988 Feb;125(2):396-409
pubmed: 3338620
Dev Genes Evol. 2014 Feb;224(1):1-11
pubmed: 24129745
Proc Biol Sci. 2007 Jun 22;274(1617):1511-6
pubmed: 17439856
Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):5955-62
pubmed: 18413610
Evol Dev. 2004 Mar-Apr;6(2):95-104
pubmed: 15009122

Auteurs

Jeffrey R Thompson (JR)

Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK. jeff.thompson@ucl.ac.uk.
UCL Center for Life's Origins and Evolution, London, UK. jeff.thompson@ucl.ac.uk.

Periklis Paganos (P)

Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy.

Giovanna Benvenuto (G)

Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy.

Maria Ina Arnone (MI)

Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy.

Paola Oliveri (P)

Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK. p.oliveri@ucl.ac.uk.
UCL Center for Life's Origins and Evolution, London, UK. p.oliveri@ucl.ac.uk.

Classifications MeSH