The evolutionary origin of bilaterian smooth and striated myocytes
Abstract
The dichotomy between smooth and striated myocytes is fundamental for bilaterian musculature, but its evolutionary origin is unsolved. In particular, interrelationships of visceral smooth muscles remain unclear. Absent in fly and nematode, they have not yet been characterized molecularly outside vertebrates. Here, we characterize expression profile, ultrastructure, contractility and innervation of the musculature in the marine annelid Platynereis dumerilii and identify smooth muscles around the midgut, hindgut and heart that resemble their vertebrate counterparts in molecular fingerprint, contraction speed, and nervous control. Our data suggest that both visceral smooth and somatic striated myocytes were present in the protostome-deuterostome ancestor, and that smooth myocytes later co-opted the striated contractile module repeatedly - for example in vertebrate heart evolution. During these smooth-to-striated myocyte conversions the core regulatory complex of transcription factors conveying myocyte identity remained unchanged, reflecting a general principle in cell type evolution.
Article and author information
Author details
Funding
European Research Council (Brain Evo-Devo)
- Thibaut Brunet
- Paola Bertucci
- Detlev Arendt
European Union's Seventh Framework Program (EVONET)
- Antonella Lauri
European Union-Marie Curie Early Training Network (ZOONET)
- Antje HL Fischer
European Molecular Biology Laboratory (International PhD Program)
- Thibaut Brunet
- Antje HL Fischer
- Patrick RH Steinmetz
- Antonella Lauri
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Alejandro Sánchez Alvarado, Stowers Institute for Medical Research, United States
Publication history
- Received: July 13, 2016
- Accepted: December 1, 2016
- Accepted Manuscript published: December 1, 2016 (version 1)
- Accepted Manuscript updated: December 2, 2016 (version 2)
- Version of Record published: December 19, 2016 (version 3)
Copyright
© 2016, Brunet et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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Development of tooth shape is regulated by the enamel knot signalling centre, at least in mammals. Fgf signalling regulates differential proliferation between the enamel knot and adjacent dental epithelia during tooth development, leading to formation of the dental cusp. The presence of an enamel knot in non-mammalian vertebrates is debated given differences in signalling. Here, we show the conservation and restriction of fgf3, fgf10, and shh to the sites of future dental cusps in the shark (Scyliorhinus canicula), whilst also highlighting striking differences between the shark and mouse. We reveal shifts in tooth size, shape, and cusp number following small molecule perturbations of canonical Wnt signalling. Resulting tooth phenotypes mirror observed effects in mammals, where canonical Wnt has been implicated as an upstream regulator of enamel knot signalling. In silico modelling of shark dental morphogenesis demonstrates how subtle changes in activatory and inhibitory signals can alter tooth shape, resembling developmental phenotypes and cusp shapes observed following experimental Wnt perturbation. Our results support the functional conservation of an enamel knot-like signalling centre throughout vertebrates and suggest that varied tooth types from sharks to mammals follow a similar developmental bauplan. Lineage-specific differences in signalling are not sufficient in refuting homology of this signalling centre, which is likely older than teeth themselves.
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- Developmental Biology
- Evolutionary Biology
The tooth shape of sharks and mice are regulated by a similar signaling center despite their teeth having very different geometries.