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Genetic regulation of amphioxus somitogenesis informs the evolution of the vertebrate head mesoderm.
Nat Ecol Evol 2019; 3(8):1233-1240NE

Abstract

The evolution of vertebrates from an ancestral chordate was accompanied by the acquisition of a predatory lifestyle closely associated to the origin of a novel anterior structure, the highly specialized head. While the vertebrate head mesoderm is unsegmented, the paraxial mesoderm of the earliest divergent chordate clade, the cephalochordates (amphioxus), is fully segmented in somites. We have previously shown that fibroblast growth factor signalling controls the formation of the most anterior somites in amphioxus; therefore, unravelling the fibroblast growth factor signalling downstream effectors is of crucial importance to shed light on the evolutionary origin of vertebrate head muscles. By using a comparative RNA sequencing approach and genetic functional analyses, we show that several transcription factors, such as Six1/2, Pax3/7 and Zic, act in combination to ensure the formation of three different somite populations. Interestingly, these proteins are orthologous to key regulators of trunk, and not head, muscle formation in vertebrates. Contrary to prevailing thinking, our results suggest that the vertebrate head mesoderm is of visceral and not paraxial origin and support a multistep evolutionary scenario for the appearance of the unsegmented mesoderm of the vertebrates new 'head'.

Authors+Show Affiliations

Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls-sur-Mer, France.Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls-sur-Mer, France.Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), INSERM, U1258, CNRS, UMR7104, Université de Strasbourg, Illkirch-Graffenstaden, France.Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls-sur-Mer, France.Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.Laboratory of Development and Evolution, Department of Cell Biology, Faculty of Biological Sciences, University of Concepción, Concepción, Chile.Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls-sur-Mer, France. stephanie.bertrand@obs-banyuls.fr.Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls-sur-Mer, France. hescriva@obs-banyuls.fr.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31263232

Citation

Aldea, Daniel, et al. "Genetic Regulation of Amphioxus Somitogenesis Informs the Evolution of the Vertebrate Head Mesoderm." Nature Ecology & Evolution, vol. 3, no. 8, 2019, pp. 1233-1240.
Aldea D, Subirana L, Keime C, et al. Genetic regulation of amphioxus somitogenesis informs the evolution of the vertebrate head mesoderm. Nat Ecol Evol. 2019;3(8):1233-1240.
Aldea, D., Subirana, L., Keime, C., Meister, L., Maeso, I., Marcellini, S., ... Escriva, H. (2019). Genetic regulation of amphioxus somitogenesis informs the evolution of the vertebrate head mesoderm. Nature Ecology & Evolution, 3(8), pp. 1233-1240. doi:10.1038/s41559-019-0933-z.
Aldea D, et al. Genetic Regulation of Amphioxus Somitogenesis Informs the Evolution of the Vertebrate Head Mesoderm. Nat Ecol Evol. 2019;3(8):1233-1240. PubMed PMID: 31263232.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genetic regulation of amphioxus somitogenesis informs the evolution of the vertebrate head mesoderm. AU - Aldea,Daniel, AU - Subirana,Lucie, AU - Keime,Celine, AU - Meister,Lydvina, AU - Maeso,Ignacio, AU - Marcellini,Sylvain, AU - Gomez-Skarmeta,Jose Luis, AU - Bertrand,Stephanie, AU - Escriva,Hector, Y1 - 2019/07/01/ PY - 2019/03/15/received PY - 2019/05/22/accepted PY - 2019/7/3/pubmed PY - 2019/7/3/medline PY - 2019/7/3/entrez SP - 1233 EP - 1240 JF - Nature ecology & evolution JO - Nat Ecol Evol VL - 3 IS - 8 N2 - The evolution of vertebrates from an ancestral chordate was accompanied by the acquisition of a predatory lifestyle closely associated to the origin of a novel anterior structure, the highly specialized head. While the vertebrate head mesoderm is unsegmented, the paraxial mesoderm of the earliest divergent chordate clade, the cephalochordates (amphioxus), is fully segmented in somites. We have previously shown that fibroblast growth factor signalling controls the formation of the most anterior somites in amphioxus; therefore, unravelling the fibroblast growth factor signalling downstream effectors is of crucial importance to shed light on the evolutionary origin of vertebrate head muscles. By using a comparative RNA sequencing approach and genetic functional analyses, we show that several transcription factors, such as Six1/2, Pax3/7 and Zic, act in combination to ensure the formation of three different somite populations. Interestingly, these proteins are orthologous to key regulators of trunk, and not head, muscle formation in vertebrates. Contrary to prevailing thinking, our results suggest that the vertebrate head mesoderm is of visceral and not paraxial origin and support a multistep evolutionary scenario for the appearance of the unsegmented mesoderm of the vertebrates new 'head'. SN - 2397-334X UR - https://www.unboundmedicine.com/medline/citation/31263232/Genetic_regulation_of_amphioxus_somitogenesis_informs_the_evolution_of_the_vertebrate_head_mesoderm L2 - http://dx.doi.org/10.1038/s41559-019-0933-z DB - PRIME DP - Unbound Medicine ER -