An amphioxus neurula stage cell atlas supports a complex scenario for the emergence of vertebrate head mesoderm

• Published in: Nature communications 2024-05, Vol.15 (1), p.4550-18, Article 4550
• Main Authors: Grau-Bové, Xavier, Subirana, Lucie, Meister, Lydvina, Soubigou, Anaël, Neto, Ana, Elek, Anamaria, Naranjo, Silvia, Fornas, Oscar, Gomez-Skarmeta, Jose Luis, Tena, Juan J., Irimia, Manuel, Bertrand, Stéphanie, Sebé-Pedrós, Arnau, Escriva, Hector
• Format: Article
• Language: English
• Subjects: 38/32; 38/91; 49/23; 631/136/1660/1986; 631/136/2086/2126; 631/181/2806; 82/51; Animals; Biological Evolution; Cells; Cephalochordata; Embryogenesis; Embryos; Evolution; Evolutionary genetics; Gene expression; Gene Expression Regulation, Developmental; Head; Head - embryology; Homology; Humanities and Social Sciences; Lancelets - embryology; Lancelets - genetics; Life Sciences; Mesoderm; Mesoderm - cytology; Mesoderm - embryology; Morphology; multidisciplinary; Muscles; Myogenesis; Pharynx; Populations; Science; Science (multidisciplinary); Somites; Somites - cytology; Somites - embryology; Somites - metabolism; Transcriptome; Transcriptomics; Vertebrates; Vertebrates - embryology; Vertebrates - genetics
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-48774-4

The emergence of new structures can often be linked to the evolution of novel cell types that follows the rewiring of developmental gene regulatory subnetworks. Vertebrates are characterized by a complex body plan compared to the other chordate clades and the question remains of whether and how the emergence of vertebrate morphological innovations can be related to the appearance of new embryonic cell populations. We previously proposed, by studying mesoderm development in the cephalochordate amphioxus, a scenario for the evolution of the vertebrate head mesoderm. To further test this scenario at the cell population level, we used scRNA-seq to construct a cell atlas of the amphioxus neurula, stage at which the main mesodermal compartments are specified. Our data allowed us to validate the presence of a prechordal-plate like territory in amphioxus. Additionally, the transcriptomic profile of somite cell populations supports the homology between specific territories of amphioxus somites and vertebrate cranial/pharyngeal and lateral plate mesoderm. Finally, our work provides evidence that the appearance of the specific mesodermal structures of the vertebrate head was associated to both segregation of pre-existing cell populations, and co-option of new genes for the control of myogenesis. The evolution of the vertebrate head mesoderm involved the emergence of new structures and cell types. Here the authors generated a cell atlas of the cephalochordate neurula to study the origins of these novelties and propose a revised scenario for the evolution of the vertebrate head muscles.