Evolution of the Role of RA and FGF Signals in the Control of Somitogenesis in Chordates

• Published in: PloS one 2015-09, Vol.10 (9), p.e0136587-e0136587
• Main Authors: Bertrand, Stéphanie, Aldea, Daniel, Oulion, Silvan, Subirana, Lucie, de Lera, Angel R, Somorjai, Ildiko, Escriva, Hector
• Format: Article
• Language: English
• Subjects: Acids; Animal biology; Animals; Asymmetry; Axial skeleton; Bone (axial); Cell interactions; Cell signaling; Cellular signal transduction; Cephalochordata; Ciona intestinalis; Dermis; Earth Sciences; Elongation; Embryos; Epidermal Growth Factor - metabolism; Evolution; Fibroblast growth factor; Fibroblast growth factors; Gene expression; Genetic aspects; Intercellular signalling; Lancelets - embryology; Life Sciences; Machinery; Machinery and equipment; Mesendoderm; Mesoderm; Morphology; Muscles; Notch protein; Oceanography; Organogenesis; Pathways; Physiological aspects; Receptors, Notch - metabolism; Sciences of the Universe; Signal transduction; Skeletal muscle; Skeleton; Somites; Somites - embryology; Somitogenesis; Tretinoin; Tretinoin - pharmacology; Tunicata; Vertebrate Zoology; Vertebrates; Wnt protein; Wnt Signaling Pathway - drug effects; Wnt Signaling Pathway - physiology
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0136587

During vertebrate development, the paraxial mesoderm becomes segmented, forming somites that will give rise to dermis, axial skeleton and skeletal muscles. Although recently challenged, the "clock and wavefront" model for somitogenesis explains how interactions between several cell-cell communication pathways, including the FGF, RA, Wnt and Notch signals, control the formation of these bilateral symmetric blocks. In the cephalochordate amphioxus, which belongs to the chordate phylum together with tunicates and vertebrates, the dorsal paraxial mesendoderm also periodically forms somites, although this process is asymmetric and extends along the whole body. It has been previously shown that the formation of the most anterior somites in amphioxus is dependent upon FGF signalling. However, the signals controlling somitogenesis during posterior elongation in amphioxus are still unknown. Here we show that, contrary to vertebrates, RA and FGF signals act independently during posterior elongation and that they are not mandatory for posterior somites to form. Moreover, we show that RA is not able to buffer the left/right asymmetry machinery that is controlled through the asymmetric expression of Nodal pathway actors. Our results give new insights into the evolution of the somitogenesis process in chordates. They suggest that RA and FGF pathways have acquired specific functions in the control of somitogenesis in vertebrates. We propose that the "clock and wavefront" system was selected specifically in vertebrates in parallel to the development of more complex somite-derived structures but that it was not required for somitogenesis in the ancestor of chordates.