Functions of the FGF signalling pathway in cephalochordates provide insight into the evolution of the prechordal plate

Abstract

The fibroblast growth factor (FGF) signalling pathway plays various roles during vertebrate embryogenesis, from mesoderm formation to brain patterning. This diversity of functions relies on the fact that vertebrates possess the largest FGF gene complement among metazoans. In the cephalochordate amphioxus, which belongs to the chordate clade together with vertebrates and tunicates, we have previously shown that the main role of FGF during early development is the control of rostral somite formation. Inhibition of this signalling pathway induces the loss of these structures, resulting in an embryo without anterior segmented mesoderm, as in the vertebrate head. Here, by combining several approaches, we show that the anterior presumptive paraxial mesoderm cells acquire an anterior axial fate when FGF signal is inhibited and that they are later incorporated in the anterior notochord. Our analysis of notochord formation in wild type and in embryos in which FGF signalling is inhibited also reveals that amphioxus anterior notochord presents transient prechordal plate features. Altogether, our results give insight into how changes in FGF functions during chordate evolution might have participated to the emergence of the complex vertebrate head.

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

“…Therefore, metacell 1 represents a potential prechordal plate-like territory showing a transcriptomic profile characterized by anterior and axial markers together with endodermal markers. Such a territory was already proposed to exist in amphioxus based on both cell behaviour and gene expression of several marker genes 12,17,79 but our data highlight the strong difference in its transcriptomic profile compared to the other notochord cells, reinforcing the idea that ancestral chordates possessed a prechordal plate-like region that later evolved specific functions in vertebrates.…”

“…4c, d ). The first somite pair in amphioxus has long been proposed as being distinct from the other pairs, and we previously showed that this somite pair is the only one whose formation is controlled by the FGF signalling pathway 11,12,54 . Our molecular atlas additionally shows that the cells of the first pair of somites transcriptionally resemble vertebrate head and lateral plate mesoderm (metacells 1 and 3, Fig.…”

“…Based on previous work, we have proposed a multi-step scenario for the evolution of the vertebrate anterior mesoderm 11,12 . The first step consists in the segregation of the ventral mesoderm from the paraxial mesoderm and loss of its segmentation.…”

Exploring tissue morphodynamics using the photoconvertible Kaede protein in amphioxus embryos

“…The embryo imaged at the late neurula stage showed expression in the ventral epidermis and in the somites ( Fig 2 ). The same protocol was succesfully undertaken to trace the fate of the presumptive anterior somite territory in embryos in which the FGF signalling pathway was inhibited by using a FGFR inhibitor (SU5402) as published in [ 12 ].…”

“…territory in embryos in which the FGF signalling pathway was inhibited by using a FGFR inhibitor (SU5402) as published in [12].…”