The expression of FoxG1 in the early development of the European river lamprey Lampetra fluviatilis demonstrates significant heterochrony with that in other vertebrates

Abstract

FoxG1, a member of the Fox/Forkhead family of winged helix transcription factors, plays key roles in the induction and spatial compartmentalization of the telencephalon in vertebrates. Loss- and gain-of-function experiments have established FoxG1 as a maintenance factor for neural progenitors and a crucial player in the specification of the ventral telencephalon (subpallium). For the first time in evolution, the telencephalon appeared in the ancestors of vertebrates, including cyclostomes. However, although FoxG1 homologues are present in cyclostomes (i.e., in lampreys and hagfishes), no systematic study of the spatial-temporal expression of FoxG1 during the embryonic development of these animals has been carried out. Given these findings, we have now studied FoxG1 spatial-temporal expression patterns in the early development of the European river lamprey Lampetra fluviatilis. We show that in contrast to other vertebrates, in which the expression of FoxG1 begins during neurulation, the expression of this gene in L. fluviatilis starts after neurulation, first at stage 21 (early head protrusion) in the area of the otic placodes and then, beginning from stage 22, in the telencephalon. Such heterochrony of FoxG1 expression in the lamprey may reflect the fact that in this basally divergent representative of vertebrates, telencephalon specification occurs relatively late. This heterochrony could be related to the evolutionary history of the telencephalon, with a recent appearance in vertebrates as an extension to more ancient anterior brain regions. Another peculiarity of FoxG1 expression in lamprey, compared to other vertebrates, is that it is not expressed in the lamprey optic structures.