Oscillating waves of Fox, Cyclin and CDK gene expression indicate unique spatiotemporal control of cell cycling during nervous system development in onychophorans

Abstract

Forkhead box (Fox) genes code for a class of transcription factors with many different fundamental functions in animal development including cell cycle control. Other important factors of cell cycle control are Cyclins and Cyclin-dependent kinases (CDKs). Here we report on the oscillating expression of three Fox genes, FoxM, FoxN14 (jumeaux) and FoxN23 (Checkpoint suppressor like-1), Cyclins and CDKs in an onychophoran, a representative of a relatively small group of animals that are closely related to the arthropods. Expression of these genes is in the form of several waves that start as dot-like domains in the center of each segment and then transform into concentric rings that run towards the periphery of the segments.This oscillating gene expression, however, occurs exclusively along the anterior-posterior body axis in the tissue ventral to the base of the appendages, a region where the central nervous system and the enigmatic ventral and preventral organs of the onychophoran develop. We suggest that the oscillating gene expression and the resulting waves of expression we report are likely correlated with cell cycle control during the development of the onychophoran nervous system. This intriguing patterning appears to be unique for onychophorans as it is not found in any of the arthropods we also investigated in this study, and is likely correlated with the slow embryonic development of onychophorans compared to arthropods.