Primary body axes of vertebrates: Generation of a near‐Cartesian coordinate system and the role of Spemann‐type organizer

Abstract

A rationale for the complex‐appearing generation of the primary body axes in vertebrates can be obtained if this process is divided into two parts. First, an ancestral system is responsible for the anteroposterior (AP) patterning of the brain and the positioning of the heart. The blastopore (marginal zone) acts as a source region that generates primary AP‐positional information for the brain, a process that is largely independent of the organizer. This evolutionary old system was once organizing the single axis of radial–symmetric ancestors. Second, the trunk is assumed to be an evolutionary later addition. The AP organization of the trunk depends on a time‐controlled posterior transformation in which an oscillation plays a crucial role. This oscillation also leads to the repetitive nature of the trunk pattern as seen in somites or segments. The function of the Spemann‐type organizer is not to specify the dorsoventral (DV) positional information directly but to initiate the formation of a stripe‐shaped midline organizer, realized with different structures in the brain and in the trunk (prechordal plate vs. notochord). The distance of the cells to this midline (rather than to the organizer) is crucial for the DV specification. The basically different modes of axes formation in vertebrates and insects is proposed to have their origin in the initial positioning of the mesoderm. Only in vertebrates the mesoderm is initiated in a ring at a posterior position. Thus, only in vertebrates complex tissue movements are required to transform the ring‐shaped posterior mesoderm into the rod‐shaped axial structures. Developmental Dynamics 235:2907–2919, 2006.