Modularity and design principles in the sea urchin embryo gene regulatory network

Abstract

The gene regulatory network (GRN) established experimentally for the pre-gastrular sea urchin embryo provides causal explanations of the biological functions required for spatial specification of embryonic regulatory states. Here we focus on the structure of the GRN which controls the progressive increase in complexity of territorial regulatory states during embryogenesis; and on the types of modular subcircuits of which the GRN is composed. Each of these subcircuit topologies executes a particular operation of spatial information processing. The GRN architecture reflects the particular mode of embryogenesis represented by sea urchin development. Network structure not only specifies the linkages constituting the genomic regulatory code for development, but also indicates the various regulatory requirements of regional developmental processes.

Fig. 1

Process Diagram indicating regulatory state domains in the sea urchin embryo up to gastrulation. (A) Optical cross sections of embryos at cleavage, 8 h (CL), hatching blastula, 18 h (HB), and mesenchyme blastula, 24 h (MB). Embryos are viewed from the side (lateral view, LV) and color coded to indicate territorial regulatory states. (B) Diagrammatic image of the concentric arrangement of regulatory states viewed from the vegetal pole (vegetal view, VV). (C) Process Diagram: the colored rectangles represent the territories of the endomesoderm. Subdivision of the embryos proceeds in a progressive manner so that just before gastrulation there are five domains indicated at the bottom of the diagram. Modified from Peter and Davidson [12].

Fig. 2

GRN model for the endomesoderm 6-18 h of development. This is a “view from the genome” in which all regulatory interactions occurring through time are portrayed in the various domains (cf. Fig. 1). For data and temporal and spatial regulatory views see http://sugp.caltech.edu/endomes/.

Fig. 3

GRN model for the endomesoderm up to 30 h of development, as in Fig. 2.

Fig. 4

Canonical subcircuit from the endomesoderm GRN utilized to execute particular spatial specification processes. Each section of the figure (A-F) describes a particular spatial specification function, the “job” to be done, and the GRN subcircuit by which this job is executed. Following appear the subcircuit as excerpted from the GRNs in Figs. 2 and 3; a spatial expression cartoon; examples of the activity state of the subcircuit in different domains of the embryo; and a Boolean activity matrix for all relevant embryonic domains.

Fig. 4

Canonical subcircuit from the endomesoderm GRN utilized to execute particular spatial specification processes. Each section of the figure (A-F) describes a particular spatial specification function, the “job” to be done, and the GRN subcircuit by which this job is executed. Following appear the subcircuit as excerpted from the GRNs in Figs. 2 and 3; a spatial expression cartoon; examples of the activity state of the subcircuit in different domains of the embryo; and a Boolean activity matrix for all relevant embryonic domains.