The origin and evolution of the endoderm gene regulatory network Athula H. Wikramanayake Department of Biology, University of Miami, Coral Gables, FL 33146 Gastrulation is a uniquely metazoan process, and the evolution of this character was arguably one of the pivotal events that drove the diversification of the metazoa. Segregation of germ layers and the onset of gastrulation movements in ancient embryos were likely preceded by the assembly and activation of a gene regulatory network (GRN) that specified a regulatory state for endoderm at one pole of ancient embryos. How this primordial GRN was assembled and activated in ancient embryos is not known, but GRN theory and comparative molecular embryology studies are providing unique insight into this process. Theory predicts that those GRNs that are activated during early development, and function to specify broad regional identities form kernels that are conserved over vast evolutionary periods due to the catastrophic consequences of losing any single link in the network. Hence, identification of endoderm GRN kernels conserved between bilaterians, and outgroups to the bilateria such as the cnidaria will likely provide key insight into the GRNs that shaped early animal evolution. In the sea urchin the nuclear entry of ß-catenin, a key signal transducer in the canonical Wnt pathway, is a critical upstream input into the now well-described endoderm GRN kernel. While endoderm GRN kernels have not been as extensively characterized in other bilaterians, nuclear ß-catenin marks the site of gastrulation in embryos of several bilaterian taxa, and in many cases, it has been shown that signaling via this protein is crucial for endoderm specification. In most bilaterians, the site of gastrulation is established predictably with respect to the animal-vegetal (AV) axis, and in general, these embryos develop endoderm from vegetal-half blastomeres. In contrast to bilaterians, cnidarians form endoderm at the animal pole. We have shown that nuclear ß-catenin signaling in blastomeres at the animal pole is essential for endoderm specification in this taxon indicating that a ß-catenin-dependent endoderm GRN kernel specified endoderm in the last common ancestor to bilaterians and cnidarians over 600 mya. We have proposed that the site of endoderm specification was moved from the animal pole of the last common ancestor to cnidarians and bilaterians, to the vegetal pole of the bilaterian last common ancestor. This radical shift in the site of endoderm GRN activation may have been enabled by the transfer of a key upstream activator of the endoderm kernel from the animal pole to the vegetal pole, thus resulting in the in toto shift of this GRN kernel in the urbilaterian. This event may have been a key trigger for the evolution of the bilaterian body plan and the subsequent radiation of this clade. This work is supported by a grant from the National Science Foundation, USA to AHW.

The origin and evolution of the endoderm gene regulatory network

Athula H. Wikramanayake

Department of Biology, University of Miami, Coral Gables, FL 33146

Gastrulation is a uniquely metazoan process, and the evolution of this character was arguably one of the pivotal events that drove the diversification of the metazoa. Segregation of germ layers and the onset of gastrulation movements in ancient embryos were likely preceded by the assembly and activation of a gene regulatory network (GRN) that specified a regulatory state for endoderm at one pole of ancient embryos. How this primordial GRN was assembled and activated in ancient embryos is not known, but GRN theory and comparative molecular embryology studies are providing unique insight into this process. Theory predicts that those GRNs that are activated during early development, and function to specify broad regional identities form kernels that are conserved over vast evolutionary periods due to the catastrophic consequences of losing any single link in the network. Hence, identification of endoderm GRN kernels conserved between bilaterians, and outgroups to the bilateria such as the cnidaria will likely provide key insight into the GRNs that shaped early animal evolution. In the sea urchin the nuclear entry of ß-catenin, a key signal transducer in the canonical Wnt pathway, is a critical upstream input into the now well-described endoderm GRN kernel. While endoderm GRN kernels have not been as extensively characterized in other bilaterians, nuclear ß-catenin marks the site of gastrulation in embryos of several bilaterian taxa, and in many cases, it has been shown that signaling via this protein is crucial for endoderm specification. In most bilaterians, the site of gastrulation is established predictably with respect to the animal-vegetal (AV) axis, and in general, these embryos develop endoderm from vegetal-half blastomeres. In contrast to bilaterians, cnidarians form endoderm at the animal pole. We have shown that nuclear ß-catenin signaling in blastomeres at the animal pole is essential for endoderm specification in this taxon indicating that a ß-catenin-dependent endoderm GRN kernel specified endoderm in the last common ancestor to bilaterians and cnidarians over 600 mya. We have proposed that the site of endoderm specification was moved from the animal pole of the last common ancestor to cnidarians and bilaterians, to the vegetal pole of the bilaterian last common ancestor. This radical shift in the site of endoderm GRN activation may have been enabled by the transfer of a key upstream activator of the endoderm kernel from the animal pole to the vegetal pole, thus resulting in the in toto shift of this GRN kernel in the urbilaterian. This event may have been a key trigger for the evolution of the bilaterian body plan and the subsequent radiation of this clade.

This work is supported by a grant from the National Science Foundation, USA to AHW.