Using ascidian embryos to study the evolution of developmental gene regulatory networks

Ascidians are ideally positioned taxonomically at the base of the chordate tree to provide a point of comparison for developmental regulatory mechanisms that operate among protostomes, non-chordate deuterostomes, invertebrate chordates, and vertebrates. In this review, we propose a model for the gene regulatory network that gives rise to the ascidian notochord. The purpose of this model is not to clarify all of the interactions between molecules of this network, but to provide a working schematic of the regulatory architecture that leads to the specification of endoderm and the patterning of mesoderm in ascidian embryos. We describe a series of approaches, both computational and biological, that are currently being used, or are in development, for the study of ascidian embryo gene regulatory networks. It is our belief that the tools now available to ascidian biologists, in combination with a streamlined mode of development and small genome size, will allow for more rapid dissection of developmental gene regulatory networks than in more complex organisms such as vertebrates. It is our hope that the analysis of gene regulatory networks in ascidians can provide a basic template which will allow developmental biologists to superimpose the modifications and novelties that have arisen during deuterostome evolution.

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A special issue of Developmental Biology will appear on June 1, devoted entirely to papers on developmental gene regulatory networks and related subjects. Its advent signals the interdisciplinary revolution that is sweeping across the landscape of bioscience, as there emerges a new level of understanding of biological systems. A system-level synthesis of genomics, developmental biology, evolutionary biology, computational biology, and gene regulation molecular biology underlies gene regulatory network analysis.

Genomics ◽

10.1006/geno.2002.6750 ◽

2002 ◽

Vol 79 (6) ◽

pp. 749

Keyword(s):

Developmental Biology ◽

Gene Regulatory Networks ◽

Regulatory Network ◽

Evolutionary Biology ◽

Regulatory Networks ◽

System Level ◽

Special Issue ◽

Developmental Gene ◽

Gene Regulatory ◽

Level Of Understanding

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Co-expression of Foxa.a, Foxd and Fgf9/16/20 defines a transient mesendoderm regulatory state in ascidian embryos

eLife ◽

10.7554/elife.14692 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 20

Author(s):

Clare Hudson ◽

Cathy Sirour ◽

Hitoyoshi Yasuo

Keyword(s):

Gene Regulatory Networks ◽

Ground State ◽

Regulatory Networks ◽

Developmental Process ◽

Regulatory State ◽

Transcriptional Targets ◽

Regulatory Architecture ◽

Ascidian Embryos ◽

Gene Regulatory

In many bilaterian embryos, nuclear β-catenin (nβ-catenin) promotes mesendoderm over ectoderm lineages. Although this is likely to represent an evolutionary ancient developmental process, the regulatory architecture of nβ-catenin-induced mesendoderm remains elusive in the majority of animals. Here, we show that, in ascidian embryos, three nβ-catenin transcriptional targets, Foxa.a, Foxd and Fgf9/16/20, are each required for the correct initiation of both the mesoderm and endoderm gene regulatory networks. Conversely, these three factors are sufficient, in combination, to produce a mesendoderm ground state that can be further programmed into mesoderm or endoderm lineages. Importantly, we show that the combinatorial activity of these three factors is sufficient to reprogramme developing ectoderm cells to mesendoderm. We conclude that in ascidian embryos, the transient mesendoderm regulatory state is defined by co-expression of Foxa.a, Foxd and Fgf9/16/20.

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Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1509845112 ◽

2015 ◽

Vol 112 (30) ◽

pp. E4075-E4084 ◽

Cited By ~ 44

Author(s):

Eric M. Erkenbrack ◽

Eric H. Davidson

Keyword(s):

Gene Regulatory Networks ◽

Regulatory Network ◽

Regulatory Networks ◽

Strongylocentrotus Purpuratus ◽

Late Paleozoic ◽

Monophyletic Clade ◽

Developmental Gene ◽

Permian Extinction ◽

Gene Regulatory ◽

Functional Analyses

Evolution of animal body plans occurs with changes in the encoded genomic programs that direct development, by alterations in the structure of encoded developmental gene-regulatory networks (GRNs). However, study of this most fundamental of evolutionary processes requires experimentally tractable, phylogenetically divergent organisms that differ morphologically while belonging to the same monophyletic clade, plus knowledge of the relevant GRNs operating in at least one of the species. These conditions are met in the divergent embryogenesis of the two extant, morphologically distinct, echinoid (sea urchin) subclasses, Euechinoidea and Cidaroidea, which diverged from a common late Paleozoic ancestor. Here we focus on striking differences in the mode of embryonic skeletogenesis in a euechinoid, the well-known model Strongylocentrotus purpuratus (Sp), vs. the cidaroid Eucidaris tribuloides (Et). At the level of descriptive embryology, skeletogenesis in Sp and Et has long been known to occur by distinct means. The complete GRN controlling this process is known for Sp. We carried out targeted functional analyses on Et skeletogenesis to identify the presence, or demonstrate the absence, of specific regulatory linkages and subcircuits key to the operation of the Sp skeletogenic GRN. Remarkably, most of the canonical design features of the Sp skeletogenic GRN that we examined are either missing or operate differently in Et. This work directly implies a dramatic reorganization of genomic regulatory circuitry concomitant with the divergence of the euechinoids, which began before the end-Permian extinction.

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