Lessons from a gene regulatory network: echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis

Abstract

Significant new insights have emerged from the analysis of a gene regulatory network (GRN) that underlies the development of the endoskeleton of the sea urchin embryo. Comparative studies have revealed ways in which this GRN has been modified (and conserved) during echinoderm evolution, and point to mechanisms associated with the evolution of a new cell lineage. The skeletogenic GRN has also recently been used to study the long-standing problem of developmental plasticity. Other recent findings have linked this transcriptional GRN to morphoregulatory proteins that control skeletal anatomy. These new studies highlight powerful new ways in which GRNs can be used to dissect development and the evolution of morphogenesis. IntroductionTo understand how development is encoded in the genome, biologists are turning increasingly to system-level approaches. The concept of transcriptional gene regulatory networks (GRNs) is proving to be a powerful one in this context. GRNs are ensembles of genes that encode transcription factors (TFs) and the genes that these proteins regulate. A central component of GRN analysis is the dissection of the cis-regulatory control systems of genes. Cisregulatory systems consist of non-coding DNA sequences that control when and where genes are transcribed. They are often viewed as modular, information-processing systems (Davidson, 2006). GRN analysis attempts to identify not only the functional interactions among genes, but also the relevant cis-regulatory DNA sequences, the proteins that bind to these sequences, and the logic by which cis-regulatory systems control gene transcription.The GRNs that operate during embryonic development (developmental GRNs) are highly dynamic. New interactions between genes are continually established as old interactions are modified or discarded. Inputs from cell signaling pathways, and intrinsic properties of regulatory networks themselves, contribute to the dynamic nature of GRNs (see Davidson, 2006). The genomic regulatory states of embryonic cells, which are a reflection of the concentrations and activities of hundreds of TFs and the global patterns of gene activity they evoke, are thus ever changing.This review considers recent studies that have applied the GRN concept in new and informative ways to examine developmental plasticity (that is, the ability of embryonic cells to switch developmental pathways), morphogenesis, and the evolution of developmental programs. It focuses on a GRN that controls skeletogenesis in sea urchins, a group of animals belonging to the phylum Echinodermata that has proven to be particularly useful for the analysis of GRNs in early development. GRNs that underlie cell specification are presently understood in greater detail in the sea urchin than in any other metazoan embryo, although work is ongoing in several other experimental models (Koide et al., 2005;Stathopoulos and Levine, 2005;Ge et al., 2006;Satou et al., 2008). For general reviews of GRNs in early sea urchin development, and of the methods used to construct and represe...

Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins

“…Previous authors have characterized the DNG as an evolutionary novelty unique to all euechinoid echinoids (1,8,21), and our ancestral state reconstructions have revealed mean PPs that strongly identify the DNG as a novelty unique to all extant euechinoids. Nonetheless, our analysis also fails to demonstrate unambiguously that the last common ancestor of echinoids (including cidaroids) did not use the DNG, and instead used the mechanism present in extant cidaroids (8,21).…”

“…evolution | evo-devo | euechinoid | cidaroid | gene regulatory networks T he investigation of gene regulatory networks (GRNs) in modern taxa allows for the understanding of evolutionary changes in the regulatory genome that have underpinned the evolution of new morphological structures in deep time (1)(2)(3)(4). Establishing a timeline for the rates at which these novel structures arise, and the rate at which the developmental GRNs that encode them evolve, lies at the heart of evolutionary developmental biology (5).…”

Role of the nanos homolog during sea urchin development

“…On the other hand, it is possible that the transformation of other cell lineages into PMCs occurred at the archenteron tip as a result of repression of PMC ingression in HpNanos-knockdown embryos. In fact, it has been reported that SMCs change their fate into skeletogenic mesenchyme cells when PMCs are removed (Ettensohn, 1990(Ettensohn, , 2008Hamada and Kiyomoto, 2003). As shown in Figure 4, in the knockdown chimera at the gastrula stage, micromere derived tracer-positive cells were detected in additional mesenchyme cells around the archenteron tip and skeletogenic mesenchyme cells.…”

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

“…Abundant comparative evidence exists for other euechinoid taxa as well, including Lytechinus variegatus (Lv) (31)(32)(33)(34)(35)(36)(37) and Paracentrotus lividus (Pl) (38)(39)(40)(41)(42). Data from these indirectdeveloping euechinoids indicate that although these taxa diverged from one another ∼90 mya (9, 43), very little appreciable change to their developmental GRNs has accrued (44)(45)(46). Although there is evidence of minor alterations to these GRNs, such as a heterochronic shift in snail expression in Lv and Sp (22), numerous studies have made clear the striking conservation of GRN linkages in these lineages.…”