Article

A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos

Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213, USA.
Developmental Biology (Impact Factor: 3.55). 11/2009; 340(2):200-8. DOI: 10.1016/j.ydbio.2009.11.020
Source: PubMed

ABSTRACT

Comparisons of orthologous developmental gene regulatory networks (GRNs) from different organisms explain how transcriptional regulation can, or cannot, change over time to cause morphological evolution and stasis. Here, we examine a subset of the GRN connections in the central vegetal pole mesoderm of the late sea star blastula and compare them to the GRN for the same embryonic territory of sea urchins. In modern sea urchins, this territory gives rise to skeletogenic mesoderm; in sea stars, it develops into other mesodermal derivatives. Orthologs of many transcription factors that function in the sea urchin skeletogenic mesoderm are co-expressed in the sea star vegetal pole, although this territory does not form a larval skeleton. Systematic perturbation of erg, hex, tbr, and tgif gene function was used to construct a snapshot of the sea star mesoderm GRN. A comparison of this network to the sea urchin skeletogenic mesoderm GRN revealed a conserved, recursively wired subcircuit operating in both organisms. We propose that, while these territories have evolved different functions in sea urchins and sea stars, this subcircuit is part of an ancestral GRN governing echinoderm vegetal pole mesoderm development. The positive regulatory feedback between these transcription factors may explain the conservation of this subcircuit.

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Available from: Veronica F Hinman
    • "Prediction: hex is likely to be expressed in mesoderm of holothurians, but endodermal expression after blastula stage is unclear At least 462 mya: in ancestral embryos prior to the holothuroid–echinoid divergence 7. erg and tgif were initiated in the mesoderm and tgif came to be expressed in the endoderm at a later time in development; whereas erg remained restricted to the mesoderm throughout early embryonic development to fulfill its ancestral function, tgif was expressed first in the mesoderm and then in the mesoderm and the endoderm 8. tgif mesoderm expression at mid-gastrula stage was either lost in asteroids or gained in the lineage leading to the last common ancestor of echinozoans 9. erg was expressed in the skeletogenic lineage at least as late in development as mid-gastrula stage 10. hex endodermal expression is acquired early in asteroid embryogenesis or lost in last common ancestor of extant echinozoans At least 268 mya: in ancestral embryos at the cidaroid–euechinoid divergence, e.g., in Archaeocidaris embryos 11. erg, hex, and tel were initiated in a few cells at the center of the vegetal pole; later in the lineage leading to camaradont euechinoids following the cidaroid–euechinoid divergence, these three genes are restricted PMCs prior to PMC ingression 12. tgif remains expressed in mesodermal cells that ingressed into the blastocoel (tgif is not expressed in mesodermal cells that have ingressed in holothuroids) mesodermal and endodermal in asteroids (McCauley et al. 2010). That the erg–hex–tgif subcircuit also exhibits these expression patterns in the same clades suggests that all four of these genes may be recursively wired. "
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    ABSTRACT: Diverse sampling of organisms across the five major classes in the phylum Echinodermata is beginning to reveal much about the structure and function of gene regulatory networks (GRNs) in development and evolution. Sea urchins are the most studied clade within this phylum, and recent work suggests there has been dramatic rewiring at the top of the skeletogenic GRN along the lineage leading to extant members of the euechinoid sea urchins. Such rewiring likely accounts for some of the observed developmental differences between the two major subclasses of sea urchins-cidaroids and euechinoids. To address effects of topmost rewiring on downstream GRN events, we cloned four downstream regulatory genes within the skeletogenic GRN and surveyed their spatiotemporal expression patterns in the cidaroid Eucidaris tribuloides. We performed phylogenetic analyses with homologs from other non-vertebrate deuterostomes and characterized their spatiotemporal expression by quantitative polymerase chain reaction (qPCR) and whole-mount in situ hybridization (WMISH). Our data suggest the erg-hex-tgif subcircuit, a putative GRN kernel, exhibits a mesoderm-specific expression pattern early in Eucidaris development that is directly downstream of the initial mesodermal GRN circuitry. Comparative analysis of the expression of this subcircuit in four echinoderm taxa allowed robust ancestral state reconstruction, supporting hypotheses that its ancestral function was to stabilize the mesodermal regulatory state and that it has been co-opted and deployed as a unit in mesodermal subdomains in distantly diverged echinoderms. Importantly, our study supports the notion that GRN kernels exhibit structural and functional modularity, locking down and stabilizing clade-specific, embryonic regulatory states.
    No preview · Article · Jan 2016 · Development Genes and Evolution
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    • "To this aim, we coinjected each construct with either 400 µM control morpholino antisense oligonucleotide (MASO) or PmTbr-specific translation blocking MASO. These modified oligonucleotides bind in a sequence specific manner to the translation start site of the transcript to block translation and have been used successfully in previous work from our lab (Hinman et al. 2007; McCauley et al. 2010). At this concentration, the Tbr MASO drastically reduces, but does not eliminate, Tbr protein. "
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    ABSTRACT: Gene regulatory networks (GRNs) describe the progression of transcriptional states that take a single-celled zygote to a multicellular organism. It is well documented that GRNs can evolve extensively through mutations to cis-regulatory modules. Transcription factor proteins that bind these cis-regulatory modules may also evolve to produce novelty. Coding changes are considered to be rarer, however, because transcription factors are multifunctional and hence are more constrained to evolve in ways that will not produce widespread detrimental effects. Recent technological advances have unearthed a surprising variation in DNA binding abilities, such that individual transcription factors may recognize both a preferred primary motif and an additional secondary motif. This provides a source of modularity in function. Here, we demonstrate that orthologous transcription factors can also evolve a changed preference for a secondary binding motif, thereby offering an unexplored mechanism for GRN evolution. Using Protein Binding Microarray, Surface Plasmon Resonance, and in vivo reporter assays, we demonstrate an important difference in DNA binding preference between Tbrain protein orthologs in two species of echinoderms, the sea star, Patiria miniata, and the sea urchin, Strongylocentrotus purpuratus. While both orthologs recognize the same primary motif, only the sea star Tbr also has a secondary binding motif. Our in vivo assays demonstrate that this difference may allow for greater evolutionary change in timing of regulatory control. This uncovers a layer of transcription factor binding divergence that could exist for many pairs of orthologs. We hypothesize that this divergence provides modularity that allows orthologous transcription factors to evolve novel roles in gene regulatory networks through modification of binding to secondary sites.
    Full-text · Article · Jul 2014 · Molecular Biology and Evolution
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    • "Current phylogeny (Pisani et al., 2012) shows the eleutherozoan outgroup to the echinoids, ophiuroids and holothuroids, to be the asteroids or sea stars, the divergence dating back to the origins of the eleutherozoans, probably in the lower Ordovician if not before. Indeed sea stars have no pigment cell lineage and expression of gcm and gataE is conspicuously absent from embryonic sea star mesoderm (Hinman and Davidson, 2007; Mccauley et al., 2010). On the other hand, the sea star embryonic mesoderm generates blastocoelar cell types similar to those descendent from oral NSM of sea urchins. "
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    ABSTRACT: Specification of the non-skeletogenic mesoderm (NSM) in sea urchin embryos depends on Delta signaling. Signal reception leads to expression of regulatory genes that later contribute to the aboral NSM regulatory state. In oral NSM, this is replaced by a distinct oral regulatory state in consequence of Nodal signaling. Through regulome wide analysis we identify the homeobox gene not as an immediate Nodal target. not expression in NSM causes extinction of the aboral regulatory state in the oral NSM, and expression of a new suite of regulatory genes. All NSM specific regulatory genes are henceforth expressed exclusively, in oral or aboral domains, presaging the mesodermal cell types that will emerge. We have analyzed the regulatory linkages within the aboral NSM gene regulatory network. A linchpin of this network is gataE which as we show is a direct Gcm target and part of a feedback loop locking down the aboral regulatory state.
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