Evolution of gene regulatory network architectures: Examples of subcircuit conservation and plasticity between classes of echinoderms. Biochimica et Biophysica Acta, 1789, 326-332

Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213, USA.
Biochimica et Biophysica Acta (Impact Factor: 4.66). 02/2009; 1789(4):326-32. DOI: 10.1016/j.bbagrm.2009.01.004
Source: PubMed


Developmental gene regulatory networks (GRNs) explain how regulatory states are established in particular cells during development and how these states then determine the final form of the embryo. Evolutionary changes to the sequence of the genome will direct reorganization of GRN architectures, which in turn will lead to the alteration of developmental programs. A comparison of GRN architectures must consequently reveal the molecular basis for the evolution of developmental programs among different organisms. This review highlights some of the important findings that have emerged from the most extensive direct comparison of GRN architectures to date. Comparison of the orthologous GRNs for endomesodermal specification in the sea urchin and sea star, provides examples of several discrete, functional GRN subcircuits and shows that they are subject to diverse selective pressures. This demonstrates that different regulatory linkages may be more or less amenable to evolutionary change. One of the more surprising findings from this comparison is that GRN-level functions may be maintained while the factors performing the functions have changed, suggesting that GRNs have a high capacity for compensatory changes involving transcription factor binding to cis regulatory modules.

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    • "If the probability of transition from the ancestral to descendant character state was only high at a specifi c phylogenetic juncture due to the (unknown) genetic background (i.e., a rare event), then the causal connection may not be demonstrable experimentally. But laboratory research has shown promising results in this regard, both for closely related species (Stern 2011 ) and broader phylogenetic comparisons (Hinman et al. 2009 ). A recurring theme at the nexus of evolution and development connected to the origin of novelty is the potential signifi cance of generic physical mechanisms, such as diffusion, viscoelasticity, and phase separation operating on soft condensed materials (Newman 1994 ). "
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    ABSTRACT: Evolutionary developmental biology (Evo-devo) is a loose conglomeration of research programs in the life sciences with two main axes: (a) the evolution of development, or inquiry into the pattern and processes of how ontogeny varies and changes over time; and, (b) the developmental basis of evolution, or inquiry into the causal impact of ontogenetic processes on evolutionary trajectories—both in terms of constraint and facilitation. Philosophical issues are found along both axes surrounding concepts such as evolvability, novelty, and modularity. The developmental basis of evolution has garnered much attention because it speaks to the possibility of revising a standard construal of evolutionary theory, but the evolution of development harbors its own conceptual questions. This article addresses the heterogeneity of Evo-devo’s conglomerate structure (including disagreements over its individuation), as well as the concepts and controversies of philosophical interest pertaining to the evolution of development and the developmental basis of evolution. Future research will benefit from a shift away from global theorizing toward the scientific practices of Evo-devo.
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    • "Endomesoderm is an ancient cell type that gives rise to a wide array of tissues in bilaterians and its origin and diversification are the subjects of great interest and debate [1-3]. One of the largest assemblages of bilaterians is the Spiralia, which includes mollusks, annelids, sipunculans, echiurans, myzostomids, nemerteans, platyhelminths, entoprocts and gnathostomulids [4]. "
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    ABSTRACT: Background Animals with a spiral cleavage program, such as mollusks and annelids, make up the majority of the superphylum Lophotrochozoa. The great diversity of larval and adult body plans in this group emerges from this highly conserved developmental program. The 4d micromere is one of the most conserved aspects of spiralian development. Unlike the preceding pattern of spiral divisions, cleavages within the 4d teloblastic sublineages are bilateral, representing a critical transition towards constructing the bilaterian body plan. These cells give rise to the visceral mesoderm in virtually all spiralians examined and in many species they also contribute to the endodermal intestine. Hence, the 4d lineage is an ideal one for studying the evolution and diversification of the bipotential endomesodermal germ layer in protostomes at the level of individual cells. Little is known of how division patterns are controlled or how mesodermal and endodermal sublineages diverge in spiralians. Detailed modern fate maps for 4d exist in only a few species of clitellate annelids, specifically in glossiphoniid leeches and the sludge worm Tubifex. We investigated the 4d lineage in the gastropod Crepidula fornicata, an established model system for spiralian biology, and in a closely related direct-developing species, C. convexa. Results High-resolution cell lineage tracing techniques were used to study the 4d lineage of C. fornicata and C. convexa. We present a new nomenclature to name the progeny of 4d, and report the fate map for the sublineages up through the birth of the first five pairs of teloblast daughter cells (when 28 cells are present in the 4d sublineage), and describe each clone’s behavior during gastrulation and later stages as these undergo differentiation. We identify the precise origin of the intestine, two cells of the larval kidney complex, the larval retractor muscles and the presumptive germ cells, among others. Other tissues that arise later in the 4d lineage include the adult heart, internal foot tissues, and additional muscle and mesenchymal cells derived from later-born progeny of the left and right teloblasts. To test whether other cells can compensate for the loss of these tissues (that is, undergo regulation), specific cells were ablated in C. fornicata. Conclusions Our results present the first fate map of the 4d micromere sublineages in a mollusk. The fate map reveals that endodermal and mesodermal fates segregate much later than previously thought. We observed little evidence of regulation between sublineages, consistent with a lineage-driven cell specification process. Our results provide a framework for comparisons with other spiralians and lay the groundwork for investigation of the molecular mechanisms of endomesoderm formation, germ line segregation and bilateral differentiation in Crepidula.
    Full-text · Article · Sep 2012 · EvoDevo
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    • "By facilitating precise comparisons of the expression patterns of genes, multiplex F-WMISH can reveal subtle differences that are very difficult to detect by other methods. Transcriptional gene regulatory networks (GRNs) are valuable as conceptual and experimental tools for the analysis of developmental and evolutionary processes (Chan et al., 2009; Davidson, 2009; Ettensohn, 2009; Hinman et al., 2009; Nikitina et al., 2009; Stathopoulos and Levine, 2005). GRN analysis is based, in part, upon the view that the genomic regulatory state of an embryonic cell is defined by the ensemble of transcription factors that is contained within the cell at any particular developmental stage. "
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    ABSTRACT: The analysis of temporal and spatial patterns of gene expression is critically important for many kinds of developmental studies, including the construction of gene regulatory networks. Recently, multiplex, fluorescent, whole mount in situ hybridization (multiplex F-WMISH), applied in combination with confocal microscopy, has emerged as the method of choice for high-resolution, three-dimensional (3D) mapping of gene expression patterns in developing tissues. We have developed an image analysis tool, GeneExpressMap (GEM), that facilitates the rapid, 3D analysis of multiplex F-WMISH data at single-cell resolution. GEM assigns F-WMISH signal to individual cells based upon the proximity of cytoplasmic hybridization signal to cell nuclei. Here, we describe the features of GEM and, as a test of its utility, we use GEM to analyze patterns of regulatory gene expression in the non-skeletogenic mesoderm of the early sea urchin embryo. GEM greatly extends the power of multiplex F-WMISH for analyzing patterns of gene expression and is a valuable tool for gene network analysis and many other kinds of developmental studies.
    Preview · Article · Jun 2011 · Developmental Biology
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