Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution

Gao, Feng; Davidson, Eric H.

doi:10.1073/pnas.0801201105

Cited by 154 publications

(209 citation statements)

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“…Expression of the Et alx1 gene is, however, ultimately required for postgastrular skeleton formation to occur (Fig. 2), just as it is required for postembryonic skeletogenesis in both sea urchins and sea stars (22). delta.…”

Section: Resultsmentioning

confidence: 99%

“…tbr. Finally, the tbr gene, which is required for and coopted to skeletogenic function in euechinoids (22,24,32,33), is again expressed very differently in Et. Although the tbr gene is first activated in the micromeres, its expression quickly spreads to the entire nonskeletogenic mesodermal domain, where by double in situ hybridization, it can be seen to totally overlap that of ets1, and, in direct contrast to Sp, there is no evidence from its expression pattern that it ever plays a skeletogenic role.…”

Section: Resultsmentioning

confidence: 99%

“…alx1. The alx1 gene is a primary driver of skeletogenic specification and differentiation in sea urchin embryo and adult development, and it is a member of a family of homeodomain genes also used in vertebrate skeletogenesis (22,(25)(26)(27). In euechinoids alx1 is one of the initial set of positively acting transcriptional regulators that set up the skeletogenic regulatory state, and it is transcriptionally activated by a double-negative derepression subcircuit (24,28), immediately upon segregation of the skeletogenic micromere founder cells early in cleavage (25).…”

Section: Resultsmentioning

confidence: 99%

“…Many relevant genes from the authenticated Sp skeletogenic specification GRN (4) were investigated, of which five essential participants are reported on in the following. These are the regulatory genes at the very top of the skeletogenic GRN hierarchy in Sp, the deployment of which our earlier work (22) predicted might have been the locus of the evolutionary changes that mobilized the skeletogenic network in the micromere lineage of the euechinoids. Experiments on another cidaroid species (23) have already cast doubt on the presence of one key component of this circuitry, the repressive paired box gene pmar1, which functions in a double negative transcriptional gate at the top of the skeletogenic GRN of Sp (4, 24).…”

Section: Significancementioning

confidence: 99%

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

Erkenbrack

Davidson

2015

Proc. Natl. Acad. Sci. U.S.A.

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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.GRN evolution | network linkages | embryonic skeletogenesis | sea urchin embryogenesis T he mechanisms responsible for evolutionary divergence of animal body plans, as so extensively documented in the Phanerozoic fossil record, lie in alterations of the encoded genomic regulatory programs that direct development. This principle has long been evident a priori (1), and overwhelmingly, accumulating current evidence precludes any other general explanation (2). However, it still remains a challenge to adduce specific examples in which evolutionary rewiring of developmental gene-regulatory networks (GRNs) can be seen to account for observed differences in morphogenetic processes that distinguish descendants of a common ancestor. Knowledge of developmental GRNs remains insufficiently extensive, and it is not trivial to locate useful examples, which require comparison within a monophyletic clade at just sufficient distance so that the diverged morphology is clearly the output of homologous networks of developmental regulatory gene interactions.In recent years, largely complete developmental GRN models have been solved that causally explain spatial specification in large domains of the embryo of the sea urchin Strongylocentrotus purpuratus (Sp), up to gastrulation (3-5). The explanatory power of these networks was demonstrated, in these pages, by a predictive computational analysis that showed that they contain sufficient informat...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

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

Erkenbrack

Davidson

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…During the transition from embryo to larval stage, the interaction of multiple genetic regulatory networks (GRNs) determines the patterns of gene activity and differentiation of developmental modules in marine invertebrates (Raff & Sly, 2000). In echinoderms, for example, the unique combination of regulatory genes (e.g., transcription factors) in embryonic space and time contribute to shaping the regulatory program for larval skeletogenesis (Dylus et al., 2016; Gao & Davidson, 2008), endomesodermal (Peter & Davidson, 2010), and ectodermal specification (Nakata & Minokawa, 2009). Despite the differences in larval development in this group (e.g., pluteus‐, bipinnaria‐, and auricularia‐like larvae), comparisons of their GRN architectures have detected highly conserved orthologous regulatory genes among the extant echinoderm classes (Hinman & Davidson, 2003a,b; Hinman, Nguyen, Cameron, & Davidson, 2003; Hinman, Nguyen, & Davidson, 2003).…”

Section: Introductionmentioning

confidence: 99%

Gene expression profiling during the embryo‐to‐larva transition in the giant red sea urchin Mesocentrotus franciscanus

Gaitán‐Espitía

Hofmann

2017

Ecology and Evolution

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In echinoderms, major morphological transitions during early development are attributed to different genetic interactions and changes in global expression patterns that shape the regulatory program for the specification of embryonic territories. In order more thoroughly to understand these biological and molecular processes, we examined the transcriptome structure and expression profiles during the embryo‐to‐larva transition of a keystone species, the giant red sea urchin Mesocentrotus franciscanus. Using a de novo assembly approach, we obtained 176,885 transcripts from which 60,439 (34%) had significant alignments to known proteins. From these transcripts, ~80% were functionally annotated allowing the identification of ~2,600 functional, structural, and regulatory genes involved in developmental process. Analysis of expression profiles between gastrula and pluteus stages of M. franciscanus revealed 791 differentially expressed genes with 251 GO overrepresented terms. For gastrula, up‐regulated GO terms were mainly linked to cell differentiation and signal transduction involved in cell cycle checkpoints. In the pluteus stage, major GO terms were associated with phosphoprotein phosphatase activity, muscle contraction, and olfactory behavior, among others. Our evolutionary comparative analysis revealed that several of these genes and functional pathways are highly conserved among echinoids, holothuroids, and ophiuroids.

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Cis‐regulatory evolution underlying the changes in wingless expression pattern associated with wing pigmentation of Drosophila

2023

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The co‐option of regulatory genes has the potential to play an important role in the evolutionary gain of new traits. However, the changes at the sequence level that underlie such a co‐option event are still elusive. We identified the changes in the cis‐regulatory sequence of wingless that caused co‐option of wingless and led to its expression in new places in Drosophila guttifera, which has unique pigmentation patterns on its wings. The newly gained function of gene expression activation was acquired evolutionarily via a combination of pre‐existing sequences containing a putative binding site for SMAD transcription factors that exhibit an ancestral function in driving expression at crossveins, and a sequence that is specific to the lineage leading to D. guttifera.

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Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution

Cited by 154 publications

References 25 publications

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

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

Gene expression profiling during the embryo‐to‐larva transition in the giant red sea urchin Mesocentrotus franciscanus

Cis‐regulatory evolution underlying the changes in wingless expression pattern associated with wing pigmentation of Drosophila

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