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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 30; pp. E4075 - E4084
• Main Authors: Erkenbrack, Eric M., Davidson, Eric H.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 28-07-2015; National Acad Sciences
• Series: PNAS Plus
• Subjects: Animals; Biological Evolution; Biological Sciences; Cell Differentiation; Echinoida; Echinoidea; Eucidaris tribuloides; Euechinoidea; Evolutionary biology; Extinction; Gene Expression Regulation, Developmental; Gene Regulatory Networks; Genomics; Green Fluorescent Proteins - metabolism; Mesoderm - metabolism; Nonnative species; Oligonucleotides; Organisms; PNAS Plus; Signal Transduction; Strongylocentrotus purpuratus; Strongylocentrotus purpuratus - embryology; Transcription, Genetic; Wnt Proteins - metabolism; sea urchin embryogenesis; GRN evolution; embryonic skeletogenesis; network linkages
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1509845112

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 modelStrongylocentrotus purpuratus(Sp), vs. the cidaroidEucidaris tribuloides(Et). At the level of descriptive embryology, skeletogenesis inSpandEthas long been known to occur by distinct means. The complete GRN controlling this process is known forSp. We carried out targeted functional analyses onEtskeletogenesis to identify the presence, or demonstrate the absence, of specific regulatory linkages and subcircuits key to the operation of theSpskeletogenic GRN. Remarkably, most of the canonical design features of theSpskeletogenic GRN that we examined are either missing or operate differently inEt. 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.