Evolutionary conservation of the eumetazoan gene regulatory landscape

Abstract

Despite considerable differences in morphology and complexity of body plans among animals, a great part of the gene set is shared among Bilateria and their basally branching sister group, the Cnidaria. This suggests that the common ancestor of eumetazoans already had a highly complex gene repertoire. At present it is therefore unclear how morphological diversification is encoded in the genome. Here we address the possibility that differences in gene regulation could contribute to the large morphological divergence between cnidarians and bilaterians. To this end, we generated the first genome-wide map of gene regulatory elements in a nonbilaterian animal, the sea anemone Nematostella vectensis. Using chromatin immunoprecipitation followed by deep sequencing of five chromatin modifications and a transcriptional cofactor, we identified over 5000 enhancers in the Nematostella genome and could validate 75% of the tested enhancers in vivo. We found that in Nematostella, but not in yeast, enhancers are characterized by the same combination of histone modifications as in bilaterians, and these enhancers preferentially target developmental regulatory genes. Surprisingly, the distribution and abundance of gene regulatory elements relative to these genes are shared between Nematostella and bilaterian model organisms. Our results suggest that complex gene regulation originated at least 600 million yr ago, predating the common ancestor of eumetazoans.

Cnidarian microRNAs frequently regulate targets by cleavage

“…Moreover, cis-regulation of transcription is very similar in Nematostella and bilaterians (Schwaiger et al 2014). These findings are in striking contrast to the vastly different body plans and cell type compositions of Cnidaria and Bilateria.…”

TALEN and CRISPR/Cas9-mediated genome editing in the early-branching metazoan Nematostella vectensis

“…On a general note, a broad effort is underway to reconstruct the evolution of animal complexity through comparative studies of phylogenetically informative lineages, including cnidarians [23][24][25] , ctenophores 26,27 , placozoans 28,29 and sponges 30,31 . While sequencing projects have produced an abundance of information about the genomic foundations of animal evolution 32 , emerging genetic tools of the kind described herein now permit functional interrogation of the ancestral molecular toolkit employed in the diversification of early animal body plans.…”

Using Nematostella vectensis to Study the Interactions between Genome, Epigenome, and Bacteria in a Changing Environment

“…Among marine invertebrates, relatively little is known about the mechanisms of epigenetic regulation. However, N. vectensis is the only marine invertebrate where existing data is available on genome methylation (Zemach et al, 2010), histone modifications (Schwaiger et al, 2014), and miRNAs (Moran et al, 2013). Thus, we suggest that N. vectensis is uniquely positioned as an organism of choice to study how these epigenetic alterations of the genome link molecular changes with acclimation observed at the organismal and physiological level.…”

“…It is easily cultured in laboratory in high numbers Uhlinger, 1992, 1995) and clonally propagated to eliminate genetic confounding effects. In addition, N. vectensis has the unique advantage amongst marine invertebrates of having extensive sequencing of transcriptomes (Helm et al, 2013;Tulin et al, 2013), preexisting data on genome methylation (Zemach et al, 2010), histone modifications (Schwaiger et al, 2014), and miRNAs (Moran et al, 2014). These existing data result in an exceptionally well-annotated genome, an essential but still rare tool for marine species.…”