Developmental expression of COE across the Metazoa supports a conserved role in neuronal cell-type specification and mesodermal development

Abstract

The transcription factor COE (collier/olfactory-1/early B cell factor) is an unusual basic helix–loop–helix transcription factor as it lacks a basic domain and is maintained as a single copy gene in the genomes of all currently analysed non-vertebrate Metazoan genomes. Given the unique features of the COE gene, its proposed ancestral role in the specification of chemosensory neurons and the wealth of functional data from vertebrates and Drosophila, the evolutionary history of the COE gene can be readily investigated. We have examined the ways in which COE expression has diversified among the Metazoa by analysing its expression from representatives of four disparate invertebrate phyla: Ctenophora (Mnemiopsis leidyi); Mollusca (Haliotis asinina); Annelida (Capitella teleta and Chaetopterus) and Echinodermata (Strongylocentrotus purpuratus). In addition, we have studied COE function with knockdown experiments in S. purpuratus, which indicate that COE is likely to be involved in repressing serotonergic cell fate in the apical ganglion of dipleurula larvae. These analyses suggest that COE has played an important role in the evolution of ectodermally derived tissues (likely primarily nervous tissues) and mesodermally derived tissues. Our results provide a broad evolutionary foundation from which further studies aimed at the functional characterisation and evolution of COE can be investigated.Electronic supplementary materialThe online version of this article (doi:10.1007/s00427-010-0343-3) contains supplementary material, which is available to authorized users.

Mollusca

“…7.13 and 7.14A-C ; Samadi and Steiner 2010a ). Several other genes have been identifi ed to act in gastropod apical organ formation, including collier , nk2.1 , tectin3 , engrailed , and otp (Table 7.2 ; Nederbragt et al 2002a , b ;Dunn et al 2007 ;Jackson et al 2010 ). Although the direct developing cephalopods lack an apical organ, preliminary data suggest that they express at least some of these genes in the developing (adult!)…”

“…Research into the molecular regulatory processes of molluscan shell formation has recently received considerable attention, especially with respect to nacre formation in gastropods and bivalves, whereby an impressive genetic toolkit has been identifi ed. This suggests independent evolution of the nacreous layer in various gastropod and bivalve lineages (Jackson et al 2010 ).…”

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

“…In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17)(18)(19)(20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22)(23)(24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.…”

Ctenophores: an evolutionary-developmental perspective

“…Most published data in the former deal with embryonic stages and the cydippid larva, whereas most studies in the latter were focused on the adult. [47][48][49][50]51 ]; T-box transcription factors [43 ,47,52]; forkhead class transcription factors [53]; the collier family of bHLH transcriptions factors [54] and nuclear receptors [55].…”