AUTHOR=Jindrich Katia , Roper Kathrein E. , Lemon Sussan , Degnan Bernard M. , Reitzel Adam M. , Degnan Sandie M. 

TITLE=Origin of the Animal Circadian Clock: Diurnal and Light-Entrained Gene Expression in the Sponge Amphimedon queenslandica

JOURNAL=Frontiers in Marine Science

VOLUME=4

YEAR=2017

URL=https://www.frontiersin.org/journals/marine-science/articles/10.3389/fmars.2017.00327

DOI=10.3389/fmars.2017.00327

ISSN=2296-7745

ABSTRACT=<p>The circadian clock is a molecular network that coordinates organismal behavior and physiology with daily environmental changes in the day-night cycle. In eumetazoans (bilaterians + cnidarians), this network appears to be largely conserved, yet different from other known eukaryotic circadian networks. To determine if the eumetazoan circadian network has an older origin, we ask here whether orthologs comprising this network are expressed in a manner consistent with a role in regulating circadian patterns in a representative of an earlier-branching animal lineage, the sponge <italic>Amphimedon queenslandica</italic>. The <italic>A. queenslandica</italic> genome encodes orthologs of many eumetazoan circadian genes, including two <italic>cryptochrome</italic> genes that encode flavoproteins, three <italic>Timeout</italic> genes, and two <italic>PAR-bZIP</italic> and seven <italic>bHLH-PAS</italic> transcription factor genes. There is no apparent <italic>Cycle</italic> ortholog, although we can identify three closely related <italic>ARNT</italic> genes. Of the putative circadian genes, only <italic>AqPARa</italic> and <italic>AqCry2</italic> have a consistent oscillating diurnal expression profile, and the rhythmic expression of both these genes is partially lost when the animals are exposed to constant light or darkness. Expression of the other putative circadian genes, in particular <italic>AqClock</italic>, is neither diurnally-oscillating nor light-dependent. <italic>AqPARa</italic> and <italic>AqCry2</italic> are also temporally and spatially co-expressed throughout embryonic and larval development. Transcripts of these genes are enriched first in cells comprising the larval posterior pigment ring, which is a simple photosensory organ that is responsible for the negative phototactic behavior displayed by larvae, and subsequently in the larval epithelial and subepithelial layers. The combined findings of no clear <italic>Cycle</italic> ortholog and of <italic>PAR-bZIP</italic> and <italic>cryptochrome</italic> being the only orthologs expressed in a pattern consistent with a circadian role suggests that either (i) the ancestral metazoan circadian network was simpler than the eumetazoan network, or (ii) that this sponge has lost some components, as has occurred in some other animals such as <italic>Hydra</italic>.</p>