Circadian Cycles of Gene Expression in the Coral, Acropora millepora

Abstract

BackgroundCircadian rhythms regulate many physiological, behavioral and reproductive processes. These rhythms are often controlled by light, and daily cycles of solar illumination entrain many clock regulated processes. In scleractinian corals a number of different processes and behaviors are associated with specific periods of solar illumination or non-illumination—for example, skeletal deposition, feeding and both brooding and broadcast spawning.Methodology/Principal FindingsWe have undertaken an analysis of diurnal expression of the whole transcriptome and more focused studies on a number of candidate circadian genes in the coral Acropora millepora using deep RNA sequencing and quantitative PCR. Many examples of diurnal cycles of RNA abundance were identified, some of which are light responsive and damped quickly under constant darkness, for example, cryptochrome 1 and timeless, but others that continue to cycle in a robust manner when kept in constant darkness, for example, clock, cryptochrome 2, cycle and eyes absent, indicating that their transcription is regulated by an endogenous clock entrained to the light-dark cycle. Many other biological processes that varied between day and night were also identified by a clustering analysis of gene ontology annotations.Conclusions/SignificanceCorals exhibit diurnal patterns of gene expression that may participate in the regulation of circadian biological processes. Rhythmic cycles of gene expression occur under constant darkness in both populations of coral larvae that lack zooxanthellae and in individual adult tissue containing zooxanthellae, indicating that transcription is under the control of a biological clock. In addition to genes potentially involved in regulating circadian processes, many other pathways were found to display diel cycles of transcription.

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

“…There are three putative Timeless/Timeout family paralogs, all of which are most similar to Timeout ( Figure 1C). This is consistent with Timeless originating along the bilaterian stem (Reitzel et al, 2010;Brady et al, 2011). Completing the circadian gene repertoire, we confirm the presence of two Type I cryptochromes, AqCyr1 and AqCry2, as previously reported (Rivera et al, 2012).…”

“…In cnidarians, timeout orthologs behave differently in different species. In the sea anemone N. vectensis, timeout expression is not light responsive (Reitzel et al, 2010) whereas the coral A. millepora timeout displays a diel expression that is lost under constant darkness (Brady et al, 2011(Brady et al, , 2016. Expression of A. queenslandica timeout orthologs was not consistently correlated with the day-night cycle.…”

“…During A. queenslandica development, AqClock and AqpARNT1 are upregulated in later stage embryos and in larvae, but neither AqClock nor any of the AqpARNT genes show consistent diurnal expression patterns in adults. In eumetazoans, CLOCK and CYCLE heterodimerise, and one of them typically has a rhythmic expression pattern (e.g., Reitzel et al, 2010Reitzel et al, , 2013Brady et al, 2011). There currently is also no evidence that AqClock heterodimerises with an AqpARNT, and thus no evidence that one of these may substitute for Cycle in A. queenslandica.…”

“…In addition to Timeout, A. queenslandica has two Type I cryptochrome genes, AqCry1 and AqCry2 (Rivera et al, 2012). Akin to its eumetazoan orthologs (Vize, 2009;Reitzel et al, 2010;Brady et al, 2011), AqCry2 shows a consistent diurnal expression profile.…”

“…The diurnal transcription profiles of many of these genes in the sea anemone Nematostella vectensis and the stony coral Acropora millepora suggest that the conserved topology of the animal circadian clock may pre-date the bilaterian-cnidarian split (Vize, 2009;Reitzel et al, 2010Reitzel et al, , 2013Brady et al, 2011). To determine if the conserved eumetazoan clock has an older evolutionary origin, we sought first to identify orthologs of these genes in a marine sponge, Amphimedon queenslandica.…”