Wuitchik DM et al. (2019), Seasonal temperature, the lunar cycle and diurn...

XB-ART-57198

Mol Ecol 2019 Aug 01;2816:3629-3641. doi: 10.1111/mec.15173.

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Seasonal temperature, the lunar cycle and diurnal rhythms interact in a combinatorial manner to modulate genomic responses to the environment in a reef-building coral.

Wuitchik DM , Wang D , Pells TJ , Karimi K , Ward S , Vize PD .

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Rhythms of various periodicities drive cyclical processes in organisms ranging from single cells to the largest mammals on earth, and on scales from cellular physiology to global migrations. The molecular mechanisms that generate circadian behaviours in model organisms have been well studied, but longer phase cycles and interactions between cycles with different periodicities remain poorly understood. Broadcast spawning corals are one of the best examples of an organism integrating inputs from multiple environmental parameters, including seasonal temperature, the lunar phase and hour of the day, to calibrate their annual reproductive event. We present a deep RNA-sequencing experiment utilizing multiple analyses to differentiate transcriptomic responses modulated by the interactions between the three aforementioned environmental parameters. Acropora millepora was sampled over multiple 24-hr periods throughout a full lunar month and at two seasonal temperatures. Temperature, lunar and diurnal cycles produce distinct transcriptomic responses, with interactions between all three variables identifying a core set of genes. These core genes include mef2, a developmental master regulator, and two heterogeneous nuclear ribonucleoproteins, one of which is known to post-transcriptionally interact with mef2 and with biological clock-regulating mRNAs. Interactions between diurnal and temperature differences impacted a range of core processes ranging from biological clocks to stress responses. Genes involved with developmental processes and transcriptional regulation were impacted by the lunar phase and seasonal temperature differences. Lastly, there was a diurnal and lunar phase interaction in which genes involved with RNA-processing and translational regulation were differentially regulated. These data illustrate the extraordinary levels of transcriptional variation across time in a simple radial cnidarian in response to the environment under normal conditions.

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Species referenced: Xenopus
Genes referenced: clock hnrnpa1 hnrnpk

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	Figure 1. Interaction of temperature, the lunar phase and hour of the day on transcription in Acropora millepora. (a) Image of an A. millepora colony. (b) Schematic of our experimental set‐up with two temperature treatments under artificial moonlight with natural sunlight cycles. (c) Venn diagram of differentially expressed genes between all interaction‐based likelihood‐ratio tests. TP, temperature/lunar phase interaction; TH, temperature/hour interaction; PH, phase/hour interaction; TPH temperature/phase/hour interaction
	Figure 2. The interaction of temperature and daily rhythms. (a) Heatmaps of differentially expressed genes from the interaction of temperature and hour of the day, which were annotated by the GO terms “Rhythmic process” and “Cellular response to stress.” Gene counts were transformed into row z‐scores and then genes were hierarchically clustered based on Euclidean distance, and this clustering is represented through a dendrogram. (b) Daily expression plots of select genes. Solid lines represent the mean counts (log2), shaded areas (blue and red) are 95% confidence intervals, and grey areas denote nighttime. Hour indicates local clock hour (time of day)
	Figure 3. The interaction of temperature and lunar rhythms. (a) Differentially expressed genes from the interaction of temperature and the lunar phase, annotated as “Transcription regulatory activity” and “Developmental process.” Methods were as in Figure 2. (b) Daily expression plots of select genes. Solid lines represent the mean counts and shaded areas (blue and red) are 95% confidence intervals. The x‐axis indicates the lunar phase: open circle indicates a full moon, filled circle is a new moon and half circles represent the appropriate quarter moons
	Figure 4. Temperature and lunar phase profiles of camk and thyroid hormone‐associated genes. Methods were as in Figure 2. Solid lines represent the mean counts and shaded areas (blue and red) are 95% confidence intervals. The x‐axis the indicates the lunar phase, and the symbols match those in Figure 3
	Figure 5. Heatmaps of the top 50 differentially expressed genes from the interaction of phase and hour of the day. Gene counts were transformed into row z‐scores and then genes were hierarchically clustered based on Euclidean distance, and this clustering is represented through a dendrogram. The x‐axis indicates the lunar phase, and the symbols match those in Figure 3
	Figure 6. The three‐way interaction between temperature, lunar phase and hour of the day indicates that post‐transcriptional processes and the mef2 gene are key responses. Daily profiles of read counts (log2) for mef2, hnrnpa1 and hnrnpk were all statistically significant under a three‐way interaction between temperature, lunar phase and hour of the day. The open circle indicates a full moon, filled circle new moon and half circles the appropriate quarter moons. Solid lines represent the mean counts and shaded areas (blue and red) are 95% confidence intervals

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