Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
Mol Ecol
2019 Aug 01;2816:3629-3641. doi: 10.1111/mec.15173.
Show Gene links
Show Anatomy links
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.
???displayArticle.abstract???
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.
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 zâ€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 hormoneâ€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 xâ€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 threeâ€way interaction between temperature, lunar phase and hour of the day indicates that postâ€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 threeâ€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
Altschul,
Basic local alignment search tool.
1990, Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed Barshis,
Genomic basis for coral resilience to climate change.
2013,
Pubmed Blanchard,
The transcription factor Mef2 is required for normal circadian behavior in Drosophila.
2010,
Pubmed Boch,
Effects of light dynamics on coral spawning synchrony.
2011,
Pubmed Brady,
Lunar Phase Modulates Circadian Gene Expression Cycles in the Broadcast Spawning Coral Acropora millepora.
2016,
Pubmed
,
Xenbase Conesa,
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research.
2005,
Pubmed Connor,
Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus.
2011,
Pubmed Crowder,
Impacts of temperature and lunar day on gene expression profiles during a monthly reproductive cycle in the brooding coral Pocillopora damicornis.
2017,
Pubmed Dijk,
Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans.
1995,
Pubmed Dixon,
CORAL REEFS. Genomic determinants of coral heat tolerance across latitudes.
2015,
Pubmed Dunlap,
Making Time: Conservation of Biological Clocks from Fungi to Animals.
2017,
Pubmed Dunlap,
Molecular bases for circadian clocks.
1999,
Pubmed Gilmour,
Coral reproduction in Western Australia.
2016,
Pubmed Grau,
Lunar phasing of the thyroxine surge preparatory to seaward migration of salmonid fish.
1981,
Pubmed Hazlerigg,
New insights into ancient seasonal life timers.
2008,
Pubmed Hemond,
The genetics of colony form and function in Caribbean Acropora corals.
2014,
Pubmed Hilton,
Photoreception and signal transduction in corals: proteomic and behavioral evidence for cytoplasmic calcium as a mediator of light responsivity.
2012,
Pubmed
,
Xenbase Hoadley,
Circadian clock gene expression in the coral Favia fragum over diel and lunar reproductive cycles.
2011,
Pubmed Hofmann,
Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus.
1995,
Pubmed Huang,
Translational regulation of the DOUBLETIME/CKIδ/ε kinase by LARK contributes to circadian period modulation.
2014,
Pubmed Kaiser,
The genomic basis of circadian and circalunar timing adaptations in a midge.
2016,
Pubmed Kaneko,
Circadian rhythm of temperature preference and its neural control in Drosophila.
2012,
Pubmed Kaniewska,
Signaling cascades and the importance of moonlight in coral broadcast mass spawning.
2015,
Pubmed Keith,
Coral mass spawning predicted by rapid seasonal rise in ocean temperature.
2016,
Pubmed Kim,
Heterogeneous nuclear ribonucleoprotein A1 regulates rhythmic synthesis of mouse Nfil3 protein via IRES-mediated translation.
2017,
Pubmed Langmead,
Fast gapped-read alignment with Bowtie 2.
2012,
Pubmed Levy,
Complex diel cycles of gene expression in coral-algal symbiosis.
2011,
Pubmed Li,
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.
2011,
Pubmed Lin,
RBM4-MEF2C network constitutes a feed-forward circuit that facilitates the differentiation of brown adipocytes.
2015,
Pubmed Love,
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
2014,
Pubmed Mallis,
Circadian rhythms, sleep, and performance in space.
2005,
Pubmed Markov,
Independent elaboration of steroid hormone signaling pathways in metazoans.
2009,
Pubmed Mercier,
Endogenous and exogenous control of gametogenesis and spawning in echinoderms.
2009,
Pubmed Moya,
Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO₂-driven acidification during the initiation of calcification.
2012,
Pubmed Nolte,
RNA around the clock - regulation at the RNA level in biological timing.
2015,
Pubmed Oldach,
Transcriptome dynamics over a lunar month in a broadcast spawning acroporid coral.
2017,
Pubmed
,
Xenbase Park,
SPDEF regulates goblet cell hyperplasia in the airway epithelium.
2007,
Pubmed Potthoff,
MEF2: a central regulator of diverse developmental programs.
2007,
Pubmed Price,
The role of casein kinase I in the Drosophila circadian clock.
2015,
Pubmed Raible,
An Overview of Monthly Rhythms and Clocks.
2017,
Pubmed Reitzel,
Circadian clocks in the cnidaria: environmental entrainment, molecular regulation, and organismal outputs.
2013,
Pubmed Ruiz-Jones,
Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis.
2017,
Pubmed Sáenz de Miera,
A circannual clock drives expression of genes central for seasonal reproduction.
2014,
Pubmed Sivachenko,
The transcription factor Mef2 links the Drosophila core clock to Fas2, neuronal morphology, and circadian behavior.
2013,
Pubmed Takeda,
Identification of jellyfish neuropeptides that act directly as oocyte maturation-inducing hormones.
2018,
Pubmed Tarrant,
Endocrine-like Signaling in Cnidarians: Current Understanding and Implications for Ecophysiology.
2005,
Pubmed Wuitchik,
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.
2020,
Pubmed
,
Xenbase
