Transcriptome dynamics over a lunar month in a broadcast spawning acroporid coral
Abstract
On one night per year, at a specific point in the lunar cycle, one of the most extraordinary reproductive events on the planet unfolds as hundreds of millions of broadcast spawning corals release their trillions of gametes into the waters of the tropical seas. Each species spawns on a specific night within the lunar cycle, typically from full moon to third quarter moon, and in a specific time window after sunset. This accuracy is essential to achieve efficient fertilization in the vastness of the oceans. In this report, we use transcriptome sequencing at noon and midnight across an entire lunar cycle to explore how acroporid corals interpret lunar signals. The data were interrogated by both time-of-day-dependent and time-of-day-independent methods to identify different types of lunar cycles. Time-of-day methods found that genes associated with biological clocks and circadian processes change their diurnal cycles over the course of a synodic lunar cycle. Some genes have large differences between day and night at some lunar phases, but little or no diurnal differences at other phases. Many clock genes display an oscillation pattern indicative of phase shifts linked to the lunar cycle. Time-independent methods found that signal transduction, protein secretion and modification, cell cycle and ion transport change over the lunar timescale and peak at various phases of the moon. Together these data provide unique insights into how the moon impinges on coral transcription cycles and how lunar light may regulate circalunar timing systems and coral biology.
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In A. gemmifera, one set of 55 isogroups showed diurnal expression patterns that fluctuated over the lunar cycle, whereas a second set of 273 isogroups exhibited differential expression over the lunar cycle when noon and midnight sampling timepoints were combined.
“Two sets of regulated transcript types were identified from the quantitative RNA sequencing: one set (55 isogroups) showed diurnal expression patterns that fluctuated over the course of the lunar cycle, whereas the second set (273 isogroups) exhibited differential expression over the lunar cycle when noon and midnight sampling timepoints were combined (26).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [26]
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
ggplot2: Elegant Graphics for Data Analysis
Wickham, H. (2009) · doi:10.1007/978-0-387-98141-3 · Cited by 14,447 · see citing works
Salmon provides fast and bias-aware quantification of transcript expression
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A., & Kingsford, C. (2017) · Nature Methods · doi:10.1038/nmeth.4197 · Cited by 12,700 · see citing works
Conesa, A., Götz, S., Garcia-Gomez, J. M., Terol, J., Talón, M., & Robles, M. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti610 · Cited by 11,417 · see citing works
Control Mechanism of the Circadian Clock for Timing of Cell Division in Vivo
Matsuo, T., Yamaguchi, S., Mitsui, S., Emi, A., Shimoda, F., & Okamura, H. (2003) · Science · doi:10.1126/science.1086271 · Cited by 1,132 · see citing works
arrayQualityMetrics—a bioconductor package for quality assessment of microarray data
Kauffmann, A., Gentleman, R., & Huber, W. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btn647 · Cited by 946 · see citing works
Notch1 is required for the coordinate segmentation of somites
Conlon, R. A., Reaume, A. G., & Rossant, J. (1995) · Development · doi:10.1242/dev.121.5.1533 · Cited by 861 · see citing works
Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef
Babcock, R. C., Bull, G. D., Harrison, P. L., Heyward, A. J., Oliver, J. K., Wallace, C. C., & Willis, B. L. (1986) · Marine Biology · doi:10.1007/bf00428562 · Cited by 788 · see citing works
Mass spawning in tropical reef corals
Harrison, P. L., Babcock, R. C., Bull, G. D., Oliver, J. K., Wallace, C. C., & Willis, B. L. (1984) · Science · doi:10.1126/science.223.4641.1186 · Cited by 763 · see citing works
Oscillations in Notch Signaling Regulate Maintenance of Neural Progenitors
Shimojo, H., Ohtsuka, T., & Kageyama, R. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.014 · Cited by 706 · see citing works
Genomic determinants of coral heat tolerance across latitudes
Dixon, G., Davies, S. W., Aglyamova, G. V., Meyer, E., Bay, L. K., & Matz, M. V. (2015) · Science · doi:10.1126/science.1261224 · Cited by 490 · see citing works
Self-citationAncestral TSH Mechanism Signals Summer in a Photoperiodic Mammal
Hanon, É. A., Lincoln, G. A., Fustin, J., Dardente, H., Masson‐Pévet, M., Morgan, P. J., & Hazlerigg, D. G. (2008) · Current Biology · doi:10.1016/j.cub.2008.06.076 · Cited by 400 · see citing works
RNA-Seq workflow: gene-level exploratory analysis and differential expression
Love, M. I., Anders, S., Kim, V., & Huber, W. K. (2015) · F1000Research · doi:10.12688/f1000research.7035.1 · Cited by 397 · see citing works
Meyer, E., Aglyamova, G. V., & Matz, M. V. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05205.x · Cited by 363 · see citing works
Self-citationTemporal Coordination of Physiologic FunctionPreprint
Halberg, F. (1960) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1960.025.01.031 · Cited by 298 · see citing works
Moya, A., Huisman, L., Ball, E. E., Hayward, D. C., Grasso, L. C., Chua, C. M., WOO, H. N., Gattuso, J., Foret, S., & Miller, D. J. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05554.x · Cited by 293 · see citing works
A molecular switch for photoperiod responsiveness in mammals
Dardente, H., Wyse, C. A., Birnie, M. J., Dupré, S. M., Loudon, A. S. I., Lincoln, G. A., & Hazlerigg, D. G. (2010) · Current Biology · doi:10.1016/j.cub.2010.10.048 · Cited by 291 · see citing works
Levitan, D. R., Fukami, H., Jara, J., Kline, D. I., McGovern, T. M., McGhee, K. E., Swanson, C. A., & Knowlton, N. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01647.x · Cited by 284 · see citing works
Unexpected features of Drosophila circadian behavioural rhythms under natural conditions
Vanin, S., Bhutani, S., Montelli, S., Menegazzi, P., Green, E. W., Pegoraro, M., Sandrelli, F., Costa, R., & Kyriacou, C. P. (2012) · Nature · doi:10.1038/nature10991 · Cited by 255 · see citing works
Levitan, D. R., Fukami, H., Jara, J., et al. (2004) · Evolution · doi:10.1554/02-700 · Cited by 230 · see citing works
Evaluation of TagSeq, a reliable low‐cost alternative for RNA seq
Lohman, B. K., Weber, J. N., & Bolnick, D. I. (2016) · Molecular Ecology Resources · doi:10.1111/1755-0998.12529 · Cited by 219 · see citing works
Inhibition of Rhodopsin Kinase by Recoverin
Klenchin, V. A., Calvert, P. D., & Bownds, M. D. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.27.16147 · Cited by 208 · see citing works
Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra
Zhang, L., Hastings, M. H., Green, E. W., Tauber, E., Sladek, M., Webster, S. G., Kyriacou, C. P., & Wilcockson, D. C. (2013) · Current Biology · doi:10.1016/j.cub.2013.08.038 · Cited by 187 · see citing works
MicroRNA-9 Modulates Hes1 Ultradian Oscillations by Forming a Double-Negative Feedback Loop
Bonev, B., Stanley, P., & Papalopulu, N. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.017 · Cited by 186 · see citing works
Signaling cascades and the importance of moonlight in coral broadcast mass spawning
Kaniewska, P., Alon, S., Karako‐Lampert, S., Hoegh‐Guldberg, O., & Levy, O. (2015) · eLife · doi:10.7554/elife.09991 · Cited by 153 · see citing works
Penland, L. K., Kloulechad, J., Idip, D., Jr., & van Woesik, R. (2004) · Coral Reefs · doi:10.1007/s00338-003-0362-x · Cited by 151 · see citing works
Circadian and circalunar clock interactions in a marine annelid
Zantke, J., Ishikawa-Fujiwara, T., Arboleda, E., Lohs, C., Schipany, K., Hallay, N., Straw, A. D., Todo, T., & Tessmar-Raible, K. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.08.031 · Cited by 148 · see citing works
Light Directs Zebrafish period2 Expression via Conserved D and E Boxes
Vatine, G. D., Vallone, D., Appelbaum, L., Mracek, P., Ben-Moshe, Z., Lahiri, K., Gothilf, Y., & Foulkes, N. S. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000223 · Cited by 140 · see citing works
Kokubo, H., Lun, Y., & Johnson, R. L. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0880 · Cited by 139 · see citing works
Reporting neural activity with genetically encoded calcium indicators
Hires, S. A., Tian, L., & Looger, L. L. (2008) · Journal of Neurocytology · doi:10.1007/s11068-008-9029-4 · Cited by 137 · see citing works
Patro, R., Duggal, G., Love, M. I., et al. (2015) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/021592 · Cited by 129 · see citing works
Moonlight shifts the endogenous clock of Drosophila melanogaster
Bachleitner, W., Kempinger, L., Wülbeck, C., Rieger, D., & Helfrich‐Förster, C. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606870104 · Cited by 128 · see citing works
Calm before the spawn: global coral spawning patterns are explained by regional wind fields
van Woesik, R. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.1524 · Cited by 127 · see citing works
Coral mass spawning predicted by rapid seasonal rise in ocean temperature
Keith, S. A., Maynard, J. A., Edwards, A. J., Guest, J. R., Bauman, A. G., van Hooidonk, R. J., Heron, S. F., Berumen, M. L., Bouwmeester, J., Piromvaragorn, S., et al. (2016) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2016.0011 · Cited by 125 · see citing works
The Light Responsive Transcriptome of the Zebrafish: Function and Regulation
Weger, B. D., Weger, M., Otto, G., Mracek, P., Armant, O., Dolle, D. D., Lahiri, K., Vallone, D., Ettwiller, L. M., Geisler, R., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017080 · Cited by 113 · see citing works
The genomic basis of circadian and circalunar timing adaptations in a midge
Kaiser, T. S., Poehn, B., Szkiba, D., Preussner, M., Sedlazeck, F. J., Zrim, A., Neumann, T., Nguyen, L.-T., Betancourt, A. J., Hummel, T., et al. (2016) · Nature · doi:10.1038/nature20151 · Cited by 109 · see citing works
Levitan, D. R., Fogarty, N. D., Jara, J., et al. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01235.x · Cited by 101 · see citing works
Circadian clocks and cell division
Johnson, C. H. (2010) · Cell Cycle · doi:10.4161/cc.9.19.13205 · Cited by 98 · see citing works
Bertucci, A., Forêt, S., Ball, E. E., & Miller, D. J. (2015) · Molecular Ecology · doi:10.1111/mec.13328 · Cited by 77 · see citing works
Brady, A. K., Hilton, J., & Vize, P. D. (2009) · Coral Reefs · doi:10.1007/s00338-009-0498-4 · Cited by 74 · see citing works
Self-citationHunter, G. L., Hadjivasiliou, Z., Bonin, H., et al. (2016) · Development · doi:10.1242/dev.134213 · Cited by 64 · see citing works
Effects of Light Dynamics on Coral Spawning Synchrony
Boch, C. A., Ananthasubramaniam, B., Sweeney, A., et al. (2011) · Biological Bulletin · doi:10.1086/bblv220n3p161 · Cited by 63 · see citing works
Circadian cycles of gene expression in the coral, Acropora millepora
Brady, A. K., Snyder, K. A., & Vize, P. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025072 · Cited by 56 · see citing works
Self-citationOren, M., Tarrant, A. M., Alon, S., Simon‐Blecher, N., Elbaz, I., Appelbaum, L., & Levy, O. (2015) · Scientific Reports · doi:10.1038/srep11418 · Cited by 52 · see citing works
Brady, A. K., Willis, B. L., Harder, L. D., & Vize, P. D. (2016) · The Biological Bulletin · doi:10.1086/bblv230n2p130 · Cited by 48 · see citing works
Self-citationVize, P. D., Embesi, J. A., Nickell, M., Brown, D. P., & Hagman, D. K. (2005) · Gulf of Mexico Science · doi:10.18785/goms.2301.08 · Cited by 48 · see citing works
Self-citationFukushiro, M., Takeuchi, T., Takeuchi, Y., Hur, S.-P., Sugama, N., Takemura, A., Kubo, Y., Okano, K., & Okano, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028643 · Cited by 47 · see citing works
Transcriptome-wide Changes in Coral Gene Expression at Noon and Midnight Under Field Conditions
Ruiz-Jones, L. J., & Palumbi, S. R. (2015) · Biological Bulletin · doi:10.1086/bblv228n3p227 · Cited by 34 · see citing works
Diurnal and nocturnal transcriptomic variation in the Caribbean staghorn coral, Acropora cervicornis
Hemond, E. M., & Vollmer, S. V. (2015) · Molecular Ecology · doi:10.1111/mec.13320 · Cited by 31 · see citing works
Huang, Y., McNeil, G. P., & Jackson, F. R. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004536 · Cited by 31 · see citing works
Hepburn, R. I., Sale, P. F., Dixon, B., et al. (2008) · Coral Reefs · doi:10.1007/s00338-008-0423-2 · Cited by 31 · see citing works
Ikegami, T., Maruyama, Y., Doi, H., Hattori, A., & Ando, H. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00009 · Cited by 24 · see citing works
Hilton, J., Brady, A. K., Spaho, S. A., & Vize, P. D. (2012) · Biological Bulletin · doi:10.1086/bblv223n3p291 · Cited by 18 · see citing works
Self-citationKashiwagi, T., Park, Y., Park, J., Imamura, S., Takeuchi, Y., Hur, S., & Takemura, A. (2013) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.1814 · Cited by 15 · see citing works
Mayfield, A. B., Fan, T., & Chen, C.-S. (2013) · Journal of Marine Biology · doi:10.1155/2013/569361 · Cited by 15 · see citing works
Self-citationSex on the reef: mass spawning of corals
Wallace, C. C., Babcock, R. C., Harrison, P. L., et al. (1986) · Cross Connect (Southern Cross University) · Cited by 13 · see citing works
Curran, K. L., Allen, L. L., Bronson, B., Dodge, J., Lope, C., Willadsen, G., Fisher, R., Johnson, N. M., Campbell, E., VonBergen, B., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108266 · Cited by 10 · see citing works
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An Overview of Monthly Rhythms and Clocks
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Andreatta, G., & Tessmar-Raible, K. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.03.009 · Cited by 111 · see citing works
Schenk, S., Bannister, S. C., Sedlazeck, F. J., Anrather, D., Minh, B. Q., Bileck, A., Hartl, M., von Haeseler, A., Gerner, C., Raible, F., et al. (2019) · eLife · doi:10.7554/elife.41556 · Cited by 59 · see citing works
- Authors
- Oldach, M. J., Workentine, M., Matz, M. V., Fan, T., & Vize, P. D.
- Affiliations
- University of Calgary (CA)
- The University of Texas at Austin (US)
- National Museum of Marine Biology and Aquarium (TW)
- The University of Queensland (AU)
- Corresponding author
- Vize, Peter D.
- Venue
- Molecular Ecology
- Publisher
- Wiley
- Published
- 2017-02-23
- Volume
- 26
- Issue
- 9
- Pages
- 2514-2526
- ISSN
- 0962-1083 (ISSN-L)
- 1365-294X
- OpenAlex
- W2583215900
- Cited by
- 39
- References
- 60
- Citations by year
- 2025: 4 · 2024: 1 · 2023: 3 · 2022: 7 · 2021: 5 · 2020: 6 · 2019: 9 · 2018: 3 · 2017: 1
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Molecular Ecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- NMMBA
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- broadcast spawning, acroporid corals, lunar cycle, circalunar rhythm, clock genes, diel gene expression, lunar phases, coral reproduction, signal transduction, protein secretion, cell cycle, ion transport, lunar light
- MeSH terms
- Animals, Biological Clocks, Light, Moon, Anthozoa, CLOCK Proteins, Transcriptome
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