Circadian and circalunar clock interactions in a marine annelid
Open accessAbstract
Life is controlled by multiple rhythms. Although the interaction of the daily (circadian) clock with environmental stimuli, such as light, is well documented, its relationship to endogenous clocks with other periods is little understood. We establish that the marine worm Platynereis dumerilii possesses endogenous circadian and circalunar (monthly) clocks and characterize their interactions. The RNAs of likely core circadian oscillator genes localize to a distinct nucleus of the worm's forebrain. The worm's forebrain also harbors a circalunar clock entrained by nocturnal light. This monthly clock regulates maturation and persists even when circadian clock oscillations are disrupted by the inhibition of casein kinase 1δ/ε. Both circadian and circalunar clocks converge on the regulation of transcript levels. Furthermore, the circalunar clock changes the period and power of circadian behavior, although the period length of the daily transcriptional oscillations remains unaltered. We conclude that a second endogenous noncircadian clock can influence circadian clock function.
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In Platynereis dumerilii, exposure to continuous nocturnal light (constant FM) or never showing nocturnal light (constant NM) throughout entire growth results in arrhythmic spawning patterns.
“The exposure to continuous nocturnal light (“constant FM”) or never showing the worms nocturnal light (“constant NM”) throughout their entire growth (no entrainment) results in arrhythmic spawning patterns.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
In Platynereis dumerilii, the circalunar clock seems to also affect locomotor activity levels, with worms showing a weaker circadian rhythmicity during free-running FM compared to NM.
“In this species, the circalunar clock seems to also affect locomotor activity levels, with worms showing a weaker circadian rhythmicity during free-running FM (FR-FM) compared to NM.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
The monthly rhythm of Platynereis dumerilii relies on an endogenous circalunar oscillator, as it free-runs in absence of lunar cues.
“This monthly rhythm has been shown to rely on an endogenous circalunar oscillator, as it free-runs in absence of lunar cues [28].”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
The potential interaction between the circadian and the circalunar clocks has been well documented in Platynereis dumerilii.
“The potential interaction between the circadian and the circalunar clocks has been well documented in the marine bristleworm Platynereis dumerilii [28].”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
Platynereis dumerilii reproduces every month in specific lunar phases also in laboratory conditions, similarly to the field.
“This annelid reproduces every month in specific lunar phases also in laboratory conditions [28,34], similarly to the field [35].”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
In Platynereis dumerilii, most analyzed circadian clock genes showed similar circadian expression profiles in NM and FR-FM, but pdp1, period, clock, and tim had significantly higher mRNA levels during FR-FM.
“Most of the genes analyzed showed similar circadian expression profiles in the two different lunar phases, but significantly higher mRNA levels during FR-FM were found for pdp1, period, clock, and tim (see Figure 2), suggesting that a subset of circadian clock transcripts is affected by the circalunar clock, independently of nocturnal light cues.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
In Platynereis dumerilii, the monthly spawning rhythm was unaffected by exposure to PF-670462, a CK1δ/ε inhibitor.
“Interestingly, the spawning profile was found unaffected.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
P. dumerilii monthly spawning patterns are broader in the lab compared to the field.
“P. dumerilii monthly spawning patterns are broader in the lab [28] compared to the field [35]”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [28]
Members of the d-Cry/Cry1/Lcry family can function as photoreceptors activated by short-wavelength light in insect and annelid circadian clocks.
“members of the d-Cry/Cry1/Lcry family can function as photoreceptors (activated by short-wavelength light) in insect and annelid circadian clocks (22, 33, 35, 36)”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Platynereis tr-Cry functions as a transcriptional repressor, but not a light receptor, when tested in S2 tissue culture cells.
“When tested in S2 tissue culture cells, Platynereis tr-Cry functions as a transcriptional repressor, but not a light receptor, consistent with a conserved function of this molecule in transcriptional circadian control.”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Platynereis L-cry transcript fluctuations do not appear to follow a regular circadian pattern.
“These, however, do not appear to follow a regular circadian pattern (22).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Platynereis L-cry functions as a light receptor when tested in S2 cells and shows fluctuations in transcript levels between day and night.
“Also, Platynereis L-cry, which functions as a light receptor when tested in S2 cells, shows fluctuations in transcript levels between day and night.”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Platynereis tr-cry transcripts show clear circadian rhythmicity both during circadian light-dark and dark-dark conditions.
“The transcripts of tr-cry show a clear circadian rhythmicity (both during circadian light–dark and dark–dark conditions).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
In Platynereis, transcript levels of core circadian clock genes pdp1, period, and clock exhibit clear changes depending on the worm's endogenous circalunar clock: levels are significantly elevated during full moon phase compared to new moon phase, even in the absence of nocturnal light.
“In the bristle worm Platynereis, transcript levels of the core circadian clock genes, pdp1, period, and clock, exhibit clear changes depending on the worm’s endogenous circalunar clock: compared to samples taken during new moon phase, levels are significantly elevated during the full moon phase, even in the absence of nocturnal light (“free-running full moon”) (22).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Under nocturnal light conditions sufficient to reset the circalunar clock of Platynereis, oscillations of tr-cry are abolished, indicating that nocturnal light stimuli can affect circadian clock gene expression.
“Under nocturnal light conditions that are sufficient to reset the circalunar clock of these animals, the oscillations of tr-cry are abolished, indicating that nocturnal light stimuli can affect circadian clock gene expression.”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Both nocturnal light and the circalunar clock appear to impact expression of Platynereis L-cry.
“Both nocturnal light and the circalunar clock appear to impact on the expression of this gene.”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
There is no significant effect of the lunar clock itself on transcript levels of Platynereis tr-cry.
“Conversely, there is no significant effect of the lunar clock itself on the transcript levels of this gene (22, 28).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
In P. dumerilii, the circalunar clock has been shown to impact circadian rhythms of locomotor activity.
“Interestingly, at least in the bristle worm P. dumerilii, the circalunar clock has also been shown to impact on circadian rhythms of locomotor activity, suggesting the possibility that the observed transcript regulations might be linked to these activity changes (22).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
Pharmacological interference experiments in P. dumerilii suggest that circadian clock gene oscillations are not required to maintain circalunar rhythms in this species.
“Pharmacological interference experiments in the bristle worm P. dumerilii suggest that circadian clock gene oscillations are not required to maintain circalunar rhythms in this species (22).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [22]
gnrhl3 is mainly expressed in symmetrical patches in the medial forebrain domains expressing core circadian clock genes.
“The gnrhl3 gene was mainly expressed in symmetrical patches in the medial forebrain domains expressing core circadian clock genes (8) (SI Appendix, Fig. S2C).”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [8]
Worms exhibit a complex life cycle where food availability, circalunar cycle, and season regulate development and sexual maturation.
“Worms exhibit a complex life cycle where food availability, circalunar cycle, and season regulate development and sexual maturation (6–8).”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [8]
The marine bristleworm Platynereis dumerilii is well suited to tackle the endocrine basis of this integration.
“The marine bristleworm Platynereis dumerilii is well suited to tackle the endocrine basis of this integration.”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [8]
The number of spawning animals resulting from this regulation is lowest during the full moon phase.
“the number of spawning animals resulting from this regulation is lowest during the full moon phase (8, 11)”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [8]
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“These have been facilitated by reliable techniques such as in situ hybridization (Tessmar-Raible et al. 2005), quantitative PCR (Dray et al. 2010; Zantke et al. 2013), and image registration (Tomer et al. 2010).”
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Self-citationTowards a systems-level understanding of development in the marine annelid Platynereis dumerilii
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A Fast And Versatile Method for Simultaneous HCR, Immunohistochemistry And Edu Labeling (SHInE)
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All Light, Everywhere? Photoreceptors at Nonconventional Sites
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Self-citationTowards an Understanding of Circatidal Clocks
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Differential Impacts of the Head on Platynereis dumerilii Peripheral Circadian Rhythms
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Self-citationDemystifying Circalunar and Diel Rhythmicity in Acropora digitifera under Constant Dim Light
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Circadian and Circalunar Clock Interactions and the Impact of Light in Platynereis dumerilii
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Self-citationCoevolution of Drosophila-type timeless with partner clock proteins
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Redefining the photic zone: beyond the autotroph-centric view of light in the ocean
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Self-citationA marine cryptochrome with an inverse photo-oligomerization mechanism
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The Annelid Platynereis dumerilii as an Experimental Model for Evo-Devo and Regeneration Studies
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- Authors
- Zantke, J., Ishikawa-Fujiwara, T., Arboleda, E., Lohs, C., Schipany, K., Hallay, N., Straw, A. D., Todo, T., & Tessmar-Raible, K.
- Affiliations
- University of Vienna (AT)
- The University of Osaka (JP)
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2013-10
- Volume
- 5
- Issue
- 1
- Pages
- 99-113
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC3913041
- OpenAlex
- W1985740972
- Cited by
- 148
- References
- 78
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 9 · 2023: 11 · 2022: 12 · 2021: 14 · 2020: 10 · 2019: 12 · 2018: 11 · 2017: 18 · 2016: 15 · 2015: 3 · 2014: 14 · 2013: 5
- FWCI
- 6.67
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Phaidra (Universität Wien) (submittedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/K009702/1, BB/E000835/1)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- circadian clock, Platynereis dumerilii, Polychaeta, clock gene expression, forebrain, transcriptional oscillations, clock period, RNA localization
- MeSH terms
- Animals, Annelida, Circadian Rhythm, Female, Male, Molecular Sequence Data, Circadian Clocks
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