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Probing entrainment of Ostreococcus tauri circadian clock by green and blue light through a mathematical modeling approach.

Thommen Q, Pfeuty B, Schatt P, Bijoux A, Bouget FY, Lefranc M - Front Genet (2015)

Bottom Line: This model agrees with clock gene expression time series representative of multiple environmental conditions in blue or green light, characterizing entrainment by light/dark cycles, free-running in constant light, and resetting.Experimental and theoretical results indicate that both blue and green light can reset O. tauri circadian clock.Moreover, our mathematical analysis suggests that Rhod-HK is a blue-green light receptor and drives the clock together with LOV-HK.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Physique, Lasers, Atomes, Molécules, Université Lille 1 Sciences et Technologies, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8523 Villeneuve d'Ascq, France.

ABSTRACT
Most organisms anticipate daily environmental variations and orchestrate cellular functions thanks to a circadian clock which entrains robustly to the day/night cycle, despite fluctuations in light intensity due to weather or seasonal variations. Marine organisms are also subjected to fluctuations in light spectral composition as their depth varies, due to differential absorption of different wavelengths by sea water. Studying how light input pathways contribute to circadian clock robustness is therefore important. Ostreococcus tauri, a unicellular picoplanktonic marine green alga with low genomic complexity and simple cellular organization, has become a promising model organism for systems biology. Functional and modeling approaches have shown that a core circadian oscillator based on orthologs of Arabidopsis TOC1 and CCA1 clock genes accounts for most experimental data acquired under a wide range of conditions. Some evidence points at putative light input pathway(s) consisting of a two-component signaling system (TCS) controlled by the only two histidine kinases (HK) of O. tauri. LOV-HK is a blue light photoreceptor under circadian control, that is required for circadian clock function. An involvement of Rhodopsin-HK (Rhod-HK) is also conceivable since rhodopsin photoreceptors mediate blue to green light input in animal circadian clocks. Here, we probe the role of LOV-HK and Rhod-HK in mediating light input to the TOC1-CCA1 oscillator using a mathematical model incorporating the TCS hypothesis. This model agrees with clock gene expression time series representative of multiple environmental conditions in blue or green light, characterizing entrainment by light/dark cycles, free-running in constant light, and resetting. Experimental and theoretical results indicate that both blue and green light can reset O. tauri circadian clock. Moreover, our mathematical analysis suggests that Rhod-HK is a blue-green light receptor and drives the clock together with LOV-HK.

No MeSH data available.


Related in: MedlinePlus

Schematic diagram of the biochemical reaction network. The upper panel recapitulates the transcriptional regulations (activation or repression) between molecular actors. The lower panel summarizes the post-translational modifications induced by the phosphate transfer cascade.
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Figure 1: Schematic diagram of the biochemical reaction network. The upper panel recapitulates the transcriptional regulations (activation or repression) between molecular actors. The lower panel summarizes the post-translational modifications induced by the phosphate transfer cascade.

Mentions: As most genes in O. tauri, LOV-HK and Rhod-HK mRNAs display strong daily variations, and peak respectively near dawn and dusk in LD 12:12 conditions (12 h of light alternating with 12 h of darkness) (Djouani-Tahri et al., 2011; Pfeuty et al., 2012). Moreover, LOV-HK-Luc luminescent reporter displays rhythms in constant light conditions, showing that LOV-HK is circadianly regulated. The simplest way to take these facts into account is to assume that the two light sensors are directly regulated by the core proteins TOC1 and CCA1, and we accordingly tested different hypotheses. We obtained good adjustment of the model to the data when we hypothesized that CCA1 represses Rhod-HK and TOC1 represses LOV-HK. However, it may seem strange that TOC1 acts both as a repressor and an activator, even though the transcriptional role of Arabidopsis TOC1 has been recently debated (Pruneda-Paz et al., 2009). Therefore, we considered in our model that while Rhod-HK is directly repressed by CCA1, LOV-HK is indirectly activated by it. More precisely, LOV-HK is assumed to be repressed by an unknown actor X, which is in turn repressed by CCA1. This is consistent with the observation that LOV-HK is most expressed in the morning and Rhod-HK in the evening. We insist that while these putative regulations are interesting and reasonable hypotheses, their correctness is not essential for our work, which focuses on the light input to the TOC1–CCA1 oscillator. At this stage, their role is only to generate the correct mRNA time profiles in the mathematical model. The corresponding molecular network is depicted in Figure 1.


Probing entrainment of Ostreococcus tauri circadian clock by green and blue light through a mathematical modeling approach.

Thommen Q, Pfeuty B, Schatt P, Bijoux A, Bouget FY, Lefranc M - Front Genet (2015)

Schematic diagram of the biochemical reaction network. The upper panel recapitulates the transcriptional regulations (activation or repression) between molecular actors. The lower panel summarizes the post-translational modifications induced by the phosphate transfer cascade.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4343026&req=5

Figure 1: Schematic diagram of the biochemical reaction network. The upper panel recapitulates the transcriptional regulations (activation or repression) between molecular actors. The lower panel summarizes the post-translational modifications induced by the phosphate transfer cascade.
Mentions: As most genes in O. tauri, LOV-HK and Rhod-HK mRNAs display strong daily variations, and peak respectively near dawn and dusk in LD 12:12 conditions (12 h of light alternating with 12 h of darkness) (Djouani-Tahri et al., 2011; Pfeuty et al., 2012). Moreover, LOV-HK-Luc luminescent reporter displays rhythms in constant light conditions, showing that LOV-HK is circadianly regulated. The simplest way to take these facts into account is to assume that the two light sensors are directly regulated by the core proteins TOC1 and CCA1, and we accordingly tested different hypotheses. We obtained good adjustment of the model to the data when we hypothesized that CCA1 represses Rhod-HK and TOC1 represses LOV-HK. However, it may seem strange that TOC1 acts both as a repressor and an activator, even though the transcriptional role of Arabidopsis TOC1 has been recently debated (Pruneda-Paz et al., 2009). Therefore, we considered in our model that while Rhod-HK is directly repressed by CCA1, LOV-HK is indirectly activated by it. More precisely, LOV-HK is assumed to be repressed by an unknown actor X, which is in turn repressed by CCA1. This is consistent with the observation that LOV-HK is most expressed in the morning and Rhod-HK in the evening. We insist that while these putative regulations are interesting and reasonable hypotheses, their correctness is not essential for our work, which focuses on the light input to the TOC1–CCA1 oscillator. At this stage, their role is only to generate the correct mRNA time profiles in the mathematical model. The corresponding molecular network is depicted in Figure 1.

Bottom Line: This model agrees with clock gene expression time series representative of multiple environmental conditions in blue or green light, characterizing entrainment by light/dark cycles, free-running in constant light, and resetting.Experimental and theoretical results indicate that both blue and green light can reset O. tauri circadian clock.Moreover, our mathematical analysis suggests that Rhod-HK is a blue-green light receptor and drives the clock together with LOV-HK.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Physique, Lasers, Atomes, Molécules, Université Lille 1 Sciences et Technologies, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8523 Villeneuve d'Ascq, France.

ABSTRACT
Most organisms anticipate daily environmental variations and orchestrate cellular functions thanks to a circadian clock which entrains robustly to the day/night cycle, despite fluctuations in light intensity due to weather or seasonal variations. Marine organisms are also subjected to fluctuations in light spectral composition as their depth varies, due to differential absorption of different wavelengths by sea water. Studying how light input pathways contribute to circadian clock robustness is therefore important. Ostreococcus tauri, a unicellular picoplanktonic marine green alga with low genomic complexity and simple cellular organization, has become a promising model organism for systems biology. Functional and modeling approaches have shown that a core circadian oscillator based on orthologs of Arabidopsis TOC1 and CCA1 clock genes accounts for most experimental data acquired under a wide range of conditions. Some evidence points at putative light input pathway(s) consisting of a two-component signaling system (TCS) controlled by the only two histidine kinases (HK) of O. tauri. LOV-HK is a blue light photoreceptor under circadian control, that is required for circadian clock function. An involvement of Rhodopsin-HK (Rhod-HK) is also conceivable since rhodopsin photoreceptors mediate blue to green light input in animal circadian clocks. Here, we probe the role of LOV-HK and Rhod-HK in mediating light input to the TOC1-CCA1 oscillator using a mathematical model incorporating the TCS hypothesis. This model agrees with clock gene expression time series representative of multiple environmental conditions in blue or green light, characterizing entrainment by light/dark cycles, free-running in constant light, and resetting. Experimental and theoretical results indicate that both blue and green light can reset O. tauri circadian clock. Moreover, our mathematical analysis suggests that Rhod-HK is a blue-green light receptor and drives the clock together with LOV-HK.

No MeSH data available.


Related in: MedlinePlus