A Flavin Binding Cryptochrome Photoreceptor Responds to Both Blue and Red Light in <i>Chlamydomonas reinhardtii</i>

Beel, Benedikt; Prager, Katja; Spexard, Meike; Sasso, Severin; Weiß, Daniel L.; Müller, Nico; Heinnickel, Mark; Dewez, David; Ikoma, Danielle; Grossman, Arthur R.; Kottke, Tilman; Mittag, Maria

doi:10.1105/tpc.112.098947

Cited by 159 publications

(255 citation statements)

References 88 publications

(111 reference statements)

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“…S7A). This decline in ROC15 mRNA abundance following exposure to light was consistent with a recent report (20). Western blot analysis indicated that ROC15-HA protein expression disappeared almost completely within 20 min under the same experimental conditions (SI Appendix, Fig.…”

Section: The Rapid Decrease In Roc15-luc Bioluminescence Occurred Mainlysupporting

confidence: 78%

Phase-resetting mechanism of the circadian clock in Chlamydomonas reinhardtii

Niwa

Matsuo

Onai

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Although the circadian clock is a self-sustaining oscillator having a periodicity of nearly 1 d, its period length is not necessarily 24 h. Therefore, daily adjustment of the clock (i.e., resetting) is an essential mechanism for the circadian clock to adapt to daily environmental changes. One of the major cues for this resetting mechanism is light. In the unicellular green alga Chlamydomonas reinhardtii, the circadian clock is reset by blue/green and red light. However, the underlying molecular mechanisms remain largely unknown. In this study, using clock protein-luciferase fusion reporters, we found that the level of RHYTHM OF CHLOROPLAST 15 (ROC15), a clock component in C. reinhardtii, decreased rapidly after light exposure in a circadian-phase-independent manner. Blue, green, and red light were able to induce this process, with red light being the most effective among them. Expression analyses and inhibitor experiments suggested that this process was regulated mainly by a proteasome-dependent protein degradation pathway. In addition, we found that the other clock gene, ROC114, encoding an F-box protein, was involved in this process. Furthermore, we demonstrated that a roc15 mutant showed defects in the phase-resetting of the circadian clock by light. Taken together, these data strongly suggest that the light-induced degradation of ROC15 protein is one of the triggers for resetting the circadian clock in C. reinhardtii. Our data provide not only a basis for understanding the molecular mechanisms of light-induced phase-resetting in C. reinhardtii, but also insights into the phase-resetting mechanisms of circadian clocks in plants.LUCnc | light pulse | phase shift C ircadian rhythms, observed ubiquitously in organisms from prokaryotic cyanobacteria to humans, are generated by the circadian clock, which is thought to rely on transcriptional/translational feedback loops and posttranslational biochemical oscillations of some genes and their protein products called clock genes/proteins (1-4). Clock genes/proteins have been identified in several organisms, including mammals, insects, fungi, land plants, cyanobacteria, and, recently, green algae (1, 2, 5-8). Except for general kinases and phosphatases (9), most of the components of circadian clocks are not conserved among evolutionarily divergent organisms. On the other hand, the components are conserved to some extent between organisms that are relatively close evolutionarily (i.e., mammals and insects, land plants and green algae) (6-8, 10).The clock components in algae were first identified in the model green alga Chlamydomonas reinhardtii. There are the RNAbinding protein complex CHLAMY1 (11), a casein kinase (12), and RHYTHM OF CHLOROPLAST (ROC) proteins, including putative DNA-binding proteins (ROC15, ROC40, ROC66, and ROC75), an F-box protein (ROC114), and a leucine-rich repeat protein (ROC55) (13). The DNA-binding motifs of ROC proteins are homologous to those of Arabidopsis thaliana proteins associated with the circadian clock and photoperiodic flowering (13)...

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Section: The Rapid Decrease In Roc15-luc Bioluminescence Occurred Mainlysupporting

confidence: 78%

Phase-resetting mechanism of the circadian clock in Chlamydomonas reinhardtii

Niwa

Matsuo

Onai

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…CrCRYa is an animal-type cryptochrome that responds to both blue and red light. In red light, CrCRYa affects the transcript levels of the genes for the glutamate-1-semialdehyde aminotransferase (GSA), light-harvesting proteins (e.g., LHCBM6) and the psbA-binding protein (Beel et al 2012b). So far no typical red light receptor, such as phytochrome, has been identified in C. reinhardtii or in the related alga V. carteri Mittag et al 2005;Prochnik et al 2010).…”

Section: Animal-like Cryptochromesmentioning

confidence: 99%

“…Recently, another cryptochrome of the alga C. reinhardtii, CrCRYa, was characterized (Beel et al 2012b). CrCRYa is an animal-type cryptochrome that responds to both blue and red light.…”

Section: Animal-like Cryptochromesmentioning

confidence: 99%

Algal photoreceptors: in vivo functions and potential applications

Kianianmomeni

Hallmann

2013

Planta

103

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“…Although chlorophytes retain the ability to synthesize chlorophyll in the absence of light and do not accumulate protochlorophyllide in darkness (45), light-dependent accumulation of chlorophyll is likely to be mediated by at least one photoreceptor. Indeed, cryptochromes and phototropins have been implicated in the lightregulated expression of various components of the C. reinhardtii photosynthetic apparatus (29,30,46). To test the hypothesis that bilins play a regulatory role during the dark-light transition in C. reinhardtii, we performed a multifactor transcriptome analysis using RNA sequencing (RNA-seq).…”

Section: Global Transcriptomic Analysis Reveals a Bilin-specific Netwmentioning

confidence: 99%

Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival

Duanmu

Casero

Dent

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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105

172

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The maintenance of functional chloroplasts in photosynthetic eukaryotes requires real-time coordination of the nuclear and plastid genomes. Tetrapyrroles play a significant role in plastid-tonucleus retrograde signaling in plants to ensure that nuclear gene expression is attuned to the needs of the chloroplast. Well-known sites of synthesis of chlorophyll for photosynthesis, plant chloroplasts also export heme and heme-derived linear tetrapyrroles (bilins), two critical metabolites respectively required for essential cellular activities and for light sensing by phytochromes. Here we establish that Chlamydomonas reinhardtii, one of many chlorophyte species that lack phytochromes, can synthesize bilins in both plastid and cytosol compartments. Genetic analyses show that both pathways contribute to iron acquisition from extracellular heme, whereas the plastid-localized pathway is essential for light-dependent greening and phototrophic growth. Our discovery of a bilin-dependent nuclear gene network implicates a widespread use of bilins as retrograde signals in oxygenic photosynthetic species. Our studies also suggest that bilins trigger critical metabolic pathways to detoxify molecular oxygen produced by photosynthesis, thereby permitting survival and phototrophic growth during the light period.biliverdin | heme oxygenase | iron homeostasis | oxidative stress | RNA-Seq analysisT he daily light-dark cycle requires all oxygenic photosynthetic species to survive the repeated transition from prolonged darkness to phototrophic metabolism at dawn. Most plants are unable to synthesize chlorophyll in darkness and therefore accumulate photosensitizing chlorophyll precursors at night (1). Sunrise induces an oxidative burst as photosynthesis resumes, so the transition to daylight requires careful coordination of many lightdependent processes. Multiple photoreceptors perform such roles in plants, the most notable being the red-sensing, linear tetrapyrrole (bilin)-based phytochromes and the blue-sensing, flavin-based cryptochromes and phototropins (2-5). Bilins are well-established plant retrograde signals, synthesized in plastids but enabling light sensing by cytosolic phytochromes. Phytochrome photoconversion then triggers nuclear translocation to positively regulate photosynthesis-associated nuclear gene (PhANG) expression (6, 7).Genetic studies suggest that plastids also export negative retrograde signals, metabolites that suppress nuclear gene networks targeted by phytochromes (8-10). Among these metabolites are abscisic acid (ABA) (11), tetrapyrroles (12-14), 3′-phosphoadenosine 5′-phosphate (PAP) (15), β-cyclocitral (16), and methylerythritol cyclodiphosphate (MEcPP) (17). Although hypothetical export of a negative tetrapyrrole signal has received considerable support, biochemical evidence for such a retrograde signal remains equivocal in plants (18)(19)(20). Chlorophyte algae diverged from the streptophyte plant lineage over 500 million years ago but share a common chlorophyll a/b-based photosynthetic lightharvesting app...

show abstract

A Flavin Binding Cryptochrome Photoreceptor Responds to Both Blue and Red Light in Chlamydomonas reinhardtii

Cited by 159 publications

References 88 publications

Phase-resetting mechanism of the circadian clock in Chlamydomonas reinhardtii

Phase-resetting mechanism of the circadian clock in Chlamydomonas reinhardtii

Algal photoreceptors: in vivo functions and potential applications

Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival

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