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PubMed2006

The polycomb group protein EZH2 is required for mammalian circadian clock function.

We examined the importance of histone methylation by the polycomb group proteins in the mouse circadian clock mechanism. Endogenous EZH2, a polycomb group enzyme that methylates lysine 27 on histone H3, co-immunoprecipitates with CLOCK and BMAL1 throughout the circadian cycle in liver nuclear extracts. Chromatin immunoprecipitation revealed EZH2 binding and di- and trimethylation of H3K27 on both the Period 1 and Period 2 promoters. A role of EZH2 in cryptochrome-mediated transcriptional repression of the clockwork was supported by overexpression and RNA interference studies. Serum-induced circadian rhythms in NIH 3T3 cells in culture were disrupted by transfection of an RNA interfering sequence targeting EZH2. These results indicate that EZH2 is important for the maintenance of circadian rhythms and extend the activity of the polycomb group proteins to the core clockwork mechanism of mammals.

ARNTL Transcription Factors↗
PubMed2006

Mapping of binding regions for the circadian regulators BMAL1 and CLOCK within the mouse Rev-erbalpha gene.

Two major interconnected feedback loops govern circadian rhythmicity in mammals. The transcriptional activators BMAL1/MOP3 and CLOCK drive one loop by binding to E-box motifs in the regulatory regions of circadian target genes. Time-of-day-dependent inhibition of the activity of BMAL1 and CLOCK by PERIOD (PER) and CRYPTOCHROME (CRY) proteins provokes consequent rhythmic gene expression. In this fashion, the Per and Cry genes can feedback onto their own synthesis. The orphan nuclear receptor Rev-erbalpha manifests the second feedback loop. Genetically linked to the molecular oscillator, it was identified as a repressor of the Bmal1 and Clock genes. In an attempt to understand the circadian regulation of the mouse Rev-erbalpha gene, we developed a screening technique for BMAL1 and CLOCK binding regions consisting of chromatin-immunoprecipitation. Here we show that the mouse Rev-erbalpha gene contains at least two binding regions for the transcriptional activators close to its previously identified promoter region and in its first intron. However, our data also indicate that not all potential E-box motifs in vitro are occupied in vivo.

ARNTL Transcription Factors↗
PubMed2003

Neural organization of the circadian system of the cockroach Leucophaea maderae.

The cockroach Leucophaea maderae was the first animal in which lesion experiments localized an endogenous circadian clock to a particular brain area, the optic lobe. The neural organization of the circadian system, however, including entrainment pathways, coupling elements of the bilaterally distributed internal clock, and output pathways controlling circadian locomotor rhythms are only recently beginning to be elucidated. As in flies and other insect species, pigment-dispersing hormone (PDH)-immunoreactive neurons of the accessory medulla of the cockroach are crucial elements of the circadian system. Lesions and transplantation experiments showed that the endogeneous circadian clock of the brain resides in neurons associated with the accessory medulla. The accessory medulla is organized into a nodular core receiving photic input, and into internodular and peripheral neuropil involved in efferent output and coupling input. Photic entrainment of the clock through compound eye photoreceptors appears to occur via parallel, indirect pathways through the medulla. Light-like phase shifts in circadian locomotor activity after injections of gamma-aminobutyric acid (GABA)- or Mas-allatotropin into the vicinity of the accessory medulla suggest that both substances are involved in photic entrainment Extraocular, cryptochrome-based photoreceptors appear to be present in the optic lobe, but their role in photic entrainment has not been examined. Pigment-dispersing hormone-immunoreactive neurons provide efferent output from the accessory medulla to several brain areas and to the peripheral visual system. Pigment-dispersing hormone-immunoreactive neurons, and additional heterolateral neurons are, furthermore, involved in bilateral coupling of the two pacemakers. The neuronal organization, as well as the prominent involvement of GABA and neuropeptides, shows striking similarities to the organization of the suprachiasmatic nucleus, the circadian clock of the mammalian brain.

Animals↗
PubMed2004

Unique self-sustaining circadian oscillators within the brain of Drosophila melanogaster.

In Drosophila circadian rhythms persist in constant darkness (DD). The small ventral Lateral Neurons (s-LNv) mainly control the behavioral circadian rhythm in consortium with the large ventral Lateral Neurons (l-LNv) and dorsal Lateral Neurons (LNd). It is believed that the molecular oscillations of clock genes are the source of this persistent behavior. Indeed the s-LNv, LNd, Dorsal Neurons (DN)-DN2 and DN3 displayed self-sustained molecular oscillations in DD both at RNA and protein levels, except the DN2 oscillates in anti-phase. In contrast, the l-LNv and DN1 displayed self-sustained oscillations at the RNA level, but protein oscillations quickly dampened. Having self-sustained and dampened molecular oscillators together in the DN groups suggested that they play different roles. However, all DN groups seemed to contribute together to the light-dark (LD) behavioral rhythm. The LD entrainment of LN oscillators is achieved through Rhodopsin (RH) and Cryptochrome (CRY). CRY's expression in all DN groups implicates also its role in LD entrainment of DN, like in DN1. However, mutations in cry and glass that did not inflict LD synchronization of the DN2, DN3 oscillator implicate the existence of a novel photoreceptor at least in DN3.

Animals↗
PubMed2005

Caenorhabditis elegans opens up new insights into circadian clock mechanisms.

The roundworm, Caenorhabditis elegans, is known to carry homologues of clock genes such as per (=period) and tim (=timeless), which constitute the core of the circadian clock in Drosophila and mammals: lin-42 and tim-1. Analyses using WormBase (C. elegans gene database) have identified with relatively high identity analogous of the clock genes recognized in Drosophila and mammals, with the notable exception of cry (=cryptochrome), which is lacking in C. elegans. All of these C. elegans cognates of the clock genes appear to belong to members of the PAS-superfamily and to participate in development or responsiveness to the environment but apparently are not involved in the C. elegans circadian clock. Nevertheless, C. elegans exhibits convincing circadian rhythms in locomotor behavior in the adult stage and in resistance to hyperosmotic stress in starved larvae (L1) after hatching, indicating that it has a circadian clock with a core design entirely different from that of Drosophila and mammals. Here two possibilities are considered. First, the core of the C. elegans circadian clock includes transcriptional/translational feedback loops between genes and their protein products that are entirely different from those of Drosophila and mammals. Second, a more basic principle such as homeostasis governs the circadian cellular physiology, and was established primarily to minimize the accumulation of DNA damage in response to an environment cycling at 24 h intervals.

Animals↗
PubMed2003

Molecular mechanism of mammalian circadian clock.

Circadian rhythms in behaviors and physiological phenomena of plants and animals have long been well known, but the frameworks of the molecular mechanism of circadian clocks have become clearer only within the last decade. A transcription-translation feedback loop has been shown to be an essential component of the clock, and this mechanism seems to be conserved over a wide range of species. The transcriptional activation by a Clock:Bmal1 heterodimer and the inhibition by Cryptochrome and Period are believed to provide the framework of the feedback loop in mammals. Posttranslational modifications such as phosphorylation, nuclear entry and degradation have also been demonstrated to be necessary for the oscillation. Complex auxiliary loops have also been found, and these are thought to contribute to the stabilization of the feedback loop. The molecular mechanisms by which the circadian clock is adjusted to external conditions such as daily light-dark cycles, and by which the oscillation of the feedback loop is transferred to the peripheral organs are also discussed.

Animals↗
PubMed2003

Light signals, phytochromes and cross-talk with other environmental cues.

Plants have evolved highly complex sensory mechanisms to monitor their surroundings and adapt their growth and development to the prevailing environmental conditions. The integration of information from multiple environmental cues enables the co-ordination of development with favourable seasonal conditions and, ultimately, determines plant form. Light signals, perceived via the phytochrome, cryptochrome and phototropin photoreceptor families, are especially important environmental signals. Redundancy of function among phytochromes and their interaction with blue light photoreceptors enhance sensitivity to light signals, facilitating the accurate detection of, and response to, environmental fluctuations. In this review, current understanding of Arabidopsis phytochrome functions will be summarized, in particular, the interactions among the phytochromes and the integration of light signals with directional and temperature sensing mechanisms.

Environment↗
PubMed2004

Cytokinins induce photomorphogenic development in dark-grown gametophytes of Ceratopteris richardii.

The cytokinins benzylaminopurine, kinetin and isopentenyladenine induce photomorphogenesis in dark-grown gametophytes of the fern Ceratopteris richardii. At sub-nanomolar concentrations each altered the rate and pattern of cell division, elongation and differentiation, mimicking aspects of the light-mediated transition from filamentous to prothallial growth. Untreated dark-grown gametophytes grow as narrow, elongate, asexual filaments with an apical meristem. Cytokinin treatments as low as 10(-12) M reduced the length-to-width ratio through decreased cell elongation, increased periclinal cell division and induced the formation of rhizoid initials in the cells immediately below the apical meristem. Higher concentrations (10(-9)-10(-8) M) induced conversion of the meristem from apical to notch morphology. Cytokinins induced both red- and blue-light-mediated photomorphogenic events, suggesting stimulation of both phytochrome and cryptochrome signaling; however, cytokinin treatment only partially substituted for light in that it did not induce hermaphroditic sexual development or spore germination in the dark. Additionally, cytokinins did not increase chlorophyll synthesis in dark-grown gametophytes, which unlike angiosperms are able to produce mature chloroplasts in the dark. Cytokinin treatment had only slight effects on light-grown gametophytes. These results suggest evolutionary conservation between angiosperms and pteridophytes in the role of cytokinins in regulating photomorphogenesis.

Cytokinins↗
PubMed2024

Alternative localization of HEME OXYGENASE 1 in plant cells regulates cytosolic heme catabolism.

Heme, an organometallic tetrapyrrole, is widely engaged in oxygen transport, electron delivery, enzymatic reactions, and signal transduction. In plants, it is also involved in photomorphogenesis and photosynthesis. HEME OXYGENASE 1 (HO1) initiates the first committed step in heme catabolism, and it has generally been thought that this reaction takes place in chloroplasts. Here, we show that HO1 in both Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa) has 2 transcription start sites (TSSs), producing long (HO1L) and short (HO1S) transcripts. Their products localize to the chloroplast and the cytosol, respectively. During early development or de-etiolation, the HO1L/HO1S ratio gradually increases. Light perception via phytochromes (Phys) and cryptochromes elevates the HO1L/HO1S ratio in the whole seedling through the functions of ELONGATED HYPOCOTYL 5 (HY5) and HY5 HOMOLOG and through the suppression of DE-ETIOLATED 1, CONSTITUTIVE PHOTOMORPHOGENESIS 1, and PHYTOCHROME INTERACTING FACTORs. HO1L introduction complements the HO1-deficient mutant; surprisingly, HO1S expression also restores the short hypocotyl phenotype and high pigment content and helps the mutant recover from the genomes uncoupled (gun) phenotype. This indicates the assembly of functional Phys within these lines. Furthermore, our findings support the hypothesis that a mobile heme signal is involved in retrograde signaling from the chloroplast. Altogether, our work clarifies the molecular mechanism of HO1 TSS regulation and highlights the presence of a cytosolic bypass for heme catabolism in plant cells.

Heme↗
PubMed2003

Redox and light regulation of gene expression in photosynthetic prokaryotes.

All photosynthetic organisms control expression of photosynthesis genes in response to alterations in light intensity as well as to changes in cellular redox potential. Light regulation in plants involves a well-defined set of red- and blue-light absorbing photoreceptors called phytochrome and cryptochrome. Less understood are the factors that control synthesis of the plant photosystem in response to changes in cellular redox. Among a diverse set of photosynthetic bacteria the best understood regulatory systems are those synthesized by the photosynthetic bacterium Rhodobacter capsulatus. This species uses the global two-component signal transduction cascade, RegB and RegA, to anaerobically de-repress anaerobic gene expression. Under reducing conditions, the phosphate on RegB is transferred to RegA, which then activates genes involved in photosynthesis, nitrogen fixation, carbon fixation, respiration and electron transport. In the presence of oxygen, there is a second regulator known as CrtJ, which is responsible for repressing photosynthesis gene expression. CrtJ responds to redox by forming an intramolecular disulphide bond under oxidizing, but not reducing, growth conditions. The presence of the disulphide bond stimulates DNA binding activity of the repressor. There is also a flavoprotein that functions as a blue-light absorbing anti-repressor of CrtJ in the related bacterial species Rhodobacter sphaeroides called AppA. AppA exhibits a novel long-lived photocycle that is initiated by blue-light absorption by the flavin. Once excited, AppA binds to CrtJ thereby inhibiting the repressor activity of CrtJ. Various mechanistic aspects of this photocycle will be discussed.

Bacteria↗
PubMed2003

The Arabidopsis SRR1 gene mediates phyB signaling and is required for normal circadian clock function.

Plants possess several photoreceptors to sense the light environment. In Arabidopsis cryptochromes and phytochromes play roles in photomorphogenesis and in the light input pathways that synchronize the circadian clock with the external world. We have identified SRR1 (sensitivity to red light reduced), a gene that plays an important role in phytochrome B (phyB)-mediated light signaling. The recessive srr1 null allele and phyB mutants display a number of similar phenotypes indicating that SRR1 is required for normal phyB signaling. Genetic analysis suggests that SRR1 works both in the phyB pathway but also independently of phyB. srr1 mutants are affected in multiple outputs of the circadian clock in continuous light conditions, including leaf movement and expression of the clock components, CCA1 and TOC1. Clock-regulated gene expression is also impaired during day-night cycles and in constant darkness. The circadian phenotypes of srr1 mutants in all three conditions suggest that SRR1 activity is required for normal oscillator function. The SRR1 gene was identified and shown to code for a protein conserved in numerous eukaryotes including mammals and flies, implicating a conserved role for this protein in both the animal and plant kingdoms.

Amino Acid Sequence↗
PubMed2006

Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock.

The circadian clock of the honey bee is implicated in ecologically relevant complex behaviors. These include time sensing, time-compensated sun-compass navigation, and social behaviors such as coordination of activity, dance language communication, and division of labor. The molecular underpinnings of the bee circadian clock are largely unknown. We show that clock gene structure and expression pattern in the honey bee are more similar to the mouse than to Drosophila. The honey bee genome does not encode an ortholog of Drosophila Timeless (Tim1), has only the mammalian type Cryptochrome (Cry-m), and has a single ortholog for each of the other canonical "clock genes." In foragers that typically have strong circadian rhythms, brain mRNA levels of amCry, but not amTim as in Drosophila, consistently oscillate with strong amplitude and a phase similar to amPeriod (amPer) under both light-dark and constant darkness illumination regimes. In contrast to Drosophila, the honey bee amCYC protein contains a transactivation domain and its brain transcript levels oscillate at virtually an anti-phase to amPer, as it does in the mouse. Phylogenetic analyses indicate that the basal insect lineage had both the mammalian and Drosophila types of Cry and Tim. Our results suggest that during evolution, Drosophila diverged from the ancestral insect clock and specialized in using a set of clock gene orthologs that was lost by both mammals and bees, which in turn converged and specialized in the other set. These findings illustrate a previously unappreciated diversity of insect clockwork and raise critical questions concerning the evolution and functional significance of species-specific variation in molecular clockwork.

Amino Acid Motifs↗
PubMed2003

A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development.

A microarray based on PCR amplicons of 1864 confirmed and predicted Arabidopsis transcription factor genes was produced and used to profile the global expression pattern in seedlings, specifically their light regulation. We detected expression of 1371 and 1241 genes in white-light- and dark-grown 6-d-old seedlings, respectively. Together they account for 84% of the transcription factor genes examined. This array was further used to study the kinetics of transcription factor gene expression change of dark-grown seedlings in response to blue light and the role of specific photoreceptors in this blue-light regulation. The expression of about 20% of those transcription factor genes are responsive to blue-light exposure, with 249 and 115 genes up or down-regulated, respectively. A large portion of blue-light-responsive transcription factor genes exhibited very rapid expression changes in response to blue light, earlier than the bulk of blue-light-regulated genes. This result suggests the involvement of transcription cascades in blue-light control of genome expression. Comparative analysis of the expression profiles of wild type and various photoreceptor mutants demonstrated that during early seedling development cryptochromes are the major photoreceptors for blue-light control of transcription factor gene expression, whereas phytochrome A and phototropins play rather limited roles.

Arabidopsis↗
PubMed2005

A brassinosteroid-hypersensitive mutant of BAK1 indicates that a convergence of photomorphogenic and hormonal signaling modulates phototropism.

The phototropic response of Arabidopsis (Arabidopsis thaliana) is induced by the phototropin photoreceptors and modulated by the cryptochrome and phytochrome photoreceptors. Downstream of these photoreceptors, asymmetric lateral redistribution of auxin underlies the differential growth, which results in phototropism. Historical physiological evidence and recent analysis of hormone-induced gene expression demonstrate that auxin and brassinosteroid signaling function interdependently. Similarly, in this study we report evidence that interactions between brassinosteroids and auxin signaling modulate phototropic responsiveness. We found that elongated, a previously identified photomorphogenesis mutant, enhances high-light phototropism and represents a unique allele of BAK1/SERK3, a receptor kinase implicated in brassinosteroid perception. Altogether, our results support the hypothesis that phototropic responsiveness is modulated by inputs that influence control of auxin response factor-mediated transcription.

Alleles↗
PubMed2006

Green light adjusts the plastid transcriptome during early photomorphogenic development.

During the transition from darkness to light, a suite of light sensors guides gene expression, biochemistry, and morphology to optimize acclimation to the new environment. Ultraviolet, blue, red, and far-red light all have demonstrated roles in modulating light responses, such as changes in gene expression and suppression of stem growth rate. However, green wavebands induce stem growth elongation, a response not likely mediated by known photosensors. In this study, etiolated Arabidopsis (Arabidopsis thaliana) seedlings were treated with a short, dim, single pulse of green light comparable in fluence and duration to that previously shown to excite robust stem elongation. Genome microarrays were then used to monitor coincident changes in gene expression. As anticipated, phytochrome A-regulated, nuclear-encoded transcripts were induced, confirming proper function of the sensitive phytochrome system. In addition, a suite of plastid-encoded transcripts decreased in abundance, including several typically up-regulated after phytochrome and/or cryptochrome activation. Further analyses using RNA gel-blot experiments demonstrated that the response is specific to green light, fluence dependent, and detectable within 30 min. The response obeys reciprocity and persists in the absence of known photosensors. Plastid transcript down-regulation was also observed in tobacco (Nicotiana tabacum) with similar temporal and fluence-response kinetics. Together, the down-regulation of plastid transcripts and increase in stem growth rate represent a mechanism that tempers progression of early commitment to the light environment, helping tailor seedling development during the critical process of establishment.

Arabidopsis↗
PubMed1998

Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis.

Many auxin responses are dependent on redistribution and/or polar transport of indoleacetic acid. Polar transport of auxin can be inhibited through the application of phytotropins such as 1-naphthylphthalamic acid (NPA). When Arabidopsis thaliana seedlings were grown in the light on medium containing 1.0 microM NPA, hypocotyl and root elongation and gravitropism were strongly inhibited. When grown in darkness, however, NPA disrupted the gravity response but did not affect elongation. The extent of inhibition of hypocotyl elongation by NPA increased in a fluence-rate-dependent manner to a maximum of about 75% inhibition at 50 mumol m-2 s-1 of white light. Plants grown under continuous blue or far-red light showed NPA-induced hypocotyl inhibition similar to that of white-light-grown plants. Plants grown under continuous red light showed less NPA-induced inhibition. Analysis of photoreceptor mutants indicates the involvement of phytochrome and cryptochrome in mediating this NPA response. Hypocotyls of some auxin-resistant mutants had decreased sensitivity to NPA in the light, but etiolated seedlings of these mutants were similar in length to the wild type. These results indicate that light has a significant effect on NPA-induced inhibition in Arabidopsis, and suggest that auxin has a more important role in elongation responses in light-grown than in dark-grown seedlings.

Arabidopsis↗
PubMed2001

Light-dependent osmoregulation in pea stem protoplasts. photoreceptors, tissue specificity, ion relationships, and physiological implications.

Light-induced changes in the volume of protoplasts bathed in a medium of constant osmolarity are useful indications of light-dependent cellular osmoregulation. With this in mind, we investigated the effect of light on the volume of protoplasts isolated from the elongating stems of pea (Pisum sativum) seedlings raised under red light. The protoplasts were isolated separately from epidermal peels and the remaining peeled stems. Under continuous red light, the protoplasts of peeled stems swelled steadily, but those of epidermal peels maintained a constant volume. Experiments employing far-red light and phytochrome-deficient mutants revealed that the observed swelling is a light-induced response mediated mainly by phytochromes A and B with a little greater contribution by phytochrome A. Protoplasts of epidermal peels and peeled stems shrank transiently in response to a pulse of blue light. The blue light responsiveness in this shrinking response, which itself is probably mediated by cryptochrome, is under the strict control of phytochromes A and B with equal contributions by these phytochromes. We suggest that the swelling response participates in the maintenance of high tissue tension of elongating stems and that the shrinking response is involved in stem growth inhibition. Other findings include the following: The swelling is caused by uptake of K+ and Cl-. The presence of Ca2+ in the bathing medium is required for phytochrome signaling in the swelling response, but not in the response establishing blue light responsiveness. Phytochrome A mediates the two responses in a totally red/far-red light reversible manner, as does phytochrome B.

Calcium↗
PubMed2001

Phytochrome A mediates blue light and UV-A-dependent chloroplast gene transcription in green leaves.

We characterized the photobiology of light-activated chloroplast transcription and transcript abundance in mature primary leaves by using the following two systems: transplastomic promoter-reporter gene fusions in tobacco (Nicotiana tabacum), and phytochrome (phyA, phyB, and hy2) and cryptochrome (cry1) mutants of Arabidopsis. In both dicots, blue light and UV-A radiation were the major signals that activated total chloroplast and psbA, rbcL, and 16S rrn transcription. In contrast, transcription activities in plants exposed to red and far-red light were 30% to 85% less than in blue light/UV-A, depending on the gene and plant species. Total chloroplast, psbA, and 16S rrn transcription were 60% to 80% less in the Arabidopsis phyA mutant exposed to blue light/UV-A relative to wild type, thus definitively linking phyA signaling to these photoresponses. To our knowledge, the major role of phyA in mediating the blue light/UV-A photoresponses is a new function for phyA in chloroplast biogenesis at this stage of leaf development. Although rbcL expression in plants exposed to UV-A was 50% less in the phyA mutant relative to wild type, blue light-induced rbcL expression was not significantly affected in the phyA, phyB, and cry1 mutants. However, rbcL expression in blue light was 60% less in the phytochrome chromophore mutant, hy2, relative to wild type, indicating that another phytochrome species (phyC, D, or E) was involved in blue light-induced rbcL transcription. Therefore, at least two different phytochromes, as well as phytochrome-independent photosensory pathways, mediated blue light/UV-A-induced transcription of chloroplast genes in mature leaves.

Arabidopsis↗