-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Role for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis
The circadian clock consists of an extensive genetic network that drives daily rhythms of physiological, biochemical and behavioural processes. The network is evolutionary conserved and has been extensively studied in a broad range of organisms. Another genetic network constitutes the photoperiodic clock and monitors the seasonal change in day-length. Here, we address a major and long-standing question in chronobiology: whether the circadian clock is involved in photoperiodic timing, also known as the Bünning hypothesis. Drosophila, as with many other insects in temperate regions, exhibits a photoperiodic response that allows the insect to anticipate and survive the winter. Here we show that the cold-tolerance of the fly is regulated by the photoperiod. We use this phenotype to test day-length timing in various circadian clock mutants and observe that in null clock mutants, the photoperiodic response is abolished, whereas in mutants that exhibit short or long daily cycles, the photoperiodic response is modified, further supporting a circadian-clock function. Overall, these results provide the first evidence in Drosophila that support for the Bünning hypothesis, and pave the way for the genetic dissection of seasonal timing in Drosophila melanogaster.
Vyšlo v časopise: Role for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004603
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004603Souhrn
The circadian clock consists of an extensive genetic network that drives daily rhythms of physiological, biochemical and behavioural processes. The network is evolutionary conserved and has been extensively studied in a broad range of organisms. Another genetic network constitutes the photoperiodic clock and monitors the seasonal change in day-length. Here, we address a major and long-standing question in chronobiology: whether the circadian clock is involved in photoperiodic timing, also known as the Bünning hypothesis. Drosophila, as with many other insects in temperate regions, exhibits a photoperiodic response that allows the insect to anticipate and survive the winter. Here we show that the cold-tolerance of the fly is regulated by the photoperiod. We use this phenotype to test day-length timing in various circadian clock mutants and observe that in null clock mutants, the photoperiodic response is abolished, whereas in mutants that exhibit short or long daily cycles, the photoperiodic response is modified, further supporting a circadian-clock function. Overall, these results provide the first evidence in Drosophila that support for the Bünning hypothesis, and pave the way for the genetic dissection of seasonal timing in Drosophila melanogaster.
Zdroje
1. BradshawWE, HolzapfelCM (2010) Light, time, and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol 72 : 147–166.
2. SaundersDS, LewisRD, WarmanGR (2004) Photoperiodic induction of diapause: Opening the black box. Physiol Entomol 29(1): 1–15.
3. SawaM, NusinowDA, KaySA, ImaizumiT (2007) FKF1 and GIGANTEA complex is required for day-length measurement in Arabidopsis. Science 318 : 261–265.
4. SawaM, KaySA, ImaizumiT (2008) Photoperiodic flowering occurs under internal and external coincidence. Plant Signal Behav 3 : 269–271.
5. DardenteH, WyseC, BirnieM, DupréS, LoudonA, et al. (2010) A molecular switch for photoperiod responsiveness in mammals. Curr Biol 20 : 2193–2198.
6. HogeneschJB, UedaHR (2011) Understanding systems-level properties: Timely stories from the study of clocks. Nat Rev Genet 12 (6) 407–416.
7. BünningE (1936) Die endonome tagesrhythmik als grundlage der photoperiodischen reaktion. Ber Dtsch Bot Ges 54 : 590–607.
8. PittendrighCS, MinisDH (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am Naturalist 98 : 261–294.
9. TauberE, KyriacouBP (2001) Insect photoperiodism and circadian clocks: Models and mechanisms. J Biol Rhythms 16 (4) 381–90.
10. BradshawWE, HolzapfelCM (2010) What season is it anyway? circadian tracking vs. photoperiodic anticipation in insects. J Biol Rhythms 25 (3) 155–165.
11. HardinPE (2005) The circadian timekeeping system of drosophila. Curr Biol 15 (17) R714–22.
12. SaundersDS, HenrichVC, GilbertLI (1989) Induction of diapause in Drosophila melanogaster - photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc Natl Acad Sci U S A 86 (10) 3748–3752.
13. SaundersDS (1990) The circadian basis of ovarian diapause regulation in Drosophila melanogaster - is the period gene causally involved in photoperiodic time measurement. J Biol Rhythms 5 (4) 315–331.
14. TauberE, ZordanM, SandrelliF, PegoraroM, OsterwalderN, et al. (2007) Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316 (5833) 1895–8.
15. SandrelliF, TauberE, PegoraroM, MazzottaG, CisottoP, et al. (2007) A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 316 (5833) 1898–1900.
16. PavelkaJ, ShimadaK, KostalV (2003) TIMELESS: A link between fly's circadian and photoperiodic clocks? Eur J Entomol 100 (2) 255–265.
17. IkenoT, TanakaSI, NumataH, GotoSG (2010) Photoperiodic diapause under the control of circadian clock genes in an insect. BMC Biol 8 : 116.
18. YamadaH, YamamotoMT (2011) Association between circadian clock genes and diapause incidence in Drosophila triauraria. PLoS One 6 (12) e27493.
19. BradshawWE, HolzapfelCM (2010) Circadian clock genes, ovarian development and diapause. BMC Biol 8 : 115.
20. Jean DavidR, GibertP, PlaE, PetavyG, KaranD, et al. (1998) Cold stress tolerance in Drosophila: Analysis of chill coma recovery in D. melanogaster. J Therm Biol 23 (5) 291–299.
21. LancianiCA, LippKE, GieselJT (1992) The effect of photoperiod on cold tolerance in Drosophila melanogaster. J Therm Biol 17 (3) 147–148.
22. RutilaJE, SuriV, LeM, SoWV, RosbashM, et al. (1998) CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93 (5) 805–814.
23. PriceJL, BlauJ, RothenfluhA, AbodeelyM, KlossB, et al. (1998) Double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94 (1) 83–95.
24. RothenfluhA, YoungMW, SaezL (2000) A TIMELESS-independent function for PERIOD proteins in the Drosophila clock. Neuron 26 (2) 505–514.
25. MajercakJ, SidoteD, HardinPE, EderyI (1999) How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24 (1) 219–30.
26. MajercakJ, ChenWF, EderyI (2004) Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol 24 (8) 3359–3372.
27. CollinsBH, RosatoE, KyriacouCP (2004) Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci U S A 101 (7) 1945–50.
28. ChengY, GvakhariaB, HardinPE (1998) Two alternatively spliced transcripts from the Drosophila period gene rescue rhythms having different molecular and behavioral characteristics. Mol Cell Biol 18 (11) 6505–6514.
29. MacmillanHA, SinclairBJ (2011) Mechanisms underlying insect chill-coma. J Insect Physiol 57 (1) 12–20.
30. VesalaL, HoikkalaA (2011) Effects of photoperiodically induced reproductive diapause and cold hardening on the cold tolerance of Drosophila montana. J Insect Physiol 57 (1) 46–51.
31. VesalaL, SalminenTS, KankareM, HoikkalaA (2012) Photoperiodic regulation of cold tolerance and expression levels of regucalcin gene in Drosophila montana. J Insect Physiol 58 : 704–709.
32. EngelmannW, MackJ (1978) Different oscillators control the circadian rhythm of eclosion and activity in Drosophila. Journal of Comparative Physiology 127 (3) 229–237.
33. SheebaV, ChandrashekaranMK, JoshiA, Kumar SharmaV (2001) A case for multiple oscillators controlling different circadian rhythms in Drosophila melanogaster. J Insect Physiol 47 (10) 1217–1225.
34. Helfrich-ForsterC (2001) The locomotor activity rhythm of Drosophila melanogaster is controlled by a dual oscillator system. J Insect Physiol 47 (8) 877–887.
35. VaninS, BhutaniS, MontelliS, MenegazziP, GreenEW, et al. (2012) Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 484 (7394) 371–375.
36. BywalezW, MenegazziP, RiegerD, SchmidB, Helfrich-ForsterC, et al. (2012) The dual-oscillator system of Drosophila melanogaster under natural-like temperature cycles. Chronobiol Int 29 (4) 395–407.
37. WulbeckC, SzaboG, ShaferOT, Helfrich-ForsterC, StanewskyR (2005) The novel Drosophila tim(blind) mutation affects behavioral rhythms but not periodic eclosion. Genetics 169 (2) 751–766.
38. MenegazziP, VaninS, YoshiiT, RiegerD, HermannC, et al. (2013) Drosophila clock neurons under natural conditions. J Biol Rhythms 28 (1) 3–14.
39. PittendrighCS, MinisDH (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Amer Nat 98 : 261–294.
40. EmersonKJ, BradshawWE, HolzapfelCM (2009) Complications of complexity: Integrating environmental, genetic and hormonal control of insect diapause. Trends Genet 25 (5) 217–225.
41. OvergaardJ, SorensenJG, PetersenSO, LoeschckeV, HolmstrupM (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 51 (11) 1173–1182.
42. GotoSG, UdakaH, UedaC, KatagiriC (2010) Fatty acids of membrane phospholipids in Drosophila melanogaster lines showing rapid and slow recovery from chill coma. Biochem Biophys Res Commun 391 (2) 1251–1254.
43. MichaudMR, DenlingerDL (2007) Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): A metabolomic comparison. J Comp Physiol B 177 (7) 753–763.
44. CzajkaMC, LeeREJr (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. J Exp Biol 148 : 245–254.
45. ShreveSM, KeltyJD, LeeRE (2004) Jr (2004) Preservation of reproductive behaviors during modest cooling: Rapid cold-hardening fine-tunes organismal response. J Exp Biol 207 (Pt 11) 1797–1802.
46. SchiesariL, KyriacouCP, CostaR (2011) The hormonal and circadian basis for insect photoperiodic timing. FEBS Lett 585 (10) 1450–1460.
47. Gesto J. (2010) Circadian clock genes and seasonal behaviour. PhD thesis (University of Leicester, Leicester, UK).
48. RothenfluhA, AbodeelyM, PriceJL, YoungMW (2000) Isolation and analysis of six timeless alleles that cause short - or long-period circadian rhythms in Drosophila. Genetics 156 (2) 665–75.
49. R Development Core Team. (2010) R: A language and environment for statistical computing, 2.10.1.
50. HarringtonDP, FlemingTR (1982) A class of rank test procedures for censored survival data. Biometrika 69 (3) 553–566.
51. QuadeD (1967) Rank analysis of covariance. Journal of the American Statistical Association 62 : 1187–1200.
52. NelsonW, TongYL, LeeJK, HalbergF (1979) Methods for cosinor-rhythmometry. Chronobiologia 6 (4) 305–323.
Štítky
Genetika Reprodukčná medicína
Článek An Evolutionarily Conserved Role for the Aryl Hydrocarbon Receptor in the Regulation of MovementČlánek Requirement for Drosophila SNMP1 for Rapid Activation and Termination of Pheromone-Induced ActivityČlánek Co-regulated Transcripts Associated to Cooperating eSNPs Define Bi-fan Motifs in Human Gene NetworksČlánek Identification of a Regulatory Variant That Binds FOXA1 and FOXA2 at the Type 2 Diabetes GWAS LocusČlánek tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa CellsČlánek Derlin-1 Regulates Mutant VCP-Linked Pathogenesis and Endoplasmic Reticulum Stress-Induced ApoptosisČlánek A Genetic Assay for Transcription Errors Reveals Multilayer Control of RNA Polymerase II FidelityČlánek The Proprotein Convertase KPC-1/Furin Controls Branching and Self-avoidance of Sensory Dendrites inČlánek Regulation of p53 and Rb Links the Alternative NF-κB Pathway to EZH2 Expression and Cell SenescenceČlánek BMPs Regulate Gene Expression in the Dorsal Neuroectoderm of and Vertebrates by Distinct MechanismsČlánek Unkempt Is Negatively Regulated by mTOR and Uncouples Neuronal Differentiation from Growth Control
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2014 Číslo 9- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- Translational Regulation of the Post-Translational Circadian Mechanism
- An Evolutionarily Conserved Role for the Aryl Hydrocarbon Receptor in the Regulation of Movement
- Eliminating Both Canonical and Short-Patch Mismatch Repair in Suggests a New Meiotic Recombination Model
- Requirement for Drosophila SNMP1 for Rapid Activation and Termination of Pheromone-Induced Activity
- Co-regulated Transcripts Associated to Cooperating eSNPs Define Bi-fan Motifs in Human Gene Networks
- Targeted H3R26 Deimination Specifically Facilitates Estrogen Receptor Binding by Modifying Nucleosome Structure
- Role for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis
- The Tandem Repeats Enabling Reversible Switching between the Two Phases of β-Lactamase Substrate Spectrum
- The Association of the Vanin-1 N131S Variant with Blood Pressure Is Mediated by Endoplasmic Reticulum-Associated Degradation and Loss of Function
- Identification of a Regulatory Variant That Binds FOXA1 and FOXA2 at the Type 2 Diabetes GWAS Locus
- Regulation of Flowering by the Histone Mark Readers MRG1/2 via Interaction with CONSTANS to Modulate Expression
- The Actomyosin Machinery Is Required for Retinal Lumen Formation
- Plays a Conserved Role in Assembly of the Ciliary Motile Apparatus
- Hidden Diversity in Honey Bee Gut Symbionts Detected by Single-Cell Genomics
- Ribosome Rescue and Translation Termination at Non-Standard Stop Codons by ICT1 in Mammalian Mitochondria
- tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa Cells
- Causal Variation in Yeast Sporulation Tends to Reside in a Pathway Bottleneck
- Tissue-Specific RNA Expression Marks Distant-Acting Developmental Enhancers
- WC-1 Recruits SWI/SNF to Remodel and Initiate a Circadian Cycle
- Clonal Expansion of Early to Mid-Life Mitochondrial DNA Point Mutations Drives Mitochondrial Dysfunction during Human Ageing
- Methylation QTLs Are Associated with Coordinated Changes in Transcription Factor Binding, Histone Modifications, and Gene Expression Levels
- Differential Management of the Replication Terminus Regions of the Two Chromosomes during Cell Division
- Obesity-Linked Homologues and Establish Meal Frequency in
- Derlin-1 Regulates Mutant VCP-Linked Pathogenesis and Endoplasmic Reticulum Stress-Induced Apoptosis
- Stress-Induced Nuclear RNA Degradation Pathways Regulate Yeast Bromodomain Factor 2 to Promote Cell Survival
- The MAPK p38c Regulates Oxidative Stress and Lipid Homeostasis in the Intestine
- Widespread Genome Reorganization of an Obligate Virus Mutualist
- Trans-kingdom Cross-Talk: Small RNAs on the Move
- The Vip1 Inositol Polyphosphate Kinase Family Regulates Polarized Growth and Modulates the Microtubule Cytoskeleton in Fungi
- Myosin Vb Mediated Plasma Membrane Homeostasis Regulates Peridermal Cell Size and Maintains Tissue Homeostasis in the Zebrafish Epidermis
- GLD-4-Mediated Translational Activation Regulates the Size of the Proliferative Germ Cell Pool in the Adult Germ Line
- Genome Wide Association Studies Using a New Nonparametric Model Reveal the Genetic Architecture of 17 Agronomic Traits in an Enlarged Maize Association Panel
- Translational Regulation of the DOUBLETIME/CKIδ/ε Kinase by LARK Contributes to Circadian Period Modulation
- Positive Selection and Multiple Losses of the LINE-1-Derived Gene in Mammals Suggest a Dual Role in Genome Defense and Pluripotency
- Out of Balance: R-loops in Human Disease
- A Genetic Assay for Transcription Errors Reveals Multilayer Control of RNA Polymerase II Fidelity
- Altered Behavioral Performance and Live Imaging of Circuit-Specific Neural Deficiencies in a Zebrafish Model for Psychomotor Retardation
- Nipbl and Mediator Cooperatively Regulate Gene Expression to Control Limb Development
- Meta-analysis of Mutations in Autism Spectrum Disorders: A Gradient of Severity in Cognitive Impairments
- The Proprotein Convertase KPC-1/Furin Controls Branching and Self-avoidance of Sensory Dendrites in
- Hydroxymethylated Cytosines Are Associated with Elevated C to G Transversion Rates
- Memory and Fitness Optimization of Bacteria under Fluctuating Environments
- Regulation of p53 and Rb Links the Alternative NF-κB Pathway to EZH2 Expression and Cell Senescence
- Interspecific Tests of Allelism Reveal the Evolutionary Timing and Pattern of Accumulation of Reproductive Isolation Mutations
- PRO40 Is a Scaffold Protein of the Cell Wall Integrity Pathway, Linking the MAP Kinase Module to the Upstream Activator Protein Kinase C
- Low Levels of p53 Protein and Chromatin Silencing of p53 Target Genes Repress Apoptosis in Endocycling Cells
- SPDEF Inhibits Prostate Carcinogenesis by Disrupting a Positive Feedback Loop in Regulation of the Foxm1 Oncogene
- RRP6L1 and RRP6L2 Function in Silencing Regulation of Antisense RNA Synthesis
- BMPs Regulate Gene Expression in the Dorsal Neuroectoderm of and Vertebrates by Distinct Mechanisms
- Unkempt Is Negatively Regulated by mTOR and Uncouples Neuronal Differentiation from Growth Control
- Atkinesin-13A Modulates Cell-Wall Synthesis and Cell Expansion in via the THESEUS1 Pathway
- Dopamine Signaling Leads to Loss of Polycomb Repression and Aberrant Gene Activation in Experimental Parkinsonism
- Histone Methyltransferase MMSET/NSD2 Alters EZH2 Binding and Reprograms the Myeloma Epigenome through Global and Focal Changes in H3K36 and H3K27 Methylation
- Bipartite Recognition of DNA by TCF/Pangolin Is Remarkably Flexible and Contributes to Transcriptional Responsiveness and Tissue Specificity of Wingless Signaling
- The Olfactory Transcriptomes of Mice
- Muscular Dystrophy-Associated and Variants Disrupt Nuclear-Cytoskeletal Connections and Myonuclear Organization
- Interplay of dFOXO and Two ETS-Family Transcription Factors Determines Lifespan in
- Evidence for Widespread Positive and Negative Selection in Coding and Conserved Noncoding Regions of
- Genome-Wide Association Meta-analysis of Neuropathologic Features of Alzheimer's Disease and Related Dementias
- Rejuvenation of Meiotic Cohesion in Oocytes during Prophase I Is Required for Chiasma Maintenance and Accurate Chromosome Segregation
- Admixture in Latin America: Geographic Structure, Phenotypic Diversity and Self-Perception of Ancestry Based on 7,342 Individuals
- Local Effect of Enhancer of Zeste-Like Reveals Cooperation of Epigenetic and -Acting Determinants for Zygotic Genome Rearrangements
- Differential Responses to Wnt and PCP Disruption Predict Expression and Developmental Function of Conserved and Novel Genes in a Cnidarian
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Admixture in Latin America: Geographic Structure, Phenotypic Diversity and Self-Perception of Ancestry Based on 7,342 Individuals
- Nipbl and Mediator Cooperatively Regulate Gene Expression to Control Limb Development
- Genome Wide Association Studies Using a New Nonparametric Model Reveal the Genetic Architecture of 17 Agronomic Traits in an Enlarged Maize Association Panel
- Histone Methyltransferase MMSET/NSD2 Alters EZH2 Binding and Reprograms the Myeloma Epigenome through Global and Focal Changes in H3K36 and H3K27 Methylation
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy