How fungi keep time: circadian system in Neurospora and other fungi

Current Opinion in Microbiology

Volumn 9, Issue 6, 2006, Pages 579-587

  Dunlap, Jay C ^a   Loros, Jennifer J ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

ASPERGILLUS FLAVUS; ASPERGILLUS NIDULANS; BASIDIOMYCETES; CIRCADIAN RHYTHM; FEEDBACK SYSTEM; FUNGAL STRAIN; GENETIC TRANSCRIPTION; MOLECULAR CLONING; MOLECULAR MODEL; NEUROSPORA; NONHUMAN; PHYLOGENY; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; ZYGOMYCETES;

BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; NEUROSPORA; TRANSCRIPTION FACTORS;

FUNGI; NEUROSPORA;

EID: 33751251331     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2006.10.008     Document Type: Review

References (91)

1. Dunlap J.C. Molecular biology of circadian pacemaker systems. In: Dunlap J.C., Loros J.J., and Decoursey P. (Eds). Chronobiology: Biological Timekeeping (2004), Sinauer Assoc 210-251
2. Tu B.P., Kudlicki A., Rowicka M., and McKnight S.L. Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310 (2005) 1152-1158
3. Jerebzoff S. Metabolic steps involved in periodicity. In: Hastings J.W., and Schweiger H.-G. (Eds). Dahlem Workshop on the Molecular Basis of Circadian Rhythms (1976), Dahlem Conferenzen 193-213
4. Bünning E. The Physiological Clock. edn 3 (1973), Springer-Verlag
5. Ingold C.T. Fungal Spores (1971), Clarendon Press, Oxford
6. Dunlap J.C., and Loros J.J. Analysis of circadian rhythms in Neurospora: overview of assays and genetic and molecular biological manipulation. Methods Enzymol 393 (2005) 3-22
7. Bell-Pedersen D, de Paula RM, Vitalini MV: The rhythms of life: circadian output pathways in Neurospora. J Biol Rhythms 2006, 21: in press.
8. McClung C.R., Fox B.A., and Dunlap J.C. The Neurospora clock gene frequency shares a sequence element with the Drosophila clock gene period. Nature 339 (1989) 558-562
9. Loros J.J., Denome S.A., and Dunlap J.C. Molecular cloning of genes under the control of the circadian clock in Neurospora. Science 243 (1989) 385-388
10. Heintzen C, Liu Y: The Neurospora circadian clock. Adv Genet 2006, in press.
11. Dunlap J.C., and Loros J.J. The Neurospora circadian system. J Biol Rhythms 19 (2004) 414-424
12. Dunlap J.C. Proteins in the Neurospora circadian clockwork. J Biol Chem 281 (2006) 28489-28493
13. Brunner M., and Schafmeier T. Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. Genes Dev 20 (2006) 1061-1074
14. Tan Y., Merrow M., and Roenneberg T. Photoperiodism in Neurospora crassa. J Biol Rhythms 19 (2004) 135-143
15. dePaula R.M., Lewis Z.A., Greene A.V., Seo K.S., Morgan L.W., Vitalini M.W., Bennett L., Gomer R.H., and Bell-Pedersen D. Two circadian timing circuits in Neurospora crassa share components and regulate distinct rhythmic processes. J Biol Rhythms 21 (2006) 159-168. Physiological and molecular evidence are presented for the existence of a novel timing circuit that might contribute to the circadian system. Although WC-1 and WC-2 are required for the oscillator, FRQ is not, and so this new circuit might be called the un-FRQ oscillator or UFO.
16. Froehlich A.C., Loros J.J., and Dunlap J.C. Rhythmic Binding of a WHITE COLLAR Containing Complex to the frequency Promoter is Inhibited by FREQUENCY. Proc Natl Acad Sci USA 100 (2003) 5914-5919
17. Kramer C., Loros J.J., Dunlap J.C., and Crosthwaite S.K. Role for antisense RNA in regulating circadian clock function in Neurospora crassa. Nature 421 (2003) 948-952
18. Froehlich A.C., Loros J.J., and Dunlap J.C. WHITE COLLAR-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297 (2002) 815-819
19. •].
20. •], the authors describe the complex environmentally influenced use of multiple promoters, alternative splicing and translational control that regulated FRQ expression.
21. Garceau N., Liu Y., Loros J.J., and Dunlap J.C. Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 89 (1997) 469-476
22. Liu Y., Garceau N., Loros J.J., and Dunlap J.C. Thermally regulated translational control mediates an aspect of temperature compensation in the Neurospora circadian clock. Cell 89 (1997) 477-486
23. Ruoff P., Loros J.J., and Dunlap J.C. The relationship between FRQ-protein stability and temperature compensation in the Neurospora circadian clock. Proc Natl Acad Sci USA 102 (2005) 17681-17686. A combined mathematical simulation and experimental study that convincingly models the temperature compensation process as the dynamic balance between the integrals of two opposing sets of processes.
24. Cheng P., Yang Y., Heintzen C., and Liu Y. Coiled coil mediated FRQ-FRQ interaction is essential for circadian clock function in Neurospora. EMBO J 20 (2001) 101-108
25. Cheng P., He Q., He Q., Wang L., and Liu Y. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev 19 (2005) 234-241. The authors purified native FRQ, identified the FRH helicase as an obligate stoichiometric interacting partner, and developed novel technology to probe the role of this essential protein in the clock.
26. Luo C., Loros J.J., and Dunlap J.C. Nuclear localization is required for function of the essential clock protein FREQUENCY. EMBO J 17 (1998) 1228-1235
27. LaCava J., Houseley J., Saveanu C., Petfalski E., Thompson E., Jacquier A., and Tollervey D. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121 (2005) 713-724
28. Cheng P., Yang Y., and Liu Y. Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc Natl Acad Sci USA 98 (2001) 7408-7413
29. Denault D.L., Loros J.J., and Dunlap J.C. WC-2 mediates WC-1-FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora crassa. EMBO J 20 (2001) 109-117
30. Merrow M., Franchi L., Dragovic Z., Gorl M., Johnson J., Brunner M., Macino G., and Roenneberg T. Circadian regulation of the light input pathway in Neurospora crassa. EMBO J 20 (2001) 307-315
31. Schafmeier T., Haase A., Kaldi K., Scholz J., Fuchs M., and Brunner M. Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 122 (2005) 235-246. With data suggesting that FRQ does not form a stoichiometric partnership with the WCC, the authors show that FRQ influences the phosphorylation of WC-2, thereby decreasing its ability to co-activate transcription. This casts details of the FRQ-WCC negative feedback loop in a new light.
32. ••], playing an important role in the circadian negative feedback loop.
33. He Q., Shu H., Cheng P., Chen S., Wang L., and Liu Y. Light-independent phosphorylation of WHITE COLLAR-1 regulates its function in the Neurospora circadian negative feedback loop. J Biol Chem 280 (2005) 17526-17532. The authors provide the first evidence of regulation of WCC function by phosphorylation and identify several of the residues in WC-1 that mediate this effect.
34. Lee K., Loros J.J., and Dunlap J.C. Interconnected feedback loops in the Neurospora circadian system. Science 289 (2000) 107-110
35. Gorl M., Merrow M., Huttner B., Johnson J., Roenneberg T., and Brunner M. A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa. EMBO J 20 (2001) 7074-7084
36. Liu Y., Loros J., and Dunlap J.C. Phosphorylation of the Neurospora clock protein FREQUENCY determines its degradation rate and strongly influences the period length of the circadian clock. Proc Natl Acad Sci USA 97 (2000) 234-239
37. Yang Y., Cheng P., and Liu Y. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev 16 (2002) 994-1006
38. Yang Y., Cheng P., Qiyang Q., He Q., Wang L., and Liu Y. Phosphorylation of FREQUENCY protein by casein kinase II is necessary for the function of the Neurospora circadian clock. Mol Cell Biol 23 (2003) 6221-6228
39. Yang Y., Cheng P., Zhi G., and Liu Y. Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J Biol Chem 276 (2001) 41064-41072
40. Pregueiro A., Liu Q., Baker C., Dunlap J.C., and Loros J.J. The Neurospora checkpoint kinase 2: a regulatory link between the circadian and cell cycles. Science 313 (2006) 644-649. Cloning of a novel clock gene, prd-4, showed it to encode the universal cell cycle regulator CHK2. Showing that DNA damage resets the clock in a PRD-4-dependent manner, and that the clock regulates PRD-4, revealed a new feedback loop conditionally connecting clock output to input and to the cell cycle. This helps to explain the role of clock genes regulation in mammalian tumorigenesis.
41. He Q., Cheng P., Yang Y., He Q., Yu Q., and Liu Y. FWD-1 mediated degradation of FREQUENCY in Neurospora establishes a conserved mechanism for circadian clock regulation. EMBO J 22 (2003) 4421-4430
42. He Q., Cheng P., He Q., and Liu Y. The COP9 signalosome regulates the Neurospora circadian clock by controlling the stability of the SCFFWD-1 complex. Genes Dev 19 (2005) 1518-1531. A nice study showing how small alterations in the cellular protein degradation machinery can impact the circadian machinery and even generate a non-circadian oscillation. Independently, a potentially important paper in explaining the COP9 signalosome paradox.
43. Aronson B., Johnson K., Loros J.J., and Dunlap J.C. Negative feedback defining a circadian clock: autoregulation in the clock gene frequency. Science 263 (1994) 1578-1584
44. Crosthwaite S.C., Loros J.J., and Dunlap J.C. Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81 (1995) 1003-1012
45. ••], perhaps not the only explanation.
46. Kaldi K., Gonzalez B.H., and Brunner M. Transcriptional regulation of the Neurospora circadian clock gene wc-1 affects the phase of circadian output. EMBO Rep 7 (2006) 199-204
47. Cheng P., Yang Y., Wang L., He Q., and Liu Y. WHITE COLLAR-1, a multifunctional Neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2. J Biol Chem 278 (2003) 3801-3808
48. Liu Y. Molecular mechanisms of entrainment in the Neurospora circadian clock. J Biol Rhythms 18 (2003) 195-205
49. Merrow M., Boesl C., Ricken J., Messerschmitt M., Goedel M., and Roenneberg T. Entrainment of the Neurospora circadian clock. Chronobiol Int 23 (2006) 71-80
50. Price-Lloyd N., Elvin M., and Heintzen C. Synchronizing the Neurospora crassa circadian clock with the rhythmic environment. Biochem Soc Trans 33 (2005) 949-952
51. Liu Y., Merrow M., Loros J.J., and Dunlap J.C. How temperature changes reset a circadian oscillator. Science 281 (1998) 825-829
52. He Q., Cheng P., Yang Y., Wang L., Gardner K., and Liu Y. WHITE COLLAR-1, a DNA binding transcription factor and a light sensor. Science 297 (2002) 840-842
53. Heintzen C., Loros J.J., and Dunlap J.C. VIVID, gating and the circadian clock: the PAS protein VVD defines a feedback loop that represses light input pathways and regulates clock resetting. Cell 104 (2001) 453-464
54. Elvin M., Loros J.J., Dunlap J.C., and Heintzen C. The PAS/LOV protein VIVID supports a rapidly dampened daytime oscillator that facilitates entrainment of the Neurospora circadian clock. Genes Dev 19 (2005) 2593-2605. A carefully executed and data-rich paper describing how a novel daytime oscillator influenced by the VVD protein acts to keep the clock running during the day and to enable the clock to reset at dusk.
55. Merrow M., Garceau N., and Dunlap J.C. Dissection of a circadian oscillation into discrete domains. Proc Natl Acad Sci USA 94 (1997) 3877-3882
56. Gonze D., Leloup J.C., and Goldbeter A. Theoretical models for circadian rhythms in Neurospora and Drosophila. C R Acad Sci III 323 (2000) 57-67
57. Gonze D., Halloy J., and Goldbeter A. Robustness of circadian rhythms with respect to molecular noise. Proc Natl Acad Sci USA 99 (2002) 673-678
58. Francois P. A model for the Neurospora circadian clock. Biophys J 88 (2005) 2369-2383
59. Kurosawa G., and Goldbeter A. Amplitude of circadian oscillations entrained by 24-h light-dark cycles. J Theor Biol 242 (2006) 478-488
60. Smolen P., Baxter D.A., and Byrne J.H. Reduced models of the circadian oscillators in Neurospora crassa and Drosophila melanogaster illustrate mechanistic similarities. OMICS 7 (2003) 337-354
61. Ruoff P., Vinsjevik M., Mohsenzadeh S., and Rensing L. The Goodwin Model: simulating the effect of cycloheximide and heat shock on the sporulation rhythm of Neurospora crassa. J Theor Biol 196 (1999) 483-494
62. Ruoff P., Vinsjevik M., Mohsenzadeh S., and Rensing L. The Goodwin Oscillator: on the importance of degradation reaction in the circadian clock. J Biol Rhythms 14 (1999) 469-479
63. Iwasaki H., and Dunlap J.C. Microbial circadian oscillatory systems in Neurospora and Synechococcus: models for cellular clocks. Curr Opin Microbiol 3 (2000) 189-196
64. •].
65. •].
66. •], are three studies aimed at understanding how temperature cycles influence FLOs, and what, if any, role FLOs might have in the circadian system.
67. Loros J.J., and Dunlap J.C. Genetic and molecular analysis of circadian rhythms in Neurospora. Annu Rev Physiol 63 (2001) 757-794
68. Correa A., Lewis Z.A., Greene A.V., March I.J., Gomer R.H., and Bell-Pedersen D. Multiple oscillators regulate circadian gene expression in Neurospora. Proc Natl Acad Sci USA 100 (2003) 13597-13602
69. Dunlap J.C. Molecular bases for circadian clocks. Cell 96 (1999) 271-290
70. Tauber E., Last K.S., and Olive P.J. Kyriacou CP-: clock gene evolution and functional divergence. J Biol Rhythms 19 (2004) 445-458
71. Dunlap J.C., and Feldman J.F. On the role of protein synthesis in the circadian clock of Neurospora crassa. Proc Natl Acad Sci USA 85 (1988) 1096-1100
72. Bell-Pedersen D., Cassone V.M., Earnest D.J., Golden S.S., Hardin P.E., Thomas T.L., and Zoran M.J. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6 (2005) 544-556
73. Lakin-Thomas P.L. New models for circadian systems in microorganisms. FEMS Microbiol Lett 259 (2006) 1-6
74. Edmunds Jr. L.N. Cellular and Molecular Bases of Biological Clocks (1988), Springer-Verlag
75. Uebelmesser E.R. The endogenous daily rhythm of conidiospore formation of Pilobolus. Arch Mikrobiol 20 (1954) 1-33
76. Greene A.V., Keller N., Haas H., and Bell-Pedersen D. A circadian oscillator in Aspergillus spp. regulates daily development and gene expression. Eukaryot Cell 2 (2003) 231-237
77. Merrow M., and Dunlap J.C. Intergeneric complementation of a circadian rhythmicity defect: phylogenetic conservation of the 989 amino acid open reading frame in the clock gene frequency. EMBO J 13 (1994) 2257-2266
78. Lombardi L.M., and Brody S. Circadian rhythms in Neurospora crassa: clock gene homologues in fungi. Fungal Genet Biol 42 (2005) 887-892
79. Lewis M., Morgan L., and Feldman J.F. Cloning of (frq) clock gene homologs from the Neurospora sitophila and Neurospora tetrasperma, Chromocrea spinulosa and Leptosphaeria australiensis. Mol Gen Genet 253 (1997) 401-414
80. Lewis M., and Feldman J.F. Evolution of the frequency clock locus in ascomycete fungi. Mol Biol Evol 13 (1997) 1233-1241
81. Froehlich A.C., Noh B., Vierstra R.D., Loros J., and Dunlap J.C. Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot Cell 4 (2005) 2140-2152
82. Blumenstein A., Vienken K., Tasler R., Purschwitz J., Veith D., Frankenberg-Dinkel N., and Fischer R. The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15 (2005) 1833-1838. This is the first description of an activity for a fungal phytochrome; a nicely crafted and satisfying study.
83. •].
84. Casas-Flores S., Rios-Momberg M., Bibbins M., Ponce-Noyola P., and Herrera-Estrella A. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiol 150 (2004) 3561-3569
85. •].
86. •].
87. •].
88. •].
89. •] comprise a sudden wave of research describing the conserved role of WC-1-like proteins in photoreception amongst the fungi. Because WC-1 also has a non-light-associated function in the Neurospora circadian system in both the FRQ-WCC oscillator, and potentially in the UFO, this conservation raises the possibility of a similarly conserved role in fungal circadian systems.
90. Christensen M., Falkeid G., Hauge I., Loros J.J., Dunlap J.C., Lillo C., and Ruoff P. A frq-independent nitrate reductase rhythm in Neurospora crassa. J Biol Rhythms 19 (2004) 280-286
91. He Q., Cha J., He Q., Lee H., Yang Y., and Liu Y. CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop. Genes Dev 20 (2006) 2552-2565. Casein kinase 1 and casein kinase 2 are identified as kinases that phosphorylate WC-1 and WC-2 in a FRQ-dependent manner to reduce the activity of the WCC.