REVEILLE8 and PSEUDO-REPONSE REGULATOR5 Form a Negative Feedback Loop within the Arabidopsis Circadian Clock
Circadian rhythms provide organisms with an adaptive advantage, allowing them to regulate physiological and developmental events so that they occur at the most appropriate time of day. In plants, as in other eukaryotes, multiple transcriptional feedback loops are central to clock function. In one such feedback loop, the Myb-like transcription factors CCA1 and LHY directly repress expression of the pseudoresponse regulator TOC1 by binding to an evening element (EE) in the TOC1 promoter. Another key regulatory circuit involves CCA1 and LHY and the TOC1 homologs PRR5, PRR7, and PRR9. Purification of EE–binding proteins from plant extracts followed by mass spectrometry led to the identification of RVE8, a homolog of CCA1 and LHY. Similar to these well-known clock genes, expression of RVE8 is circadian-regulated with a dawn phase of expression, and RVE8 binds specifically to the EE. However, whereas cca1 and lhy mutants have short period phenotypes and overexpression of either gene causes arrhythmia, rve8 mutants have long-period and RVE8-OX plants have short-period phenotypes. Light input to the clock is normal in rve8, but temperature compensation (a hallmark of circadian rhythms) is perturbed. RVE8 binds to the promoters of both TOC1 and PRR5 in the subjective afternoon, but surprisingly only PRR5 expression is perturbed by overexpression of RVE8. Together, our data indicate that RVE8 promotes expression of a subset of EE–containing clock genes towards the end of the subjective day and forms a negative feedback loop with PRR5. Thus RVE8 and its homologs CCA1 and LHY function close to the circadian oscillator but act via distinct molecular mechanisms.
Vyšlo v časopise:
REVEILLE8 and PSEUDO-REPONSE REGULATOR5 Form a Negative Feedback Loop within the Arabidopsis Circadian Clock. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001350
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001350
Souhrn
Circadian rhythms provide organisms with an adaptive advantage, allowing them to regulate physiological and developmental events so that they occur at the most appropriate time of day. In plants, as in other eukaryotes, multiple transcriptional feedback loops are central to clock function. In one such feedback loop, the Myb-like transcription factors CCA1 and LHY directly repress expression of the pseudoresponse regulator TOC1 by binding to an evening element (EE) in the TOC1 promoter. Another key regulatory circuit involves CCA1 and LHY and the TOC1 homologs PRR5, PRR7, and PRR9. Purification of EE–binding proteins from plant extracts followed by mass spectrometry led to the identification of RVE8, a homolog of CCA1 and LHY. Similar to these well-known clock genes, expression of RVE8 is circadian-regulated with a dawn phase of expression, and RVE8 binds specifically to the EE. However, whereas cca1 and lhy mutants have short period phenotypes and overexpression of either gene causes arrhythmia, rve8 mutants have long-period and RVE8-OX plants have short-period phenotypes. Light input to the clock is normal in rve8, but temperature compensation (a hallmark of circadian rhythms) is perturbed. RVE8 binds to the promoters of both TOC1 and PRR5 in the subjective afternoon, but surprisingly only PRR5 expression is perturbed by overexpression of RVE8. Together, our data indicate that RVE8 promotes expression of a subset of EE–containing clock genes towards the end of the subjective day and forms a negative feedback loop with PRR5. Thus RVE8 and its homologs CCA1 and LHY function close to the circadian oscillator but act via distinct molecular mechanisms.
Zdroje
1. HarmerSL
2009 The circadian system in higher plants. Annu Rev Plant Biol 60 357 377
2. AlladaR
ChungBY
2010 Circadian organization of behavior and physiology in Drosophila. Annu Rev Physiol 72 605 624
3. MichaelTP
McClungCR
2003 Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis. Plant Physiol 132 629 639
4. CovingtonMF
MaloofJN
StraumeM
KaySA
HarmerSL
2008 Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9
5. PandaS
AntochMP
MillerBH
SuAI
SchookAB
2002 Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109 307 320
6. AkhtarRA
ReddyAB
MaywoodES
ClaytonJD
KingVM
2002 Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12 540 550
7. WelshDK
YooSH
LiuAC
TakahashiJS
KaySA
2004 Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr Biol 14 2289 2295
8. NagoshiE
SainiC
BauerC
LarocheT
NaefF
2004 Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 119 693 705
9. MihalcescuI
HsingW
LeiblerS
2004 Resilient circadian oscillator revealed in individual cyanobacteria. Nature 430 81 85
10. DunlapJC
LorosJJ
ColotHV
MehraA
BeldenWJ
2007 A circadian clock in Neurospora: how genes and proteins cooperate to produce a sustained, entrainable, and compensated biological oscillator with a period of about a day. Cold Spring Harb Symp Quant Biol 72 57 68
11. JohnsonCH
MoriT
XuY
2008 A cyanobacterial circadian clockwork. Curr Biol 18 R816 R825
12. MehraA
BakerCL
LorosJJ
DunlapJC
2009 Post-translational modifications in circadian rhythms. Trends Biochem Sci 34 483 490
13. AlabadiD
OyamaT
YanovskyMJ
HarmonFG
MasP
2001 Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293 880 883
14. Pruneda-PazJL
BretonG
ParaA
KaySA
2009 A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323 1481 1485
15. NakamichiN
KitaM
ItoS
YamashinoT
MizunoT
2005 Pseudo-Response Regulators, PRR9, PRR7, and PRR5, Play Together Essential Roles Close to the Circadian Clock of Arabidopsis thaliana. Plant Cell Physiol
16. FarreEM
HarmerSL
HarmonFG
YanovskyMJ
KaySA
2005 Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr Biol 15 47 54
17. NakamichiN
KibaT
HenriquesR
MizunoT
ChuaNH
2010 PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22 594 605
18. LockeJC
SouthernMM
Kozma-BognarL
HibberdV
BrownPE
2005 Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1 0013
19. MasP
KimWY
SomersDE
KaySA
2003 Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426 567 570
20. KimWY
FujiwaraS
SuhSS
KimJ
KimY
2007 ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449 356 360
21. FujiwaraS
WangL
HanL
SuhSS
SalomePA
2008 Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo- response regulator proteins. J Biol Chem
22. DanielX
SuganoS
TobinEM
2004 CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis. Proc Natl Acad Sci U S A 101 3292 3297
23. WangL
FujiwaraS
SomersDE
2010 PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock. EMBO J 29 1903 1915
24. HarmerSL
HogeneschJB
StraumeM
ChangHS
HanB
2000 Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290 2110 2113
25. MichaelTP
MocklerTC
BretonG
McEnteeC
ByerA
2008 Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet 4 e14 doi:10.1371/journal.pgen.0040014
26. HudsonME
QuailPH
2003 Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133 1605 1616
27. HarmerSL
KaySA
2005 Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis. Plant Cell 17 1926 1940
28. RawatR
SchwartzJ
JonesMA
SairanenI
ChengY
2009 REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci U S A 106 16883 16888
29. KunoN
MollerSG
ShinomuraT
XuX
ChuaNH
2003 The novel MYB protein EARLY-PHYTOCHROME-RESPONSIVE1 is a component of a slave circadian oscillator in Arabidopsis. Plant Cell 15 2476 2488
30. ZhangX
ChenY
WangZY
ChenZ
GuH
2007 Constitutive expression of CIR1 (RVE2) affects several circadian-regulated processes and seed germination in Arabidopsis. Plant J 51 512 525
31. GongW
HeaK
CovingtonMF
Dinesh-KumarSP
SnyderM
2008 The development of protein microarrays and their applications in DNA–protein and protein–protein interaction analyses of Arabidopsis transcription factors. Molecular Plant 1 27 41
32. EdwardsKD
LynnJR
GyulaP
NagyF
MillarAJ
2005 Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170 387 400
33. WangZY
TobinEM
1998 Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93 1207 1217
34. SchafferR
RamsayN
SamachA
CordenS
PutterillJ
1998 The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93 1219 1229
35. NozueK
MaloofJN
2006 Diurnal regulation of plant growth. Plant Cell Environ 29 396 408
36. ImaizumiT
2010 Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13 83 89
37. MizoguchiT
WheatleyK
HanzawaY
WrightL
MizoguchiM
2002 LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2 629 641
38. AlonsoJM
StepanovaAN
LeisseTJ
KimCJ
ChenH
2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657
39. KimJY
SongHR
TaylorBL
CarreIA
2003 Light-regulated translation mediates gated induction of the Arabidopsis clock protein LHY. Embo J 22 935 944
40. FarreEM
KaySA
2007 PRR7 protein levels are regulated by light and the circadian clock in Arabidopsis. Plant J 52 548 560
41. ItoS
NakamichiN
KibaT
YamashinoT
MizunoT
2007 Rhythmic and light-inducible appearance of clock-associated pseudo-response regulator protein PRR9 through programmed degradation in the dark in Arabidopsis thaliana. Plant Cell Physiol 48 1644 1651
42. KibaT
HenriquesR
SakakibaraH
ChuaNH
2007 Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant Cell 19 2516 2530
43. HardinPE
HallJC
RosbashM
1990 Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343 536 540
44. ZerrDM
HallJC
RosbashM
SiwickiKK
1990 Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci 10 2749 2762
45. GreenRM
TobinEM
1999 Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc Natl Acad Sci U S A 96 4176 4179
46. AlabadiD
YanovskyMJ
MasP
HarmerSL
KaySA
2002 Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr Biol 12 757 761
47. SomersDE
DevlinPF
KaySA
1998 Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282 1488 1490
48. McWattersHG
KolmosE
HallA
DoyleMR
AmasinoRM
2007 ELF4 is required for oscillatory properties of the circadian clock. Plant Physiol 144 391 401
49. WangZY
KenigsbuchD
SunL
HarelE
OngMS
1997 A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9 491 507
50. CraigonDJ
JamesN
OkyereJ
HigginsJ
JothamJ
2004 NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res 32 D575 577
51. GouldCM
DiellaF
ViaA
PuntervollP
GemundC
2010 ELM: the status of the 2010 eukaryotic linear motif resource. Nucleic Acids Res 38 D167 180
52. OeckingC
JaspertN
2009 Plant 14-3-3 proteins catch up with their mammalian orthologs. Curr Opin Plant Biol 12 760 765
53. MehraA
ShiM
BakerCL
ColotHV
LorosJJ
2009 A role for casein kinase 2 in the mechanism underlying circadian temperature compensation. Cell 137 749 760
54. TosiniG
MenakerM
1998 The tau mutation affects temperature compensation of hamster retinal circadian oscillators. Neuroreport 9 1001 1005
55. KonopkaRJ
PittendrighC
OrrD
1989 Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants. J Neurogenet 6 1 10
56. GouldPD
LockeJC
LarueC
SouthernMM
DavisSJ
2006 The molecular basis of temperature compensation in the Arabidopsis circadian clock. Plant Cell 18 1177 1187
57. SalomePA
WeigelD
McClungCR
2010 The Role of the Arabidopsis Morning Loop Components CCA1, LHY, PRR7, and PRR9 in Temperature Compensation. Plant Cell 22 3650 3661
58. Dowson-DayMJ
MillarAJ
1999 Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J 17 63 71
59. MasP
AlabadiD
YanovskyMJ
OyamaT
KaySA
2003 Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell 15 223 236
60. KeveiE
GyulaP
HallA
Kozma-BognarL
KimWY
2006 Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE. Plant Physiol 140 933 945
61. ItoS
NakamichiN
NakamuraY
NiwaY
KatoT
2007 Genetic linkages between circadian clock-associated components and phytochrome-dependent red light signal transduction in Arabidopsis thaliana. Plant Cell Physiol 48 971 983
62. KaczorowskiKA
QuailPH
2003 Arabidopsis PSEUDO-RESPONSE REGULATOR7 is a signaling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock. Plant Cell 15 2654 2665
63. YanovskyMJ
WhitelamGC
CasalJJ
2000 fhy3-1 retains inductive responses of phytochrome A. Plant Physiol 123 235 242
64. HicksKA
MillarAJ
CarreIA
SomersDE
StraumeM
1996 Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274 790 792
65. JonesMA
CovingtonMF
DitacchioL
VollmersC
PandaS
2010 Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc Natl Acad Sci U S A
66. ErikssonME
HananoS
SouthernMM
HallA
MillarAJ
2003 Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock. Planta 218 159 162
67. ZhengY
RenN
WangH
StrombergAJ
PerrySE
2009 Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21 2563 2577
68. OhE
KangH
YamaguchiS
ParkJ
LeeD
2009 Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21 403 419
69. BernardF
KrejciA
HousdenB
AdryanB
BraySJ
2010 Specificity of Notch pathway activation: twist controls the transcriptional output in adult muscle progenitors. Development 137 2633 2642
70. ItoS
MatsushikaA
YamadaH
SatoS
KatoT
2003 Characterization of the APRR9 pseudo-response regulator belonging to the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol 44 1237 1245
71. YamamotoY
SatoE
ShimizuT
NakamichN
SatoS
2003 Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant Cell Physiol 44 1119 1130
72. NozueK
CovingtonMF
DuekPD
LorrainS
FankhauserC
2007 Rhythmic growth explained by coincidence between internal and external cues. Nature 448 358 361
73. SchmidM
DavisonTS
HenzSR
PapeUJ
DemarM
2005 A gene expression map of Arabidopsis thaliana development. Nat Genet 37 501 506
74. KellerA
NesvizhskiiAI
KolkerE
AebersoldR
2002 Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74 5383 5392
75. NesvizhskiiAI
KellerA
KolkerE
AebersoldR
2003 A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75 4646 4658
76. TabbDL
2008 What's driving false discovery rates? J Proteome Res 7 45 46
77. StrayerC
OyamaT
SchultzTF
RamanR
SomersDE
2000 Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289 768 771
78. CloughSJ
BentAF
1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743
79. PlautzJD
StraumeM
StanewskyR
JamisonCF
BrandesC
1997 Quantitative analysis of Drosophila period gene transcription in living animals. J Biol Rhythms 12 204 217
80. Martin-TryonEL
KrepsJA
HarmerSL
2007 GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol 143 473 486
81. MocklerTC
YuX
ShalitinD
ParikhD
MichaelTP
2004 Regulation of flowering time in Arabidopsis by K homology domain proteins. Proc Natl Acad Sci U S A 101 12759 12764
82. StoneSL
BraybrookSA
PaulaSL
KwongLW
MeuserJ
2008 Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis. Proc Natl Acad Sci U S A 105 3151 3156
83. CovingtonMF
HarmerSL
2007 The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol 5 e222 doi:10.1371/journal.pbio.0050222
84. FukushimaA
KusanoM
NakamichiN
KobayashiM
HayashiN
2009 Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc Natl Acad Sci U S A 106 7251 7256
85. NakamichiN
KusanoM
FukushimaA
KitaM
ItoS
2009 Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50 447 462
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 3
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Whole-Exome Re-Sequencing in a Family Quartet Identifies Mutations As the Cause of a Novel Skeletal Dysplasia
- Origin-Dependent Inverted-Repeat Amplification: A Replication-Based Model for Generating Palindromic Amplicons
- FUS Transgenic Rats Develop the Phenotypes of Amyotrophic Lateral Sclerosis and Frontotemporal Lobar Degeneration
- Limited dCTP Availability Accounts for Mitochondrial DNA Depletion in Mitochondrial Neurogastrointestinal Encephalomyopathy (MNGIE)