Home LiteratureArticle Details
PMID: 14973171 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

The F-box protein ZEITLUPE confers dosage-dependent control on the circadian clock, photomorphogenesis, and flowering time.

The Plant cell ·Vol. 16 ·No. 3 ·2004-03-00 ·Pages 769-82

Somers DE, Kim WY, Geng R

Abstract

As an F-box protein, ZEITLUPE (ZTL) is involved in targeting one or more substrates for ubiquitination and degradation via the proteasome. The initial characterization of ZTL suggested a function limited largely to the regulation of the circadian clock. Here, we show a considerably broader role for ZTL in the control of circadian period and photomorphogenesis. Using a ZTL-specific antibody, we quantitated and characterized a ZTL dosage series that ranges from a null mutation to a strong ZTL overexpressor. In the dark, ztl null mutations lengthen circadian period, and overexpression causes arrhythmicity, suggesting a more comprehensive role for this protein in the clock than previously suspected. In the light, circadian period becomes increasingly shorter at higher levels of ZTL, to the point of arrhythmicity. By contrast, hypocotyl length increases and flowering time is delayed in direct proportion to the level of ZTL. We propose a novel testable mechanism by which circadian period and amplitude may act together to gate phytochrome B-mediated suppression of hypocotyl. We also demonstrate that ZTL-dependent delay of flowering is mediated through decreases in CONSTANS and FLOWERING LOCUS T message levels, thus directly linking proteasome-dependent proteolysis to flowering.

MeSH Terms
Arabidopsis/genetics,growth & development,physiology Arabidopsis Proteins/genetics,physiology Base Sequence Circadian Rhythm/genetics,physiology DNA, Plant/genetics Flowers/growth & development Gene Dosage Gene Expression Regulation, Plant Genes, Plant Hypocotyl/growth & development Photobiology Plasmids/genetics
Chemicals
Arabidopsis Proteins DNA, Plant ZTL protein, Arabidopsis
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Somers David E
Department of Plant Biology/Plant Biotechnology Center, Ohio State University, Columbus, Ohio 43210, USA. somers.24@osu.edu
Kim Woe-Yeon
Geng Ruishuang
References (63)
63 references, click to expand
  1. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.
    Nature. 2001 Apr 26;410(6832):1116-20 PMID: 11323677
  2. A role for LKP2 in the circadian clock of Arabidopsis.
    Plant Cell. 2001 Dec;13(12):2659-70 PMID: 11752379
  3. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis.
    Plant J. 1999 Jan;17(1):63-71 PMID: 10069068
  4. The out of phase 1 mutant defines a role for PHYB in circadian phase control in Arabidopsis.
    Plant Physiol. 2002 Aug;129(4):1674-85 PMID: 12177480
  5. Time zones: a comparative genetics of circadian clocks.
    Nat Rev Genet. 2001 Sep;2(9):702-15 PMID: 11533719
  6. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis.
    Cell. 2000 Apr 28;101(3):331-40 PMID: 10847687
  7. Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis.
    Curr Biol. 2002 Apr 30;12(9):757-61 PMID: 12007421
  8. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins.
    Trends Plant Sci. 2003 Mar;8(3):135-42 PMID: 12663224
  9. Molecular bases of circadian rhythms.
    Annu Rev Cell Dev Biol. 2001;17:215-53 PMID: 11687489
  10. Phototropins 1 and 2: versatile plant blue-light receptors.
    Trends Plant Sci. 2002 May;7(5):204-10 PMID: 11992825
  11. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.
    Science. 2000 Dec 15;290(5499):2110-3 PMID: 11118138
  12. All in good time: the Arabidopsis circadian clock.
    Trends Plant Sci. 2000 Dec;5(12):517-22 PMID: 11120473
  13. Circadian clock mutants in Arabidopsis identified by luciferase imaging.
    Science. 1995 Feb 24;267(5201):1161-3 PMID: 7855595
  14. SCF and Cullin/Ring H2-based ubiquitin ligases.
    Annu Rev Cell Dev Biol. 1999;15:435-67 PMID: 10611969
  15. LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis.
    Dev Cell. 2002 May;2(5):629-41 PMID: 12015970
  16. EARLY FLOWERING3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis.
    Plant Cell. 2001 Jun;13(6):1281-92 PMID: 11402160
  17. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis.
    Nature. 2003 Nov 20;426(6964):302-6 PMID: 14628054
  18. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis.
    Cell. 2000 Apr 28;101(3):319-29 PMID: 10847686
  19. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana.
    Nature. 2002 Sep 5;419(6902):74-7 PMID: 12214234
  20. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  21. Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9124-9 PMID: 10430906
  22. Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock.
    Plant Cell Physiol. 2000 Sep;41(9):1002-12 PMID: 11100772
  23. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering.
    Cell. 1998 Jun 26;93(7):1219-29 PMID: 9657154
  24. The network of time: understanding the molecular circadian system.
    Curr Biol. 2003 Mar 4;13(5):R198-207 PMID: 12620213
  25. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation.
    Plant Mol Biol. 1994 Sep;25(6):989-94 PMID: 7919218
  26. Control of flowering time: interacting pathways as a basis for diversity.
    Plant Cell. 2002;14 Suppl:S111-30 PMID: 12045273
  27. Quantitative analysis of Drosophila period gene transcription in living animals.
    J Biol Rhythms. 1997 Jun;12(3):204-17 PMID: 9181432
  28. Distinct regulation of CAB and PHYB gene expression by similar circadian clocks.
    Plant J. 2002 Nov;32(4):529-37 PMID: 12445124
  29. Living by the calendar: how plants know when to flower.
    Nat Rev Mol Cell Biol. 2003 Apr;4(4):265-75 PMID: 12671649
  30. LKP1 (LOV kelch protein 1): a factor involved in the regulation of flowering time in arabidopsis.
    Plant J. 2000 Sep;23(6):807-15 PMID: 10998191
  31. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog.
    Science. 2000 Aug 4;289(5480):768-71 PMID: 10926537
  32. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock.
    Science. 1998 Nov 20;282(5393):1488-90 PMID: 9822379
  33. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana.
    Nature. 2003 Dec 4;426(6966):567-70 PMID: 14654842
  34. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression.
    Cell. 1998 Jun 26;93(7):1207-17 PMID: 9657153
  35. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter.
    Science. 2002 Aug 2;297(5582):815-9 PMID: 12098706
  36. An Arabidopsis circadian clock component interacts with both CRY1 and phyB.
    Nature. 2001 Mar 22;410(6827):487-90 PMID: 11260718
  37. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant.
    Science. 1996 Nov 1;274(5288):790-2 PMID: 8864121
  38. Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4933-8 PMID: 12665620
  39. The Arabidopsis SRR1 gene mediates phyB signaling and is required for normal circadian clock function.
    Genes Dev. 2003 Jan 15;17(2):256-68 PMID: 12533513
  40. Molecular basis of seasonal time measurement in Arabidopsis.
    Nature. 2002 Sep 19;419(6904):308-12 PMID: 12239570
  41. ELF3 modulates resetting of the circadian clock in Arabidopsis.
    Plant Cell. 2001 Jun;13(6):1305-15 PMID: 11402162
  42. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases.
    Trends Cell Biol. 2000 Oct;10(10):429-39 PMID: 10998601
  43. Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis.
    Plant Physiol. 2001 Dec;127(4):1607-16 PMID: 11743105
  44. The COP/DET/FUS proteins-regulators of eukaryotic growth and development.
    Semin Cell Dev Biol. 2000 Dec;11(6):495-503 PMID: 11145879
  45. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.
    Science. 2001 Aug 3;293(5531):880-3 PMID: 11486091
  46. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene.
    Science. 1999 Sep 3;285(5433):1579-82 PMID: 10477524
  47. The kelch repeat superfamily of proteins: propellers of cell function.
    Trends Cell Biol. 2000 Jan;10(1):17-24 PMID: 10603472
  48. Light-regulated translation mediates gated induction of the Arabidopsis clock protein LHY.
    EMBO J. 2003 Feb 17;22(4):935-44 PMID: 12574129
  49. Nuclear transport of plant potyviral proteins.
    Plant Cell. 1990 Oct;2(10):987-98 PMID: 2136629
  50. Patterns of expression and normalized levels of the five Arabidopsis phytochromes.
    Plant Physiol. 2002 Sep;130(1):442-56 PMID: 12226523
  51. MYB transcription factors in the Arabidopsis circadian clock.
    J Exp Bot. 2002 Jul;53(374):1551-7 PMID: 12096093
  52. Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4176-9 PMID: 10097183
  53. Selected Components of the Shade-Avoidance Syndrome Are Displayed in a Normal Manner in Mutants of Arabidopsis thaliana and Brassica rapa Deficient in Phytochrome B.
    Plant Physiol. 1993 Aug;102(4):1179-1184 PMID: 12231894
  54. Clock-associated genes in Arabidopsis: a family affair.
    Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1745-53 PMID: 11710981
  55. White collar-1, a DNA binding transcription factor and a light sensor.
    Science. 2002 Aug 2;297(5582):840-3 PMID: 12098705
  56. Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis.
    Plant Cell. 2003 Jan;15(1):223-36 PMID: 12509533
  57. A suite of photoreceptors entrains the plant circadian clock.
    J Biol Rhythms. 2003 Jun;18(3):217-26 PMID: 12828279
  58. The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction.
    Prog Biophys Mol Biol. 1999;72(3):299-328 PMID: 10581972
  59. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity.
    Plant Cell. 2000 Dec;12(12):2499-2510 PMID: 11148293
  60. The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context.
    Curr Biol. 2002 Sep 3;12(17):1529-34 PMID: 12225670
  61. De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis.
    Curr Biol. 2002 Sep 3;12(17):1462-72 PMID: 12225661
  62. CIRCADIAN RHYTHMS IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:139-162 PMID: 11337395
  63. WHITE COLLAR-1, a multifunctional neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2.
    J Biol Chem. 2003 Feb 7;278(6):3801-8 PMID: 12454012
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-03-00
Epub
2004-00-18
Pages
769-82
Language
English
Region
England
NLM ID
9208688
PMCID
PMC385287
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com