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Philos Trans R Soc Lond B Biol Sci. Nov 29, 2001; 356(1415): 1755–1759.
PMCID: PMC1088551

RNA-binding proteins and circadian rhythms in Arabidopsis thaliana.

Abstract

An Arabidopsis transcript preferentially expressed at the end of the daily light period codes for the RNA-binding protein AtGRP7. A reverse genetic approach in Arabidopsis thaliana has revealed its role in the generation of circadian rhythmicity: AtGRP7 is part of a negative feedback loop through which it influences the oscillations of its own transcript. Biochemical and genetic experiments indicate a mechanism for this autoregulatory circuit: Atgrp7 gene transcription is rhythmically activated by the circadian clock during the day. The AtGPR7 protein accumulates with a certain delay and represses further accumulation of its transcript, presumably at the post-transcriptional level. In this respect, the AtGRP7 feedback loop differs from known circadian oscillators in the fruitfly Drosophila and mammals based on oscillating clock proteins that repress transcription of their own genes with a 24 h rhythm. It is proposed that the AtGRP7 feedback loop may act within an output pathway from the Arabidopsis clock.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aronson BD, Johnson KA, Loros JJ, Dunlap JC. Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science. 1994 Mar 18;263(5153):1578–1584. [PubMed]
  • Carpenter CD, Kreps JA, Simon AE. Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol. 1994 Mar;104(3):1015–1025. [PMC free article] [PubMed]
  • Carre IA, Kay SA. Multiple DNA-Protein Complexes at a Circadian-Regulated Promoter Element. Plant Cell. 1995 Dec;7(12):2039–2051. [PMC free article] [PubMed]
  • Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, Steeves TD, Weitz CJ, Takahashi JS, Kay SA. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science. 1998 Jun 5;280(5369):1599–1603. [PubMed]
  • Deschamps S, Viel A, Garrigos M, Denis H, le Maire M. mRNP4, a major mRNA-binding protein from Xenopus oocytes is identical to transcription factor FRG Y2. J Biol Chem. 1992 Jul 15;267(20):13799–13802. [PubMed]
  • Dowson-Day MJ, Millar AJ. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J. 1999 Jan;17(1):63–71. [PubMed]
  • Dumas B, Freyssinet G, Pallett KE. Tissue-Specific Expression of Germin-Like Oxalate Oxidase during Development and Fungal Infection of Barley Seedlings. Plant Physiol. 1995 Apr;107(4):1091–1096. [PMC free article] [PubMed]
  • Dunlap J. Circadian rhythms. An end in the beginning. Science. 1998 Jun 5;280(5369):1548–1549. [PubMed]
  • Dunlap JC. Molecular bases for circadian clocks. Cell. 1999 Jan 22;96(2):271–290. [PubMed]
  • Edery I. Role of posttranscriptional regulation in circadian clocks: lessons from Drosophila. Chronobiol Int. 1999 Jul;16(4):377–414. [PubMed]
  • Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 1999 Sep 1;18(17):4679–4688. [PMC free article] [PubMed]
  • Green RM, Tobin EM. 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):4176–4179. [PMC free article] [PubMed]
  • Hardin PE, Hall JC, Rosbash M. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature. 1990 Feb 8;343(6258):536–540. [PubMed]
  • Heintzen C, Melzer S, Fischer R, Kappeler S, Apel K, Staiger D. A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. Plant J. 1994 Jun;5(6):799–813. [PubMed]
  • Heintzen C, Fischer R, Melzer S, Kappeler K, Apel K, Staiger D. Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L. Plant Physiol. 1994 Nov;106(3):905–915. [PMC free article] [PubMed]
  • Heintzen C, Nater M, Apel K, Staiger D. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8515–8520. [PMC free article] [PubMed]
  • Hicks KA, Millar AJ, Carré IA, Somers DE, Straume M, Meeks-Wagner DR, Kay SA. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science. 1996 Nov 1;274(5288):790–792. [PubMed]
  • Hurkman WJ, Tanaka CK. Germin Gene Expression Is Induced in Wheat Leaves by Powdery Mildew Infection. Plant Physiol. 1996 Jul;111(3):735–739. [PMC free article] [PubMed]
  • Lane BG, Cuming AC, Frégeau J, Carpita NC, Hurkman WJ, Bernier F, Dratewka-Kos E, Kennedy TD. Germin isoforms are discrete temporal markers of wheat development. Pseudogermin is a uniquely thermostable water-soluble oligomeric protein in ungerminated embryos and like germin in germinated embryos, it is incorporated into cell walls. Eur J Biochem. 1992 Nov 1;209(3):961–969. [PubMed]
  • Liu Z, Taub CC, McClung CR. Identification of an Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase activase (RCA) minimal promoter regulated by light and the circadian clock. Plant Physiol. 1996 Sep;112(1):43–51. [PMC free article] [PubMed]
  • McNeil GP, Zhang X, Genova G, Jackson FR. A molecular rhythm mediating circadian clock output in Drosophila. Neuron. 1998 Feb;20(2):297–303. [PubMed]
  • McWatters HG, Roden LC, Staiger D. Picking out parallels: plant circadian clocks in context. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1735–1743. [PMC free article] [PubMed]
  • Membré N, Berna A, Neutelings G, David A, David H, Staiger D, Sáez Vásquez J, Raynal M, Delseny M, Bernier F. cDNA sequence, genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins. Plant Mol Biol. 1997 Nov;35(4):459–469. [PubMed]
  • Membré N, Bernier F, Staiger D, Berna A. Arabidopsis thaliana germin-like proteins: common and specific features point to a variety of functions. Planta. 2000 Aug;211(3):345–354. [PubMed]
  • Michalowski CB, Bohnert HJ. Nucleotide Sequence of a Root-Specific Transcript Encoding a Germin-Like Protein from the Halophyte Mesembryanthemum crystallinum. Plant Physiol. 1992 Sep;100(1):537–538. [PMC free article] [PubMed]
  • Michelotti EF, Michelotti GA, Aronsohn AI, Levens D. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol Cell Biol. 1996 May;16(5):2350–2360. [PMC free article] [PubMed]
  • Millar AJ, Kay SA. Circadian Control of cab Gene Transcription and mRNA Accumulation in Arabidopsis. Plant Cell. 1991 May;3(5):541–550. [PMC free article] [PubMed]
  • Millar AJ, Carré IA, Strayer CA, Chua NH, Kay SA. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science. 1995 Feb 24;267(5201):1161–1163. [PubMed]
  • Mittag M, Lee DH, Hastings JW. Circadian expression of the luciferin-binding protein correlates with the binding of a protein to the 3' untranslated region of its mRNA. Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5257–5261. [PMC free article] [PubMed]
  • Morse D, Milos PM, Roux E, Hastings JW. Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proc Natl Acad Sci U S A. 1989 Jan;86(1):172–176. [PMC free article] [PubMed]
  • Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell. 2000 Apr 28;101(3):331–340. [PubMed]
  • Newby LM, Jackson FR. Regulation of a specific circadian clock output pathway by lark, a putative RNA-binding protein with repressor activity. J Neurobiol. 1996 Sep;31(1):117–128. [PubMed]
  • Ono M, Sage-Ono K, Inoue M, Kamada H, Harada H. Transient increase in the level of mRNA for a germin-like protein in leaves of the short-day plant Pharbitis nil during the photoperiodic induction of flowering. Plant Cell Physiol. 1996 Sep;37(6):855–861. [PubMed]
  • Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science. 1999 Sep 3;285(5433):1579–1582. [PubMed]
  • Pilgrim ML, Caspar T, Quail PH, McClung CR. Circadian and light-regulated expression of nitrate reductase in Arabidopsis. Plant Mol Biol. 1993 Oct;23(2):349–364. [PubMed]
  • PITTENDRIGH CS. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp Quant Biol. 1960;25:159–184. [PubMed]
  • Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998 Jun 26;93(7):1219–1229. [PubMed]
  • So WV, Rosbash M. Post-transcriptional regulation contributes to Drosophila clock gene mRNA cycling. EMBO J. 1997 Dec 1;16(23):7146–7155. [PMC free article] [PubMed]
  • Somers DE, Webb AA, Pearson M, Kay SA. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development. 1998 Feb;125(3):485–494. [PubMed]
  • Somers DE. The physiology and molecular bases of the plant circadian clock. Plant Physiol. 1999 Sep;121(1):9–20. [PMC free article] [PubMed]
  • Somers DE, Schultz TF, Milnamow M, Kay SA. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell. 2000 Apr 28;101(3):319–329. [PubMed]
  • Staiger D, Apel K. Circadian clock-regulated expression of an RNA-binding protein in Arabidopsis: characterisation of a minimal promoter element. Mol Gen Genet. 1999 Jun;261(4-5):811–819. [PubMed]
  • Staiger D, Heintzen C. The circadian system of Arabidopsis thaliana: forward and reverse genetic approaches. Chronobiol Int. 1999 Jan;16(1):1–16. [PubMed]
  • Staiger D, Apel K, Trepp G. The Atger3 promoter confers circadian clock-regulated transcription with peak expression at the beginning of the night. Plant Mol Biol. 1999 Jul;40(5):873–882. [PubMed]
  • Stanewsky R, Jamison CF, Plautz JD, Kay SA, Hall JC. Multiple circadian-regulated elements contribute to cycling period gene expression in Drosophila. EMBO J. 1997 Aug 15;16(16):5006–5018. [PMC free article] [PubMed]
  • Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Más P, Panda S, Kreps JA, Kay SA. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science. 2000 Aug 4;289(5480):768–771. [PubMed]
  • van Nocker S, Vierstra RD. Two cDNAs from Arabidopsis thaliana encode putative RNA binding proteins containing glycine-rich domains. Plant Mol Biol. 1993 Feb;21(4):695–699. [PubMed]
  • Wang ZY, Tobin EM. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998 Jun 26;93(7):1207–1217. [PubMed]
  • Zhong HH, McClung CR. The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol Gen Genet. 1996 May 23;251(2):196–203. [PubMed]

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