Regulation of Iron Homeostasis in Arabidopsis Thaliana by the Clock Regulator Time for Coffee

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2009 Oct 16

PMID 19828447

Citations 28

Authors

Celine Duc

Francoise Cellier

Stephane Lobreaux

Jean-Francois Briat

Frederic Gaymard

Affiliations

Soon will be listed here.

Abstract

In plants, iron homeostasis is tightly regulated to supply sufficient amounts of this metal for an optimal growth while preventing excess accumulation to avoid oxidative stress. To identify new regulators of iron homeostasis, a luciferase-based genetic screen using the Arabidopsis AtFer1 ferritin promoter as a target was developed. This screen identified TIME FOR COFFEE (TIC) as a regulator of AtFer1 gene expression. TIC was previously described as a nuclear regulator of the circadian clock. Mutants in the TIC gene exhibited a chlorotic phenotype rescued by exogenous iron addition and are hypersensitive to iron during the early stages of development. We showed that iron overload-responsive genes are regulated by TIC and by the central oscillator of the circadian clock. TIC represses their expression under low iron conditions, and its activity requires light and light/dark cycles. Regarding AtFer1, this repression is independent of the previously characterized cis-acting element iron-dependent regulatory sequence, known to be involved in AtFer1 repression. These results showed that the regulation of iron homeostasis in plants is a major output of the TIC- and central oscillator-dependent signaling pathways.

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References

McWatters H, Bastow R, Hall A, Millar A . The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature. 2000; 408(6813):716-20. DOI: 10.1038/35047079. View

Liu X, Covington M, Fankhauser C, Chory J, Wagner D . ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell. 2001; 13(6):1293-304. PMC: 135570. DOI: 10.1105/tpc.13.6.1293. View

Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre I . The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998; 93(7):1219-29. DOI: 10.1016/s0092-8674(00)81465-8. View

Mas P . Circadian clock signaling in Arabidopsis thaliana: from gene expression to physiology and development. Int J Dev Biol. 2005; 49(5-6):491-500. DOI: 10.1387/ijdb.041968pm. View

BEINERT H . Micro methods for the quantitative determination of iron and copper in biological material. Methods Enzymol. 1978; 54:435-45. DOI: 10.1016/s0076-6879(78)54027-5. View

Arnaud N, Murgia I, Boucherez J, Briat J, Cellier F, Gaymard F . An iron-induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. J Biol Chem. 2006; 281(33):23579-88. DOI: 10.1074/jbc.M602135200. View

Kim S, Guerinot M . Mining iron: iron uptake and transport in plants. FEBS Lett. 2007; 581(12):2273-80. DOI: 10.1016/j.febslet.2007.04.043. View

McWatters H, Kolmos E, Hall A, Doyle M, Amasino R, Gyula P . ELF4 is required for oscillatory properties of the circadian clock. Plant Physiol. 2007; 144(1):391-401. PMC: 1913775. DOI: 10.1104/pp.107.096206. View

Moore B, Zhou L, Rolland F, Hall Q, Cheng W, Liu Y . Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science. 2003; 300(5617):332-6. DOI: 10.1126/science.1080585. View

10.

Dellagi A, Rigault M, Segond D, Roux C, Kraepiel Y, Cellier F . Siderophore-mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J. 2005; 43(2):262-72. DOI: 10.1111/j.1365-313X.2005.02451.x. View

11.

Tarantino D, Petit J, Lobreaux S, Briat J, Soave C, Murgia I . Differential involvement of the IDRS cis-element in the developmental and environmental regulation of the AtFer1 ferritin gene from Arabidopsis. Planta. 2003; 217(5):709-16. DOI: 10.1007/s00425-003-1038-z. View

12.

Baena-Gonzalez E, Rolland F, Thevelein J, Sheen J . A central integrator of transcription networks in plant stress and energy signalling. Nature. 2007; 448(7156):938-42. DOI: 10.1038/nature06069. View

13.

Covington M, Panda S, Liu X, Strayer C, Wagner D, Kay S . ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant Cell. 2001; 13(6):1305-15. PMC: 135573. DOI: 10.1105/tpc.13.6.1305. View

14.

Lobreaux S, Briat J . Ferritin accumulation and degradation in different organs of pea (Pisum sativum) during development. Biochem J. 1991; 274 ( Pt 2):601-6. PMC: 1150181. DOI: 10.1042/bj2740601. View

15.

Briat J, Curie C, Gaymard F . Iron utilization and metabolism in plants. Curr Opin Plant Biol. 2007; 10(3):276-82. DOI: 10.1016/j.pbi.2007.04.003. View

16.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

17.

Ravet K, Touraine B, Kim S, Cellier F, Thomine S, Guerinot M . Post-translational regulation of AtFER2 ferritin in response to intracellular iron trafficking during fruit development in Arabidopsis. Mol Plant. 2009; 2(5):1095-106. DOI: 10.1093/mp/ssp041. View

18.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

19.

Petit J, Van Wuytswinkel O, Briat J, Lobreaux S . Characterization of an iron-dependent regulatory sequence involved in the transcriptional control of AtFer1 and ZmFer1 plant ferritin genes by iron. J Biol Chem. 2000; 276(8):5584-90. DOI: 10.1074/jbc.M005903200. View

20.

Smith A, Stitt M . Coordination of carbon supply and plant growth. Plant Cell Environ. 2007; 30(9):1126-49. DOI: 10.1111/j.1365-3040.2007.01708.x. View