The Calcium Rhythms of Different Cell Types Oscillate with Different Circadian Phases

Overview

Journal Plant Physiol

Specialty Physiology

Date 2001 Feb 13

PMID 11161036

Citations 17

Authors

N T Wood

A Haley

C H Johnson

A H van der Luit

A J Trewavas

Affiliations

Soon will be listed here.

Abstract

Transgenic tobacco (Nicotiana plumbaginifolia) seedlings containing the Ca(2+)-sensitive luminescent protein aequorin have been shown to exhibit circadian variations in cytosolic calcium. Concomitant measurements of cytosolic and nuclear calcium show that circadian variations in the cytoplasm are not expressed in the nucleus. To investigate whether all cells of transgenic seedlings contribute equally to circadian variations in cytosolic calcium, different promoters eliciting different expression patterns have been placed upstream of aequorin and used for transformation. The circadian peak occurred at different times in the three transgenic lines constructed. Luminescence imaging of these transgenic lines indicated that aequorin was differentially accumulated among the main tissues and cells of the seedlings and overcoat technology with applied epidermal strips indicated that the surface cell layers contribute the vast majority of luminescent light. We conclude that the Ca(2+) rhythmicities of cells and tissues oscillate with distinct differences in phase, that this might represent different underlying cellular control mechanisms and that these observations have significant implications for our understanding and study of Ca(2+) mediated signal transduction in plant cells.

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References

Sai J, Johnson C . Different circadian oscillators control Ca(2+) fluxes and lhcb gene expression. Proc Natl Acad Sci U S A. 1999; 96(20):11659-63. PMC: 18090. DOI: 10.1073/pnas.96.20.11659. View

van der Luit A, Olivari C, Haley A, Knight M, Trewavas A . Distinct calcium signaling pathways regulate calmodulin gene expression in tobacco. Plant Physiol. 1999; 121(3):705-14. PMC: 59432. DOI: 10.1104/pp.121.3.705. View

Thain S, Hall A, Millar A . Functional independence of circadian clocks that regulate plant gene expression. Curr Biol. 2000; 10(16):951-6. DOI: 10.1016/s0960-9822(00)00630-8. View

Wood N, Allan A, Haley A, Trewavas A . The characterization of differential calcium signalling in tobacco guard cells. Plant J. 2000; 24(3):335-44. DOI: 10.1046/j.1365-313x.2000.00881.x. View

Gleave A . A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol. 1992; 20(6):1203-7. DOI: 10.1007/BF00028910. View

Hennessey T, Field C . Evidence of multiple circadian oscillators in bean plants. J Biol Rhythms. 1992; 7(2):105-13. DOI: 10.1177/074873049200700202. View

Gorton H, Williams W, Binns M, Gemmell C, Leheny E, Shepherd A . Circadian Stomatal Rhythms in Epidermal Peels from Vicia faba. Plant Physiol. 1989; 90(4):1329-34. PMC: 1061891. DOI: 10.1104/pp.90.4.1329. View

. A simple and general method for transferring genes into plants. Science. 1985; 227(4691):1229-31. DOI: 10.1126/science.227.4691.1229. View

Knight M, Campbell A, Smith S, Trewavas A . Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature. 1991; 352(6335):524-6. DOI: 10.1038/352524a0. View

10.

Hastings M . Neuroendocrine rhythms. Pharmacol Ther. 1991; 50(1):35-71. DOI: 10.1016/0163-7258(91)90072-t. View

11.

Gilroy S, Read N, Trewavas A . Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature. 1990; 346(6286):769-71. DOI: 10.1038/346769a0. View

12.

Roenneberg T, Morse D . Two circadian oscillators in one cell. Nature. 2018; 362(6418):362-364. DOI: 10.1038/362362a0. View

13.

Holsters M, De Waele D, Depicker A, Messens E, Van Montagu M, Schell J . Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet. 1978; 163(2):181-7. DOI: 10.1007/BF00267408. View

14.

Johnson C, Knight M, Kondo T, Masson P, Sedbrook J, Haley A . Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science. 1995; 269(5232):1863-5. DOI: 10.1126/science.7569925. View

15.

Liu Y, Tsinoremas N, Johnson C, Lebedeva N, Golden S, Ishiura M . Circadian orchestration of gene expression in cyanobacteria. Genes Dev. 1995; 9(12):1469-78. DOI: 10.1101/gad.9.12.1469. View

16.

Taylor J, Renwick K, Webb A, McAinsh M, Furini A, Bartels D . ABA-regulated promoter activity in stomatal guard cells. Plant J. 1995; 7(1):129-34. DOI: 10.1046/j.1365-313x.1995.07010129.x. View

17.

Thoma S, Hecht U, Kippers A, Botella J, de Vries S, Somerville C . Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol. 1994; 105(1):35-45. PMC: 159326. DOI: 10.1104/pp.105.1.35. View

18.

Michel D, Furini A, Salamini F, Bartels D . Structure and regulation of an ABA- and desiccation-responsive gene from the resurrection plant Craterostigma plantagineum. Plant Mol Biol. 1994; 24(4):549-60. DOI: 10.1007/BF00023553. View

19.

Shimomura O, Kishi Y, Inouye S . The relative rate of aequorin regeneration from apoaequorin and coelenterazine analogues. Biochem J. 1993; 296 ( Pt 3):549-51. PMC: 1137732. DOI: 10.1042/bj2960549. View

20.

Neuhaus G, Bowler C, Kern R, Chua N . Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell. 1993; 73(5):937-52. DOI: 10.1016/0092-8674(93)90272-r. View