Skip to main content
NCBI home page
Plant Physiology logoLink to Plant Physiology
. 1993 Oct;103(2):553–564. doi: 10.1104/pp.103.2.553

Differential Involvement of the Circadian Clock in the Expression of Genes Required for Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Synthesis, Assembly, and Activation in Arabidopsis thaliana.

M L Pilgrim 1, C R McClung 1
PMCID: PMC159015  PMID: 12231961

Abstract

We have investigated the role of the circadian clock in the regulation of expression of genes required for ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) synthesis, assembly, and activation. Circadian oscillations in RCA (the gene encoding Rubisco activase) and RBCS (the gene encoding Rubisco small subunit) mRNA accumulation, with peak abundance occurring soon after dawn, occur in Arabidopsis thaliana grown in a light-dark (LD) photoperiod. These oscillations persist in plants that have been transferred from LD to either continuous darkness (DD) or continuous light (LL). In contrast, CPN60[alpha] (the gene encoding [alpha]-chaperonin) and CPN60[beta] (the gene encoding [beta]-chaperonin) mRNA abundance oscillates in a diurnal, but not in a circadian, fashion. Although rapid damping of the circadian oscillation in RCA mRNA abundance is observed in Arabidopsis that have been grown in LD and then transferred to DD for 2 d, the circadian oscillations in RCA and RBCS mRNA abundance persist for at least five continuous cycles in LL, demonstrating the robustness of the circadian oscillator.

Full Text

The Full Text of this article is available as a PDF (2.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adamska I., Scheel B., Kloppstech K. Circadian oscillations of nuclear-encoded chloroplast proteins in pea (Pisum sativum). Plant Mol Biol. 1991 Nov;17(5):1055–1065. doi: 10.1007/BF00037144. [DOI] [PubMed] [Google Scholar]
  2. Berry J. A., Lorimer G. H., Pierce J., Seemann J. R., Meek J., Freas S. Isolation, identification, and synthesis of 2-carboxyarabinitol 1-phosphate, a diurnal regulator of ribulose-bisphosphate carboxylase activity. Proc Natl Acad Sci U S A. 1987 Feb;84(3):734–738. doi: 10.1073/pnas.84.3.734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brooks A., Portis A. R. Protein-bound ribulose bisphosphate correlates with deactivation of ribulose bisphosphate carboxylase in leaves. Plant Physiol. 1988 May;87(1):244–249. doi: 10.1104/pp.87.1.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Busheva M., Garab G., Liker E., Tóth Z., Szèll M., Nagy F. Diurnal Fluctuations in the Content and Functional Properties of the Light Harvesting Chlorophyll a/b Complex in Thylakoid Membranes : Correlation with the Diurnal Rhythm of the mRNA Level. Plant Physiol. 1991 Apr;95(4):997–1003. doi: 10.1104/pp.95.4.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Campell B. R., Song Y., Posch T. E., Cullis C. A., Town C. D. Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene. 1992 Mar 15;112(2):225–228. doi: 10.1016/0378-1119(92)90380-8. [DOI] [PubMed] [Google Scholar]
  6. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  7. Giuliano G., Hoffman N. E., Ko K., Scolnik P. A., Cashmore A. R. A light-entrained circadian clock controls transcription of several plant genes. EMBO J. 1988 Dec 1;7(12):3635–3642. doi: 10.1002/j.1460-2075.1988.tb03244.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gorton H. L., Williams W. E., Binns M. E., Gemmell C. N., Leheny E. A., Shepherd A. C. Circadian Stomatal Rhythms in Epidermal Peels from Vicia faba. Plant Physiol. 1989 Aug;90(4):1329–1334. doi: 10.1104/pp.90.4.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Holmes M. G., Klein W. H. Photocontrol of Dark Circadian Rhythms in Stomata of Phaseolus vulgaris L. Plant Physiol. 1986 Sep;82(1):28–33. doi: 10.1104/pp.82.1.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kay S. A., Nagatani A., Keith B., Deak M., Furuya M., Chua N. H. Rice Phytochrome Is Biologically Active in Transgenic Tobacco. Plant Cell. 1989 Aug;1(8):775–782. doi: 10.1105/tpc.1.8.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kerr P. S., Rufty T. W., Huber S. C. Endogenous Rhythms in Photosynthesis, Sucrose Phosphate Synthase Activity, and Stomatal Resistance in Leaves of Soybean (Glycine max [L.] Merr.). Plant Physiol. 1985 Feb;77(2):275–280. doi: 10.1104/pp.77.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kim Y., Zhang H., Scholl R. L. Two evolutionarily divergent genes encode a cytoplasmic ribosomal protein of Arabidopsis thaliana. Gene. 1990 Sep 14;93(2):177–182. doi: 10.1016/0378-1119(90)90222-d. [DOI] [PubMed] [Google Scholar]
  13. Kobza J., Seemann J. R. Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to diurnal changes in irradiance. Plant Physiol. 1989 Mar;89(3):918–924. doi: 10.1104/pp.89.3.918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lan Y., Woodrow I. E., Mott K. A. Light-dependent changes in ribulose bisphosphate carboxylase activase activity in leaves. Plant Physiol. 1992 May;99(1):304–309. doi: 10.1104/pp.99.1.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Leutwiler L. S., Meyerowitz E. M., Tobin E. M. Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res. 1986 May 27;14(10):4051–4064. doi: 10.1093/nar/14.10.4051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ludwig S. R., Oppenheimer D. G., Silflow C. D., Snustad D. P. Characterization of the alpha-tubulin gene family of Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5833–5837. doi: 10.1073/pnas.84.16.5833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Martel R., Cloney L. P., Pelcher L. E., Hemmingsen S. M. Unique composition of plastid chaperonin-60: alpha and beta polypeptide-encoding genes are highly divergent. Gene. 1990 Oct 15;94(2):181–187. doi: 10.1016/0378-1119(90)90385-5. [DOI] [PubMed] [Google Scholar]
  18. Millar A. J., Kay S. A. Circadian Control of cab Gene Transcription and mRNA Accumulation in Arabidopsis. Plant Cell. 1991 May;3(5):541–550. doi: 10.1105/tpc.3.5.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Millar A. J., Short S. R., Chua N. H., Kay S. A. A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell. 1992 Sep;4(9):1075–1087. doi: 10.1105/tpc.4.9.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Moore B. D., Kobza J., Seemann J. R. Measurement of 2-carboxyarabinitol 1-phosphate in plant leaves by isotope dilution. Plant Physiol. 1991 May;96(1):208–213. doi: 10.1104/pp.96.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pallas J. E., Samish Y. B., Willmer C. M. Endogenous rhythmic activity of photosynthesis, transpiration, dark respiration, and carbon dioxide compensation point of peanut leaves. Plant Physiol. 1974 Jun;53(6):907–911. doi: 10.1104/pp.53.6.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Piechulla B., Gruissem W. Diurnal mRNA fluctuations of nuclear and plastid genes in developing tomato fruits. EMBO J. 1987 Dec 1;6(12):3593–3599. doi: 10.1002/j.1460-2075.1987.tb02690.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Portis A. R., Salvucci M. E., Ogren W. L. Activation of Ribulosebisphosphate Carboxylase/Oxygenase at Physiological CO(2) and Ribulosebisphosphate Concentrations by Rubisco Activase. Plant Physiol. 1986 Dec;82(4):967–971. doi: 10.1104/pp.82.4.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Richards E. J., Ausubel F. M. Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell. 1988 Apr 8;53(1):127–136. doi: 10.1016/0092-8674(88)90494-1. [DOI] [PubMed] [Google Scholar]
  25. Roy H. Rubisco assembly: a model system for studying the mechanism of chaperonin action. Plant Cell. 1989 Nov;1(11):1035–1042. doi: 10.1105/tpc.1.11.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Servaites J. C. Binding of a Phosphorylated Inhibitor to Ribulose Bisphosphate Carboxylase/Oxygenase during the Night. Plant Physiol. 1985 Aug;78(4):839–843. doi: 10.1104/pp.78.4.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shen J. B., Orozco E. M., Jr, Ogren W. L. Expression of the two isoforms of spinach ribulose 1,5-bisphosphate carboxylase activase and essentiality of the conserved lysine in the consensus nucleotide-binding domain. J Biol Chem. 1991 May 15;266(14):8963–8968. [PubMed] [Google Scholar]
  28. Somerville C. R., Portis A. R., Ogren W. L. A Mutant of Arabidopsis thaliana Which Lacks Activation of RuBP Carboxylase In Vivo. Plant Physiol. 1982 Aug;70(2):381–387. doi: 10.1104/pp.70.2.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Streusand V. J., Portis A. R. Rubisco Activase Mediates ATP-Dependent Activation of Ribulose Bisphosphate Carboxylase. Plant Physiol. 1987 Sep;85(1):152–154. doi: 10.1104/pp.85.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vu J. C., Allen L. H., Bowes G. Dark/Light modulation of ribulose bisphosphate carboxylase activity in plants from different photosynthetic categories. Plant Physiol. 1984 Nov;76(3):843–845. doi: 10.1104/pp.76.3.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Werneke J. M., Zielinski R. E., Ogren W. L. Structure and expression of spinach leaf cDNA encoding ribulosebisphosphate carboxylase/oxygenase activase. Proc Natl Acad Sci U S A. 1988 Feb;85(3):787–791. doi: 10.1073/pnas.85.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zerr D. M., Hall J. C., Rosbash M., Siwicki K. K. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci. 1990 Aug;10(8):2749–2762. doi: 10.1523/JNEUROSCI.10-08-02749.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES