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. 1997 Apr;113(4):1167–1175. doi: 10.1104/pp.113.4.1167

Circadian Regulation of Sucrose Phosphate Synthase Activity in Tomato by Protein Phosphatase Activity.

T L Jones 1, D R Ort 1
PMCID: PMC158239  PMID: 12223667

Abstract

Sucrose phosphate synthase (SPS), a key enzyme in sucrose biosynthesis, is regulated by protein phosphorylation and shows a circadian pattern of activity in tomato. SPS is most active in its dephosphorylated state, which normally coincides with daytime. Applying okadaic acid, a potent protein phosphatase inhibitor, prevents SPS activation. More interesting is that a brief treatment with cycloheximide, a cytoplasmic translation inhibitor, also prevents the light activation of SPS without any effect on the amount of SPS protein. Cordycepin, an inhibitor of transcript synthesis and processing, has the same effect. Both of these inhibitors also prevent the activation phase of the circadian rhythm in SPS activity. Conversely, cycloheximide and cordycepin do not prevent the decline in circadian SPS activity that normally occurs at night. These observations indicate that SPS phosphatase activity but not SPS kinase activity is controlled, directly or indirectly, at the level of gene expression. Taken together, these data imply that there is a circadian rhythm controlling the transcription of a protein phosphatase that subsequently dictates the circadian rhythm in SPS activity via effects on this enzyme's phosphorylation state.

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Selected References

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  1. Anderson S. L., Kay S. A. Functional dissection of circadian clock- and phytochrome-regulated transcription of the Arabidopsis CAB2 gene. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1500–1504. doi: 10.1073/pnas.92.5.1500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cline M. G., Rehm M. M. Rapid Inhibition of Auxin-induced Elongation of Avena Coleoptile Segments by Cordycepin. Plant Physiol. 1974 Aug;54(2):160–163. doi: 10.1104/pp.54.2.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Comolli J., Taylor W., Rehman J., Hastings J. W. Inhibitors of serine/threonine phosphoprotein phosphatases alter circadian properties in Gonyaulax polyedra. Plant Physiol. 1996 May;111(1):285–291. doi: 10.1104/pp.111.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cooper P., Ort D. R. Changes in protein synthesis induced in tomato by chilling. Plant Physiol. 1988 Oct;88(2):454–461. doi: 10.1104/pp.88.2.454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Duncan R. F. Cordycepin blocks recovery of non-heat-shock mRNA translation following heat shock in Drosophila. Eur J Biochem. 1995 Nov 1;233(3):784–792. doi: 10.1111/j.1432-1033.1995.784_3.x. [DOI] [PubMed] [Google Scholar]
  6. Galtier N., Foyer C. H., Huber J., Voelker T. A., Huber S. C. Effects of Elevated Sucrose-Phosphate Synthase Activity on Photosynthesis, Assimilate Partitioning, and Growth in Tomato (Lycopersicon esculentum var UC82B). Plant Physiol. 1993 Feb;101(2):535–543. doi: 10.1104/pp.101.2.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Graan T., Ort D. R. Quantitation of the rapid electron donors to P700, the functional plastoquinone pool, and the ratio of the photosystems in spinach chloroplasts. J Biol Chem. 1984 Nov 25;259(22):14003–14010. [PubMed] [Google Scholar]
  8. Hennessey T. L., Field C. B. Circadian Rhythms in Photosynthesis : Oscillations in Carbon Assimilation and Stomatal Conductance under Constant Conditions. Plant Physiol. 1991 Jul;96(3):831–836. doi: 10.1104/pp.96.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hennessey T. L., Field C. B. Evidence of multiple circadian oscillators in bean plants. J Biol Rhythms. 1992 Summer;7(2):105–113. doi: 10.1177/074873049200700202. [DOI] [PubMed] [Google Scholar]
  10. Huber J. L., Huber S. C., Nielsen T. H. Protein phosphorylation as a mechanism for regulation of spinach leaf sucrose-phosphate synthase activity. Arch Biochem Biophys. 1989 May 1;270(2):681–690. doi: 10.1016/0003-9861(89)90551-1. [DOI] [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. Kondo T., Strayer C. A., Kulkarni R. D., Taylor W., Ishiura M., Golden S. S., Johnson C. H. Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5672–5676. doi: 10.1073/pnas.90.12.5672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Li B., Geiger D. R., Shieh W. J. Evidence for circadian regulation of starch and sucrose synthesis in sugar beet leaves. Plant Physiol. 1992 Aug;99(4):1393–1399. doi: 10.1104/pp.99.4.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Martin B., Ort D. R., Boyer J. S. Impairment of photosynthesis by chilling-temperatures in tomato. Plant Physiol. 1981 Aug;68(2):329–334. doi: 10.1104/pp.68.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Martino-Catt S. J., Jones T. L., Ort D. R. In vivo pulse labeling of proteins in attached leaves with radioactive amino acids. Anal Biochem. 1993 Jun;211(2):188–196. doi: 10.1006/abio.1993.1255. [DOI] [PubMed] [Google Scholar]
  17. Martino-Catt S., Ort D. R. Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3731–3735. doi: 10.1073/pnas.89.9.3731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mumby M. C., Walter G. Protein serine/threonine phosphatases: structure, regulation, and functions in cell growth. Physiol Rev. 1993 Oct;73(4):673–699. doi: 10.1152/physrev.1993.73.4.673. [DOI] [PubMed] [Google Scholar]
  19. Otto B., Grimm B., Ottersbach P., Kloppstech K. Circadian Control of the Accumulation of mRNAs for Light- and Heat-Inducible Chloroplast Proteins in Pea (Pisum sativum L.). Plant Physiol. 1988 Sep;88(1):21–25. doi: 10.1104/pp.88.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Piechulla B. 'Circadian clock' directs the expression of plant genes. Plant Mol Biol. 1993 Jun;22(3):533–542. doi: 10.1007/BF00015982. [DOI] [PubMed] [Google Scholar]
  21. Ramalho C. B., Hastings J. W., Colepicolo P. Circadian oscillation of nitrate reductase activity in Gonyaulax polyedra is due to changes in cellular protein levels. Plant Physiol. 1995 Jan;107(1):225–231. doi: 10.1104/pp.107.1.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Salvucci M. E., Drake R. R., Haley B. E. Purification and photoaffinity labeling of sucrose phosphate synthase from spinach leaves. Arch Biochem Biophys. 1990 Sep;281(2):212–218. doi: 10.1016/0003-9861(90)90434-z. [DOI] [PubMed] [Google Scholar]
  23. Siegl G., MacKintosh C., Stitt M. Sucrose-phosphate synthase is dephosphorylated by protein phosphatase 2A in spinach leaves. Evidence from the effects of okadaic acid and microcystin. FEBS Lett. 1990 Sep 17;270(1-2):198–202. doi: 10.1016/0014-5793(90)81267-r. [DOI] [PubMed] [Google Scholar]
  24. Sonnewald U., Quick W. P., MacRae E., Krause K. P., Stitt M. Purification, cloning and expression of spinach leaf sucrose-phosphate synthase in Escherichia coli. Planta. 1993 Feb;189(2):174–181. doi: 10.1007/BF00195074. [DOI] [PubMed] [Google Scholar]
  25. Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun. 1986 Mar 13;135(2):397–402. doi: 10.1016/0006-291x(86)90008-2. [DOI] [PubMed] [Google Scholar]
  26. Tavladoraki P., Kloppstech K., Argyroudi-Akoyunoglou J. Circadian Rhythm in the Expression of the mRNA Coding for the Apoprotein of the Light-Harvesting Complex of Photosystem II : Phytochrome Control and Persistent Far Red Reversibility. Plant Physiol. 1989 Jun;90(2):665–672. doi: 10.1104/pp.90.2.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Verwoerd T. C., Dekker B. M., Hoekema A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989 Mar 25;17(6):2362–2362. doi: 10.1093/nar/17.6.2362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Walker J. L., Huber S. C. Purification and preliminary characterization of sucrose-phosphate synthase using monoclonal antibodies. Plant Physiol. 1989 Feb;89(2):518–524. doi: 10.1104/pp.89.2.518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weiner H., McMichael R. W., Huber S. C. Identification of factors regulating the phosphorylation status of sucrose-phosphate synthase in vivo. Plant Physiol. 1992 Aug;99(4):1435–1442. doi: 10.1104/pp.99.4.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Weiner H., Weiner H., Stitt M. Sucrose-phosphate synthase phosphatase, a type 2A protein phosphatase, changes its sensitivity towards inhibition by inorganic phosphate in spinach leaves. FEBS Lett. 1993 Oct 25;333(1-2):159–164. doi: 10.1016/0014-5793(93)80396-c. [DOI] [PubMed] [Google Scholar]
  31. Worrell A. C., Bruneau J. M., Summerfelt K., Boersig M., Voelker T. A. Expression of a maize sucrose phosphate synthase in tomato alters leaf carbohydrate partitioning. Plant Cell. 1991 Oct;3(10):1121–1130. doi: 10.1105/tpc.3.10.1121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zhong H. H., Young J. C., Pease E. A., Hangarter R. P., McClung C. R. Interactions between Light and the Circadian Clock in the Regulation of CAT2 Expression in Arabidopsis. Plant Physiol. 1994 Mar;104(3):889–898. doi: 10.1104/pp.104.3.889. [DOI] [PMC free article] [PubMed] [Google Scholar]

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