Degradation of the light-stress protein is mediated by an ATP-independent, serine-type protease under low-light conditions

European Journal of Biochemistry

Volumn 236, Issue 2, 1996, Pages 591-599

  Adamska, Iwona ^a,b   Lindahl, Marika ^b   Roobol Bóza, Margrit ^b   Andersson, Bertil ^b  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

degradation; light stress protein; protease; recovery; thylakoid membranes

Indexed keywords

HEAT SHOCK PROTEIN; MEMBRANE PROTEIN; PROTEINASE;

ARTICLE; CYTOCHEMISTRY; ENZYME ANALYSIS; PHOTODEGRADATION; PLANT; PRIORITY JOURNAL; THYLAKOID;

PISUM SATIVUM; SATIVUM; VIRIDIPLANTAE;

EID: 0029872716     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.00591.x     Document Type: Article

References (48)

1. Adamska, I. & Kloppstech, K. (1991) Evidence for an association of the early light-inducible protein (ELIP) of pea with photosystem II, Plant Mol. Biol. 16, 209-223.
2. Adamska, I., Ohad, I. & Kloppstech, K. (1992) Synthesis of the early light-inducible protein is controlled by blue light and related to light stress, Proc. Natl Acad Sci. USA 89, 2610-2613.
3. Adamska, I., Kloppstech, K. & Ohad, I. (1993) Early light-inducible protein in pea is stable during light stress hut is degraded during recovery at low light intensity, J. Biol. Chem. 268, 5438-5444.
4. Anastassiou, R. K. & Argyroudi-Akoyunoglou, J. (1992) Thylakoid-bound protease activity as monitored by azo-dye release from azocoll substrate is affected by thylakoid development and chlorophyll synthesis inhibitors, in Regulation of chloroplast biogenesis (Argyroudi-Akoyunoglou, J., ed.) pp. 331-336, Plenum Press, New York and London.
5. Andersson, B. & Åkerlund, H. E. (1987) Proteins of the oxygen-evolving complex, in Topics in photosynthesis (Barber, J., ed.) vol. 8, pp. 380-414, Elsevier Science Publishers, Amsterdam.
6. Andersson, B. & Styring, S. (1991) Photosystem II: molecular organization, function and acclimation, Curr. Top. Bioenerg. 16, 2-21.
7. Argyroudi-Akoyunoglou, J., Bei-Paraskevopoulou, T., Triantaphyllopoulos, K. & Anastassiou, R. K. (1992) Regulation of photosynthetic unit assembly: Regulation of light-harvesting apoprotein transcription, translation and stabilization in thylakoids, in Regulation of chloroplast biogenesis (Argyroudi-Akoyunoglou, J, ed.) pp. 313-321, Plenum Press, New York and London.
8. Aro, E. M., Virgin, I. & Andersson, B. (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover, Biochim. Biophys. Acta 1143, 113-134.
9. Blum, H., Beier, H. & Gross, H. J. (1987), Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels, Electrophoresis 8, 93-99.
10. Bracht, K. & Trebst, A. (1994) Hypothesis on the control of D1 protein turnover by nuclear coded proteins in Chlamydomonas reinhardtii, Z. Naturforsch. 49c, 439-446.
11. Ciechanover, A., Finley, D. & Varshavsky, A. (1984). Ubiquitin dependence of selective protein degradation demonstrated in the mammalian cell cycle mutant ts85, Cell 37, 57-66.
12. Clarke, A., Gustafsson, P. & Lidholm, A. (1994) Identification and expression of the chloroplast clpP gene in the conifer Pinus contorta, Plant Mol. Biol. 26, 851-862.
13. Dalling, M. J. & Nettleton, A. M. (1986) Chloroplast senescence and proteolytic enzymes, in Plant proteolytic enzymes (Dalling, M. J., ed.) vol. 2, pp. 125-153, CRC Press, Boca Raton FL.
14. Finley, D. & Chau, V. (1991) Ubiquitination, Annu. Rev. Cell Biol. 7, 25-69.
15. Goldberg, A. L. (1992), The mechanism and functions of ATP-dependent proteases in bacterial and animal cells, Eur. J. Biochem. 203, 9-23.
16. Gottesman, S., Squires, C., Pichersky, E., Carrington, M., Hobbs, M., Mattick, J. S., Dalrymple, B., Kuramitsu, H., Shirosa, T., Foster, T., Clark, W. P., Ross, B., Squires, C. L. & Maurizi, M. (1990) Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes, Proc. Natl Acad. Sci. USA 87, 3513-3517.
17. Greenberg, B. M., Gaba, V., Mattoo, A. K. & Edelman, M. (1987) Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II, EMBO J. 6, 2865-2869.
18. Grimm, B., Kruse, E. & Kloppstech, K. (1989) Transiently expressed early light-inducible thylakoid proteins share transmembrane domains with light-harvesting chlorophyll binding proteins, Plant Mol. Biol. 13, 583-593.
19. Hatfield, P. M. & Vierstra, R. D. (1992) Multiple forms of ubiquitin activating enzyme (E1) from wheat: identification of an essential cysteine by in vitro mutagenesis, J. Biol. Chem. 267, 14799-14803.
20. Hoober, J. K. & Hughes, M. J. (1992) Purification and characterization of a membrane-bound protease from Chlamydomonas reinhardtii, Plant Physiol. 99, 932-937.
21. Kuwabara, T. & Hashimoto, Y. (1990) Purification of a dithiothreitol-sensitive tetramenric protease from spinach PS II membranes, Plant Cell Physiol. 31, 581-589.
22. Kuwabara, T. (1992) Characterization of a prolyl endopeptidase from spinach thylakoids, FEBS Lett. 300, 127-130.
23. Kuwabara, T. & Suzuki, K. (1992) Degradation of the extrinsic 23-kDa protein of photosystem II induced by p-chloromercuriphenylsulfonic acid, in Research in photosynthesis (Murata, N., ed.) vol. III, pp. 201-204, Kluwer Academic Publishers, Dordrecht.
24. Laemmli, U. K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4, Nature 227, 680-685.
25. Lindahl, M. & Andersson, B. (1992) A proteolytic activity associated with loss of LHC II during accimation of spinach leaves from low to high light, in Research in photosynthesis (Murata, N., ed.) vol. I, pp. 307-310, Kluwer Academic Publishers, Dordrecht.
26. Lindahl, M., Yang, D. H. & Andersson, B. (1995) Regulatory proteolysis of the major light-harvesting chlorophll a/b protein of photosystem II by a light-induced membrane-associated enzymic system, Eur. J. Biochem. 231, 503-509.
27. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) Protein measurements with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
28. Malek, I., Bogorad, I., Ayers, A. & Goldberg, A. L. (1984) Newly synthesized proteins are degraded by an ATP-stimulated proteolytic process in isolated pea chloroplasts, FEBS Lett. 166, 253-255.
29. Maurizi, M. R. (1992) Proteases and protein degradation in Escherichia coli, Experientia 48, 178-201.
30. Maurizi, M. R., Clark, W. P., Kim, S. H. & Gottesman, S. (1990) Clp represents a unique family of serine proteases, J. Biol. Chem. 265, 12546-12552.
31. Merchant, S. & Bogorad, I. (1986) Rapid degradation of apoplastocyanin in Cu(II)-deficient cells of Chlamydomonas reinhardtii, J. Biol. Chem. 261, 15850-15853.
32. Meyer, G. & Kloppstech, K. (1984) A rapidly light-induced chloroplast protein with a high turnover coded for by pea nuclear DNA, Eur. J. Biochem. 138, 201-207.
33. Moore, T. & Keegstra, K. (1993) Characterization of a cDNA clone encoding a chloroplast-targeted Clp homologue, Plant Mol. Biol. 21, 525-537.
34. Mullet, J. E., Klein, P. G. & Klein, R. R. (1990) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability, Proc. Natl Acad. Sci. USA 87, 4038-4042.
35. Pötter, E. & Kloppstech, K. (1993) Effects of light stress on the expression of early light-inducible proteins in barley, Eur. J. Biochem. 214, 779-786.
36. Prasil, O., Adir, N. & Ohad, I. (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery process, Top. Photosynth. 11, 295-348.
37. Regnier, T. E. (1991) Perfusion chromatography, Nature 350, 634-635.
38. Rogers, S., Wells, R. & Rechsteiner, M. (1986) Amino acid sequences common to rapidly degraded proteins: The PEST-hypothesis, Science 234, 364-368.
39. Roobol-Bóza, M., Shochat, S., Tjus, S. E., Hagman, Å., Gast, P. & Andersson, B. (1995) Perfusion chromatography - a new procedure for very rapid isolation of integral photosynthetic membrane proteins, Photosynth. Res. 46, 339-345.
40. Salter, A. H., Virgin, I., Hagmann, Å. & Andersson, B. (1992) On the molecular mechanisms of light induced D1 protein degradation in photosystem II core particles, Biochemistry 31, 3990-3998.
41. Schmidt, G. W. & Mishkind, M. L. (1983) Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunit in chloroplasts, Proc. Natl Acad. Sci. USA 80, 2632-2636.
42. Towbin, H., Staehelin, T. & Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications, Proc. Natl Acad. Sci. USA 76, 4350-4354.
43. Umesono, K. & Ozeki, H. (1987) Chloroplast gene organization in plants, Trends Genet. 3, 281-287.
44. Umezawa, H. & Aoyagi, T. (1983) Trends in research of low molecular mass protease inhibitors of microbial origin, in Proteinase inhibitors: medical and biological aspects (Katsunuma, N., Umezawa, H. & Holzer, H., eds) pp. 3-15, Japan Scientific Societies Press, Tokyo/Springer-Verlag, Berlin.
45. van Nocker, S. & Vierstra, R. D. (1991) Cloning and characterization of a 20-kilodalton ubiquitin carrier protein (E2) from wheat that catalyzes multi-ubiquitin chain formation in vitro, Proc. Natl Acad. Sci. USA 88, 10297-10301.
46. Veierskov, B. & Ferguson, I. B. (1991) Conjugation of ubiquitin to proteins from green plant tissues, J. Plant Physiol. 138, 608-613.
47. Vierstra, R. D. (1993) Protein degradation in plants, Annu. Rev. Plant Mol. Biol. 44, 385-410.
48. Wettern. M., Parag, H. A., Pollmann, L., Ohad, I. & Kulka, R. (1990) Ubiquitin in Chlamydomonas reinhardtii: distribution in the cell and effect of heat shock and photoinhibition on its conjugate pattern, Eur. J. Biochem. 191, 571-576.