The BSD2 ortholog in Chlamydomonas reinhardtii is a polysome-associated chaperone that co-migrates on sucrose gradients with the rbcL transcript encoding the Rubisco large subunit

Plant Journal

Volumn 80, Issue 2, 2014, Pages 345-355

  Doron, Lior ^a   Segal, Na'ama ^a   Gibori, Hadas ^a,b   Shapira, Michal ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

BSD 2; Chaperone; Chlamydomonas; Oxidative stress; Rubisco; Translation

Indexed keywords

TRANSLATION (LANGUAGES);

BSD-2; CHAPERONE; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; ORTHOLOGS; RUBISCO; SUCROSE GRADIENTS;

OXIDATIVE STRESS;

CHAPERONE; MESSENGER RNA; RIBULOSEBISPHOSPHATE CARBOXYLASE; SUCROSE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; CHEMISTRY; CHLAMYDOMONAS REINHARDTII; GENETICS; METABOLISM; MOLECULAR GENETICS; OXIDATIVE STRESS; POLYSOME; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CHLAMYDOMONAS REINHARDTII; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PLANT PROTEINS; POLYRIBOSOMES; RIBULOSE-BISPHOSPHATE CARBOXYLASE; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SUCROSE;

EID: 84908117556     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12638     Document Type: Article

References (43)

1. Banecki, B., Liberek, K., Wall, D., Wawrzynow, A., Georgopoulos, C., Bertoli, E., Tanfani, F. and Zylicz, M. (1996) Structure-function analysis of the zinc finger region of the DnaJ molecular chaperone. J. Biol. Chem. 271, 14840-14848.
2. Barneche, F., Winter, V., Crevecoeur, M. and Rochaix, J.D. (2006) ATAB 2 is a novel factor in the signalling pathway of light-controlled synthesis of photosystem proteins. EMBO J. 25 5907-5918.
3. Belknap, W.R. (1983) Partial purification of intact chloroplasts from Chlamydomonas reinhardtii. Plant Physiol. 72, 1130-1132.
4. Brutnell, T.P., Sawers, R.J., Mant, A. and Langdale, J.A. (1999) BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell, 11, 849-864.
5. Cheng, Y. and Patel, D.J. (2004) An efficient system for small protein expression and refolding. Biochem. Biophys. Res. Commun. 317, 401-405.
6. Cohen, I., Knopf, J.A., Irihimovitch, V. and Shapira, M. (2005) A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression. Plant Physiol. 137, 738-746.
7. Cohen, I., Sapir, Y. and Shapira, M. (2006) A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms. Plant Physiol. 141, 1089-1097.
8. Danon, A. and Mayfield, S.P. (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J. 10, 3993-4001.
9. Ellis, R.J. (1990) The molecular chaperone concept. Semin. Cell Biol. 1, 1-9.
10. Feiz, L., Williams-Carrier, R., Wostrikoff, K., Belcher, S., Barkan, A. and Stern, D.B. (2012) Ribulose-1,5-bis-phosphate carboxylase/oxygenase accumulation factor1 is required for holoenzyme assembly in maize. Plant Cell, 24, 3435-3446.
11. Gatenby, A.A. and Ellis, R.J. (1990) Chaperone function: the assembly of ribulose biphosphate carboxylase-oxygenase. Annu. Rev. Cell Biol. 6, 125-149.
12. Goldschmidt-Clermont, M., Malnoe, P. and Rochaix, J.D. (1989) Preparation of Chlamydomonas chloroplasts for the in vitro import of polypeptide precursors. Plant Physiol. 89, 15-18.
13. Gong, H. and Ohad, I. (1995) Rapid turnover of the RCII-D1 protein in the dark induced by photoinactivation of Photosystem II in Scenedesmus wild type and the PS-II-donor defective LF-1 mutant cells. Biochim. Biophys. Acta 1228, 181-188.
14. Halperin, T. and Adam, Z. (1996) Degradation of mistargeted OEE33 in the chloroplast stroma. Plant Mol. Biol. 30, 925-933.
15. Holmgren, A. (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J. Biol. Chem. 254, 9627-9632.
16. Irihimovitch, V. and Shapira, M. (2000) Glutathione redox potential modulated by reactive oxygen species regulates translation of Rubisco large subunit in the chloroplast. J. Biol. Chem. 275, 16289-16295.
17. Jensen, K.H., Herrin, D.L., Plumley, F.G. and Schmidt, G.W. (1986) Biogenesis of photosystem II complexes: transcriptional, translational, and posttranslational regulation. J. Cell Biol. 103, 1315-1325.
18. Klein, R.R., Mason, H.S. and Mullet, J.E. (1988) Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA, and rbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J. Cell Biol. 106, 289-301.
19. Liu, C., Young, A.L., Starling-Windhof, A. et al. (2010) Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 463, 197-202.
20. Martin, J. and Hartl, F.U. (1997) Chaperone-assisted protein folding. Curr. Opin. Struct. Biol. 7, 41-52.
21. McCarty, J.S., Buchberger, A., Reinstein, J. and Bukau, B. (1995) The role of ATP in the functional cycle of the DnaK chaperone system. J. Mol. Biol. 249, 126-137.
22. Moerke, N.J., Aktas, H., Chen, H. et al. (2007) Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128, 257-267.
23. Moreno, J., Garcia-Murria, M.J. and Marin-Navarro, J. (2008) Redox modulation of Rubisco conformation and activity through its cysteine residues. J. Exp. Botany 59, 1605-1614.
24. Nordhues, A., Miller, S.M., Muhlhaus, T. and Schroda, M. (2010) New insights into the roles of molecular chaperones in Chlamydomonas and Volvox. Int. Rev. Cell Mol. Biol. 285, 75-113.
25. Prásil, O., Adir, N. and Ohad, I. (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In The Photosystems: Structure, Function and Molecular Biology (Barber, J. ed.). Amsterdam: Elsevier, pp. 295-348.
26. Ranty, B., Lorimer, G. and Gutteridge, S. (1991) An intra-dimeric crosslink of large subunits of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase is formed by oxidation of cysteine 247. Eur. J. Biochem. FEBS 200, 353-358.
27. Rochaix, J.D., Kuchka, M., Mayfield, S., Schirmer-Rahire, M., Girard-Bascou, J. and Bennoun, P. (1989) Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 8, 1013-1021.
28. Ryle, A.P., Sanger, F., Smith, L.F. and Kitai, R. (1955) The disulphide bonds of insulin. Biochem. J. 60, 541-556.
29. Saschenbrecker, S., Bracher, A., Rao, K.V., Rao, B.V., Hartl, F.U. and Hayer-Hartl, M. (2007) Structure and function of RbcX, an assembly chaperone for hexadecameric Rubisco. Cell, 129, 1189-1200.
30. Schottkowski, M., Peters, M., Zhan, Y., Rifai, O., Zhang, Y. and Zerges, W. (2012) Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 109, 19286-19291.
31. Schreuder, H.A., Knight, S., Curmi, P.M., Andersson, I., Cascio, D., Sweet, R.M., Branden, C.I. and Eisenberg, D. (1993) Crystal structure of activated tobacco rubisco complexed with the reaction-intermediate analogue 2-carboxy-arabinitol 1,5-bisphosphate. Protein Sci. 2, 1136-1146.
32. Shalgi, R., Hurt, J.A., Krykbaeva, I., Taipale, M., Lindquist, S. and Burge, C.B. (2012) Widespread regulation of translation by elongation pausing in heat shock. Mol. Cell 49, 439-452.
33. Shapira, M., Lers, A., Heifetz, P., Yrihimovitz, V., Osmond, B.C., Gillham, N.W. and Boynton, J.E. (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PSII D1 protein. Plant Mol. Biol. 33, 1001-1011.
34. Sheffield, P., Garard, S. and Derewenda, Z. (1999) Overcoming expression and purification problems of RhoGDI using a family of TMParallel expression vectors. Prot. Exp. Purif. 15, 34-39.
35. Shi, Y.Y., Tang, W., Hao, S.F. and Wang, C.C. (2005) Contributions of cysteine residues in Zn2 to zinc fingers and thiol-disulfide oxidoreductase activities of chaperone DnaJ. Biochemistry 44, 1683-1689.
36. Spreitzer, R.J. (1993) Genetic dissection of Rubisco structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 1-49.
37. Spreitzer, R.J., Goldschmidt-Clermont, M., Rahire, M. and Rochaix, J.D. (1985) Nonsense mutations in the Chlamydomonas chloroplast gene that codes for the large subunit of ribulosebisphosphate carboxylase/oxygenase. Proc. Natl Acad. Sci. USA 82, 5460-5464.
38. Szabo, A., Korszun, R., Hartl, F.U. and Flanagan, J. (1996) A zinc finger-like domain of the molecular chaperone DnaJ is involved in binding to denatured protein substrates. EMBO J. 15, 408-417.
39. Tang, W. and Wang, C.C. (2001) Zinc fingers and thiol-disulfide oxidoreductase activities of chaperone DnaJ. Biochemistry 40, 14985-14994.
40. Willmund, F., Dorn, K.V., Schulz-Raffelt, M. and Schroda, M. (2008) The chloroplast DnaJ homolog CDJ1 of Chlamydomonas reinhardtii is part of a multichaperone complex containing HSP70B, CGE1, and HSP90C. Plant Physiol. 148, 2070-2082.
41. Wostrikoff, K. and Stern, D. (2007) Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc. Natl Acad. Sci. USA 104, 6466-6471.
42. Wostrikoff, K., Clark, A., Sato, S., Clemente, T. and Stern, D. (2012) Ectopic expression of Rubisco subunits in maize mesophyll cells does notovercome barriers to cell type-specific accumulation. Plant Physiol. 160, 419-432.
43. Yosef, I., Irihimovitch, V., Knopf, J.A., Cohen, I., Orr-Dahan, I., Nahum, E., Keasar, C. and Shapira, M. (2004) RNA binding activity of the ribulose- 1,5-bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. J. Biol. Chem. 279, 10148-10156.