Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40

Plant Cell

Volumn 19, Issue 11, 2007, Pages 3627-3639

  Schwarz, Christian ^a   Elles, Ingolf ^a   Kortmann, Jens ^a   Piotrowski, Markus ^b   Nickelsen, Jörg ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BINDING SITES; BIOSYNTHESIS; ELECTROPHORESIS; GENE EXPRESSION; RNA;

BINDING PROTEIN; CHLOROPLASTS; POLYACRYLAMIDE GEL ELECTROPHORESIS; POSTTRANSCRIPTIONAL LEVEL;

PROTEINS;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

EID: 37849006499     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.051722     Document Type: Article

References (38)

1. Auchincloss, A.H., Zerges, W., Perron, K., Girard-Bascou, J., and Rochaix, J.D. (2002). Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii. J. Cell Biol. 157: 953-962.
2. Barkan, A., Walker, M., Nolasco, M., and Johnson, D. (1994). A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 13: 3170-3181.
3. Barneche, F., Winter, V., Crevecoeur, M., and Rochaix, J.-D. (2006). ATAB2 is a novel factor in the signalling pathway of light-controlled synthesis of photosystem proteins. EMBO J. 25: 5907-5918.
4. Barnes, D., Cohen, A., Bruick, R.K., Kantardjieff, K., Fowler, S., Efuet, E., and Mayfield, S.P. (2004). Identification and characterization of a novel RNA binding protein that associates with the 5′ untranslated region of the chloroplast psbA mRNA. Biochemistry 43: 8541-8550.
5. Boudreau, E., Nickelsen, J., Lemaire, S.D., Ossenbuhl, F., and Rochaix, J.D. (2000). The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J. 19: 3366-3376.
6. Bruick, R.K., and Mayfield, S.P. (1999). Light-activated translation of chloroplast mRNAs. Trends Plant Sci. 4: 190-195.
7. Danon, A., and Mayfield, S.P. (1991). Light regulated translational activators: Identification of chloroplast gene-specific mRNA binding proteins. EMBO J. 10: 3993-4001.
8. Danon, A., and Mayfield, S.P. (1994). Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266: 1717-1719.
9. Dauvillee, D., Stampacchia, O., Girard-Bascou, J., and Rochaix, J.D. (2003). Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA. EMBO J. 22: 6378-6388.
10. de Vitry, C., Olive, J., Drapier, D., Recouvreur, M., and Wollman, F.A. (1989). Posttranslational events leading to the assembly of photosystem II protein complex: A study using photosynthesis mutants from Chlamydomonas reinhardtii. J. Cell Biol. 109: 991-1006.
11. Harris, E.H. (1989). The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. (San Diego, CA: Academic Press).
12. Higgs, D.C., Shapiro, R.S., Kindle, K.L., and Stern, D.B. (1999). Small cis-acting sequences that specify secondary structures in a chloroplast mRNA are essential for RNA stability and translation. Mol. Cell. Biol. 19: 8479-8491.
13. Hirose, T., and Sugiura, M. (1996). Cis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: Development of an in vitro translation system from tobacco chloroplasts. EMBO J. 15: 1687-1695.
14. Kim, J., and Mayfield, S.P. (1997). Protein disulphide isomerase as a regulator of chloroplast translational activation. Science 278: 1954-1957.
15. Klinkert, B., Elles, I., and Nickelsen, J. (2006). Translation of chloroplast psbD mRNA in Chlamydomonas is controlled by a secondary RNA structure blocking the AUG start codon. Nucleic Acids Res. 34: 386-394.
16. Komenda, J., Reisinger, V., Muller, B.C., Dobakova, M., Granvogl, B., and Eichacker, L.A. (2004). Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J. Biol. Chem. 279: 48620-48629.
17. Kuchka, M.R., Goldschmidt-Clermont, M., van Dillewijn, J., and Rochaix, J.-D. (1989). Mutation of the Chlamydomonas nuclear Nac2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 58: 869-876.
18. Kuchka, M.R., Mayfield, S.P., and Rochaix, J.-D. (1988). Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii. EMBO J. 7: 319-324.
19. Manuell, A., Beligni, M.V., Yamaguchi, K., and Mayfield, S.P. (2004). Regulation of chloroplast translation: Interactions of RNA elements, RNA-binding proteins and the plastid ribosome. Biochem. Soc. Trans. 32: 601-605.
20. Minai, L., Wostrikoff, K., Wollman, F.A., and Choquet, Y. (2006). Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 18: 159-175.
21. Mussgnug, J.H., et al. (2005). NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17: 3409-3421.
22. Nickelsen, J. (2000). Mutations at three different nuclear loci of Chlamydomonas suppress a defect in chloroplast psbD mRNA accumulation. Curr. Genet. 37: 136-142.
23. Nickelsen, J. (2003). Chloroplast RNA-binding proteins. Curr. Genet. 43: 392-399.
24. Nickelsen, J., Fleischmann, M., Boudreau, E., Rahire, M., and Rochaix, J.-D. (1999). Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell 11: 957-970.
25. Nickelsen, J., van Dillewijn, J., Rahire, M., and Rochaix, J.-D. (1994). Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J. 13: 3182-3191.
26. Ossenbühl, F., and Nickelsen, J. (2000). Cis- and trans-acting determinants for translation of psbD mRNA in Chlamydomonas reinhardtii. Mol. Cell. Biol. 20: 8134-8142.
27. Piotrowski, M., and Volmer, J.J. (2006). Cyanide metabolism in higher plants: Cyanoalanine hydratase is a NIT4 homolog. Plant Mol. Biol. 61: 111-122.
28. Rohr, J., Sarkar, N., Balenger, S., Jeong, B.R., and Cerutti, H. (2004). Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas. Plant J. 40: 611-621.
29. Sane, A.P., Stein, B., and Westhoff, P. (2005). The nuclear gene HCF107 encodes a membrane-associated R-TPR (RNA tetratricopeptide repeat)-containing protein involved in expression of the plastidial psbH gene in Arabidopsis. Plant J. 42: 720-730.
30. Schmitz-Linneweber, C., Williams-Carrier, R., and Barkan, A. (2005). RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5′ region of mRNAs whose translation it activates. Plant Cell 17: 2791-2804.
31. Schult, K., Meierhoff, K., Paradies, S., Töller, T., Wolff, P., and Westhoff, P. (2007). The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19: 1329-1346.
32. Somanchi, A., Barnes, D., and Mayfield, S.P. (2005). A nuclear gene of Chlamydomonas reinhardtii, Tba1, encodes a putative oxidoreductase required for translation of the chloroplast psbA mRNA. Plant J. 42: 341-352.
33. Uniacke, J., and Zerges, W. (2007). Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell 19: 3640-3654.
34. Yohn, C.B., Cohen, A., Danon, A., and Mayfield, S.P. (1998a). A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc. Natl. Acad. Sci. USA 95: 2238-2243.
35. Yohn, C.B., Cohen, A., Rosch, C., Kuchka, M.R., and Mayfield, S.P. (1998b). Translation of the chloroplast psbA mRNA requires the nuclearencoded poly(A) binding protein RB47. J. Cell Biol. 142: 435-442.
36. Yukawa, M., Kuroda, H., and Sugiura, M. (2007). A new in vitro translation system for non-radioactive assay from tobacco chloroplasts: Effect of pre-mRNA processing on translation in vitro. Plant J. 49: 367-376.
37. Zerges, W. (2000). Translation in chloroplasts. Biochimie 82: 583-601.
38. Zerges, W., and Rochaix, J.D. (1998). Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J. Cell Biol. 140: 101-110.