A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana

EMBO Journal

Volumn 17, Issue 18, 1998, Pages 5286-5297

  Meurer, Jörg ^a,b   Plücken, Henning ^a   Kowallik, Klaus V ^a   Westhoff, Peter ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Arabidopsis; High chlorophyll fluorescence mutants; Nuclear regulator gene; Photosystem II assembly

Indexed keywords

CYCLOHEXIMIDE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; CONTROLLED STUDY; CYANOBACTERIUM; GENE ISOLATION; IMMUNOBLOTTING; MUTANT; NONHUMAN; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN STABILITY; THYLAKOID;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPHYLL; CHLOROPLASTS; CLONING, MOLECULAR; CYANOBACTERIA; EVOLUTION, MOLECULAR; GENES, PLANT; GENETIC COMPLEMENTATION TEST; LIGHT-HARVESTING PROTEIN COMPLEXES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; RNA, MESSENGER; RNA, PLANT; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CHLOROPHYTA; CHROMOPHYTA; CYANOBACTERIA; CYANOPHORA PARADOXA; EUKARYOTA; PROKARYOTA; STREPTOPHYTA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 0344404400     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.18.5286     Document Type: Article

References (68)

1. Altamura, N., Capitanio, N., Bonnefoy, N., Papa, S. and Dujardin, G. (1996) The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase. FEBS Lett., 382, 111-115.
2. Altschul, S.F., Boguski, M.S., Gish, W. and Wootton, J.C. (1994) Issues in searching molecular sequence databases. Nature Genet., 6, 119-129.
3. Anderson, J.M. (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Annu. Rev. Plant Physiol., 37, 93-136.
4. Bartsevich, V.V. and Pakrasi, H.B. (1997) Molecular identification of a novel protein that regulates biogenesis of photosystem I. A membrane protein complex. J. Biol. Chem., 272, 6382-6387.
5. Blum, H., Beier, H. and Gross, H.J. (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis, 8, 93-99.
6. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M. and Rochaix, J.D. (1997) The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J., 16, 6095-6104.
7. Brent, R. and Finley, R.L., Jr (1997) Understanding gene and allele function with two-hybrid methods. Annu. Rev. Genet., 31, 663-704.
8. Chen, E.Y. and Seeburg, P.H. (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA, 4, 165-170.
9. Cline, K., Andrews, J., Mersey, B., Newcomb, E.H. and Keegstra, K. (1981) Separation and characterization of inner and outer envelope membranes of pea chloroplasts. Proc. Natl Acad. Sci. USA, 78, 3595-3599.
10. Cline, K., Werner-Washburne, M., Lubben, T.H. and Keegstra, K. (1984) Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol., 75, 675-678.
11. 559 of oxygenic photosynthesis. Physiol. Plant., 88, 705-711.
12. Danon, A. and Mayfield, S.P.Y. (1991) Light-regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J., 10, 3993-4001.
13. Danon, A. and Mayfield, S.P. (1994) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science, 266, 1717-1719.
14. Dellaporta, S.L., Wood, J. and Hicks, J.B. (1983) A plant DNA minipreparation: version II. Plant Mol. Biol. Rep., 1, 19-21.
15. Feldmann, K.A. (1991) T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant J., 1, 71-82.
16. Glerum, D.M., Koerner, T.J. and Tzagoloff, A. (1995) Cloning and characterization of COX14, whose product is required for assembly of yeast cytochrome oxidase. J. Biol. Chem., 270, 15585-15590.
17. Glerum, D.M., Muroff, I., Jin, C. and Tzagoloff, A. (1997) COX15 codes for a mitochondrial protein essential for the assembly of yeast cytochrome oxidase. J. Biol. Chem., 272, 19088-19094.
18. Guenther, J.E. and Melis, A. (1990) The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynth. Res., 23, 105-109.
19. Hankamer, B., Barber, J. and Boekema, E.J. (1997) Structure and membrane organization of photosystem II in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 48, 641-671.
20. Henikoff, S. (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene, 28, 351-359.
21. Kim, J., Klein, P.G. and Mullet, J.E. (1994) Synthesis and turnover of photosystem II reaction center protein D1. Ribosome pausing increases during chloroplast development. J. Biol. Chem., 269, 17918-17923.
22. Koncz, C., Martini, N., Szabados, L., Hrouda, M., Bachmair, A. and Schell, J. (1994) Specialized vectors for gene tagging and expression studies. In Gelvin, S.B. and Schilperoort, R.A. (eds), Plant Molecular Biology Manual. Vol. B2. Kluwer Academic Publishers, Dordrecht, pp. 1-22.
23. Krause, G.H. and Weis, E. (1991) Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol., 42, 313-349.
24. Krugh, B.K. and Miles, D. (1995) Energy transfer for low temperature fluorescence in PS II mutant thylakoids. Photosynth. Res., 44, 117-125.
25. Kubicki, A., Funk, E., Westhoff, P. and Steinmüller, K. (1996) Differential expression of plastome-encoded ndh-genes in mesophyll and bundle sheath chloroplasts of the C4-plant Sorghum bicolor indicates that the complex I-homologous NAD (P)H-plastoquinone-oxidoreductase is involved in cyclic electron transport. Planta, 199, 276-281.
26. Kuchka, M.R., Goldschmidt-Clermont, M., van Dillewijn, J. and Rochaix, J.-D. (1989) Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell, 58, 869-876.
27. Künstner, P., Guardiola, A., Takahashi, Y. and Rochaix, J.-D. (1995) A mutant strain of Chlamydomonas reinhardtii lacking the chloroplast photosystem II psbI gene grows photoautotrophically. J. Biol. Chem., 270, 9651-9654.
28. Laskey, R.A. (1980) The use of intensifying screens or organic scintillators for visualizing radioactive molecules resolved by gel electrophoresis. Methods Enzymol., 65, 363-371.
29. Liu, X.L. and DeMoss, J.A. (1997) Characterization of NarJ, a system-specific chaperone required for nitrate reductase biogenesis in Escherichia coli. J. Biol. Chem., 272, 24266-24271.
30. Lutcke, H.A., Chow, F.S., Mickel, K.F.S., Moss, K.A., Kern, H.F. and Scheele, G.A. (1987) Selection of AUG initiation codon differs in plants and animals. EMBO J., 6, 43-48.
31. Mans, R.J. and Novelli, G.D. (1961) Measurement of the incorporation of radioactive amino acids into protein by a filter-paper disk method. Arch. Biochem. Biophys., 94, 48-53.
32. Marshall, J.S., DeRocher, A.E., Keegstra, K. and Vierling, E. (1990) Identification of heat shock protein hsp70 homologues in chloroplasts. Proc. Natl Acad. Sci. USA, 87, 374-378.
33. Mayfield, S.P., Bennoun, P. and Rochaix, J.D. (1987) Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J., 6, 313-318.
34. Mayfield, S.P., Yohn, C.B., Cohen, A. and Danon, A. (1995) Regulation of chloroplast gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol., 46, 147-166.
35. Melis, A. (1991) Dynamics of photosynthetic membrane composition and function. Biochim. Biophys. Acta Bio-Energetics, 1058, 87-106.
36. Meurer, J., Berger, A. and Westhoff, P. (1996a) A nuclear mutant of Arabidopsis with impaired stability on distinct transcripts of the plastid psbB, psbD/C, ndhH and ndhC operons. Plant Cell, 8, 1193-1207.
37. Meurer, J., Meierhoff, K. and Westhoff, P. (1996b) Isolation of high-chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterisation by spectroscopy, immunoblotting and Northern hybridisation. Planta, 198, 385-396.
38. Miles, D. (1982) The use of mutations to probe photosynthesis in higher plants. In Edelman, M., Hallick, R. and Chua, N.-H. (eds), Methods in Chloroplast Molecular Biology. Elsevier Biomedical Press, Amsterdam, The Netherlands, pp. 75-107.
39. Monod, C., Takahashi, Y., Goldschmidt-Clermont, M. and Rochaix, J.-D. (1994) The chloroplast ycf8 open reading frame encodes a photosystem II polypeptide which maintains photosynthetic activity under adverse growth conditions. EMBO J., 13, 2747-2754.
40. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant., 15, 473-197.
41. Ochman, H., Ayala, F.J. and Hartl, D.L. (1993) Use of polymerase chain reaction to amplify segments outside boundaries of known sequences. Methods Enzymol., 218, 309-321.
42. Oswald, A., Streubel, M., Ljungberg, U., Hermans, J., Eskins, K. and Westhoff, P. (1990) Differential biogenesis of photosystem II in mesophyll and bundle sheath cells of NADP malic enzyme-type C4 plants. A comparative protein and RNA analysis. Eur. J. Biochem., 190, 185-194.
43. 559 protein inactivates the reaction center of photosystem II. Plant Cell, 1, 591-597.
44. 559 affects the stability of the photosystem II complex. EMBO J., 10, 1619-1627.
45. Rhee, K.-H., Morris, E.P., Zheleva, D., Hankamer, B., Kühlbrandt, W. and Barber, J. (1997) Two dimensional structure of plant photosystem II at 8 Å resolution. Nature, 389, 522-526.
46. Robinson, C. and Mant, A. (1997) Targeting of proteins into and across the thylakoid membrane. Trends Plant Sci., 2, 431-437.
47. Rochaix, J.-D. (1992) Post-transcriptional steps in the expression of chloroplast genes. Annu. Rev. Cell Biol., 8, 1-28.
48. Rochaix, J.D. (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu. Rev. Genet., 29, 209-230.
49. Schlicher, T. and Soll, J. (1997) Chloroplastic isoforms of DnaJ and GrpE in pea. Plant Mol. Biol., 33, 181-185.
50. Schuster, G., Ohad, I., Martineau, B. and Taylor, W.C. (1985) Differentiation and development of bundle sheath and mesophyll thylakoids in maize. Thylakoid polypeptide composition, phosphorylation and organization of photosystem II. J. Biol. Chem., 260, 11866-11873.
51. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem., 166, 368-379.
52. 559 accumulate in appressed thylakoids. Biochim. Biophys. Acta, 975, 164-174.
53. Strizhov, N., Keller, M., Mathur, J., Koncz-Kálmán, Z., Bosch, D., Prudovsky, E., Schell, J., Sneh, B., Koncz, C. and Zilberstein, A. (1996) A synthetic cryIC gene, encoding a Bacillus thuringiensis δ-endotoxin, confers Spodoptera resistance in alfalfa and tobacco. Proc. Natl Acad. Sci. USA, 93, 15012-15017.
54. Suzuki, C.K., Rep, M., Van Dijl, J.M., Suda, K., Grivell, L.A. and Schatz, G. (1997) ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem. Sci., 22, 118-123.
55. Takahashi, Y., Matsumoto, H., Goldschmidt-Clermont, M. and Rochaix, J.-D. (1994) Directed disruption of the Chlamydomonas chloroplast psbK gene destabilizes the photosystem II reaction center complex. Plant Mol. Biol., 24, 779-788.
56. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
57. Tzagoloff, A., Yue, J., Jang, J. and Paul, M.F. (1994) A new member of a family of ATPases is essential for assembly of mitochondrial respiratory and ATP synthase complexes in Saccharomyces cerevisiae. J. Biol. Chem., 269, 26144-26151.
58. Valvekens, D., van Montagu, M. and van Lijsebettens, M. (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl Acad. Sci. USA, 85, 5536-5540.
59. Van Wijk, K.J. Andersson, B. and Aro, E.M. (1996) Kinetic resolution of the incorporation of the D1 protein into photosystem II and localization of assembly intermediates in thylakoid membranes of spinach chloroplasts. J. Biol. Chem., 271, 9627-9636.
60. Viitanen, P.V., Schmidt, M., Buchner, J., Suzuki, T., Vierling, E., Dickson, R., Lorimer, G.H., Gatenby, A. and Soll, J. (1995) Functional characterization of the higher plant chloroplast chaperonins. J. Biol. Chem., 270, 18158-18164.
61. von Heijne, G., Steppuhn, J. and Herrmann, R.G. (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem., 180, 535-545.
62. Weis, E. (1985) Chlorophyll fluorescence at 77 K in intact leaves: characterization of a technique to eliminate artifacts related to self-absorption. Photosynth. Res., 6, 73-86.
63. Westhoff, R. Schrubar, H., Oswald, A., Streubel, M. and Offermann, K. (1990) Biogenesis of photosystem II in C3 and C4 plants - a model system to study developmentally regulated and cell-specific expression of plastid genes. In Baltscheffsky, M. (ed.), Current Research in Photosynthesis. Vol. III. Kluwer Academic Publishers, Dordrecht, pp. 483-490.
64. Westhoff, P., Offermann-Steinhard, K., Höfer, M., Eskins, K., Oswald, A. and Streubel, M. (1991) Differential accumulation of plastid transcripts encoding photosystem II components in the mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants. Planta, 184, 377-388.
65. Wilde, A., Härtel, H., Hübschmann, T., Hoffmann, P., Shestakov, S.V. and Börner, T. (1995) Inactivation of a Synechocystis sp strain PCC 6803 gene with homology to conserved chloroplast open reading frame 184 increases the photosystem II-to-photosystem I ratio. Plant Cell, 7, 649-658.
66. Wolk, C.P., Ernst, A. and Elhai, J. (1997) Heterocyst metabolism and development. In Bryant, D.A. (ed.), The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp. 769-823.
67. Wollenberger, L., Stefansson, H., Yu, S.G. and Albertsson, P., (1994) Isolation and characterization of vesicles originating from the chloroplast grana margins. Biochim. Biophys. Acta, 1184, 93-102.
68. Zerges, W., Girard-Bascou, J. and Rochaix, J.D. (1997) Translation of the chloroplast psbC mRNA is controlled by interactions between its 5′ leader and the nuclear loci TBC1 and TBC3 in Chlamydomanas reinhardtii. Mol. Cell. Biol., 17, 3440-3448.