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Nuclear genes required for post-translational steps in the biogenesis of the chloroplast cytochrome b 6 f complex in maize

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Abstract

Nuclear genes essential for the biogenesis of the chloroplast cytochrome b 6 f complex were identified by mutations that cause the specific loss of the complex. We describe four transposon-induced maize mutants that lack cytochrome b 6 f proteins but contain normal levels of other photosynthetic complexes. The four mutations define two nuclear genes. To identify the step at which each mutation blocks protein accumulation, mRNAs encoding each subunit were examined by Northern hybridization analysis and the rates of subunit synthesis were examined in pulse-labeling experiments. In each mutant the mRNAs encoding the known subunits of the complex were normal in size and abundance and the major subunits were synthesized at normal rates. Thus, these mutations block the biogenesis of the cytochrome b 6 f complex at a post-translational step. The two nuclear genes identified by these mutations may encode previously unknown subunits, be involved in prosthetic group synthesis or attachment, or facilitate assembly of the complex. These mutations were also used to provide evidence for the authenticity of a proposed fifth subunit of the complex and to demonstrate a role for the cytochrome b 6 f complex in protecting photosystem 11 from light-induced degradation.

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References

  • Barkan A (1988) Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J 7:2637–2644

    Google Scholar 

  • Barkan A (1993) Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 5:389–402

    Google Scholar 

  • Barkan A, Miles D, Taylor W (1986) Chloroplast gene expression in nuclear, photosynthetic mutants of maize. EMBO J 5:1421–1427

    Google Scholar 

  • Barkan A, Walker M, Nolasco M, 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

    Google Scholar 

  • Barkan A, Voelker R, Mendel-Hartvig J, Johnson D, Walker M (1995) Genetic analysis of chloroplast biogenesis in higher plants. Physiol Plant 93:163–170

    Google Scholar 

  • Bendall DS, Sanguansermsri M, Girard-Bascou J, Bennoun P (1986) Mutations of Chlamydomonas reinhardtii affecting the cytochrome bf complex. FEBS Lett 203:31–35

    Google Scholar 

  • Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42:281–311

    Google Scholar 

  • Bruce BD, Malkin R (1991) Biosynthesis of the chloroplast cytochrome b 6 f complex: studies in a photosynthetic mutant of Lemna. Plant Cell 3:203–212

    Google Scholar 

  • Cramer WA, Furbacher PN, Szczepaniak A, Tae G-S (1991) Electron transport between photosystem II and photosystem I. Curr Topics Bioenerg 16:179–222

    Google Scholar 

  • de Boer AD, Weisbeek PJ (1991) Chloroplast protein topogenesis: import, sorting, and assembly. Biochim Biophys Acta 1071:221–253

    Google Scholar 

  • Gonzales D, Neupert W (1990) Biogenesis of mitochondrial c-type cytochromes. J Bioenerg Biomembr 22:753–768

    Google Scholar 

  • Haley J, Bogorad L (1989) A 4-kDa maize chloroplast polypeptide associated with the cytochrome b 6 f complex: subunit 5, encoded by the chloroplast petE gene. Proc Natl Acad Sci USA 86:1534–1538

    Google Scholar 

  • Haley J, Bogorad L (1990) Alternative promoters are used for genes within maize chloroplast polycistronic transcription units. Plant Cell 2:323–333

    Google Scholar 

  • Howe G, Merchant S (1992) The biosynthesis of membrane and soluble plastidic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products. EMBO J 11:2789–2801

    Google Scholar 

  • Kuras R, Wollman F-A (1994) The assembly of cytochrome b 6 f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J 13:1019–1027

    Google Scholar 

  • Lemaire C, Girard-Bascou J, Wollman F-A, Bennoun P (1986) Studies on the cytochrome b 6 f complex. I. Characterization of the complex subunits in Chlamydomonas reinhardtii. Biochim Biophys Acta 851:229–238

    Google Scholar 

  • Lubben TH, Donaldson GK, Viitanen PV, Gatenby AA (1989) Several proteins imported into chloroplasts form stable complexes with the GroEL-related chloroplast molecular chaperone. Plant Cell 1:1223–1230

    Google Scholar 

  • Madueño F, Napier JA, Gray JC (1993) Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5:1865–1876

    Google Scholar 

  • Malkin R (1992) Cytochrome bc 1 and b 6 f complexes of photosynthetic membranes. Photosyn Res 33:121–136

    Google Scholar 

  • Metz JG, Miles D, Rutherford AW (1983) Characterization of nuclear mutants of maize which lack the cytochrome f/b-563 complex. Plant Physiol 73:452–459

    Google Scholar 

  • Miles D (1980) Mutants of higher plants: maize. Methods Enzymol 69:3–23

    Google Scholar 

  • Nobrega FG, Nobrega MP, Tzagoloff A (1992) BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. EMBO J 11:3821–3829

    Google Scholar 

  • Pakrasi HB, De Ciechi P, Whitmarsh J (1991) Site-directed mutagenesis of the heme axial ligands of cytochrome b559 affects the stability of the photosystem II complex. EMBO J 10:1619–1627

    Google Scholar 

  • Pierre Y, Popot J-L (1993) Identification of two 4-kDa miniproteins in the cytochrome b 6 f complex from Chlamydomonas reinhardtii. CR Acad Sci Paris 316:1404–1409

    Google Scholar 

  • Rochaix J-D (1992) Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol 8:1–28

    Google Scholar 

  • Schmidt CL, Malkin R (1993) Low molecular weight subunits associated with the cytochrome b 6 f complexes from spinach and Chlamydomonas reinhardtii. Photosyn Res 38:73–81

    Google Scholar 

  • Somerville CR (1986) Analysis of photosynthesis with mutants of higher plants and algae. Annu Rev Plant Physiol Plant Mol Biol 37:467–507

    Google Scholar 

  • Taylor W, Barkan A, Martienssen R (1987) Use of nuclear mutants in the analysis of chloroplast development. Devel Genet 8:305–320

    Google Scholar 

  • Willey DL, Gray JC (1988) Synthesis and assembly of the cytochrome bf complex in higher plants. Photosyn Res 17:125–144

    Google Scholar 

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Communicated by R. G. Herrmann

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Voelker, R., Barkan, A. Nuclear genes required for post-translational steps in the biogenesis of the chloroplast cytochrome b 6 f complex in maize. Molec. Gen. Genet. 249, 507–514 (1995). https://doi.org/10.1007/BF00290576

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  • DOI: https://doi.org/10.1007/BF00290576

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