Skip to main content
SpringerLink
Log in

Synthesis and assembly of the cytochrome b-f complex in higher plants

  • Chapter
Molecular Biology of Photosynthesis

Abstract

The cytochrome b-f complex is composed of four polypeptide subunits, three of which, cytochrome f, cytochrome b-563 and subunit IV, are encoded in chloroplast DNA and synthesised within the chloroplast, and the fourth, the Rieske FeS protein, is encoded in nuclear DNA and synthesised in the cytoplasm. The assembly of the cytochrome b-fcomplex therefore requires the interaction of subunits encoded by different genomes. A key role for the nuclear-encoded Rieske FeS protein in the assembly of the complex is suggested by a study of cytochrome b-f complex mutants. The assembly of individual subunits of the complex may be regulated by the availability of prosthetic groups. The genes for the chloroplast-encoded subunits and cDNA clones for the Rieske FeS protein have been isolated and characterised. Cytochrome f and the Rieske FeS protein are synthesised initially with N-terminal presequen-ces required for their correct assembly within the chloroplast. The deduced amino acid sequences of the four subunits have been used to suggest models for the arrangement of the polypeptides in the thylakoid membrane.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alt J, Westhoff P, Sears BB, Nelson N, Hurt E, Hauska G and Herrmann RG (1983) Genes and transcripts for the polypeptides of the cytochrome b6/f complex from spinach thylakoid membranes. EMBO J 2: 979–986

    PubMed  CAS  Google Scholar 

  • Alt J and Herrmann RG (1984) Nucleotide sequence of the gene for pre-apocytochrome f in the spinach plastid chromosome. Curr Genet 8: 551–557

    Article  CAS  Google Scholar 

  • Anderson JM and Boardman NK (1973) Localization of low potential cytochrome 6–559 in photosystem I. FEBS Lett 32: 157–160

    Article  PubMed  CAS  Google Scholar 

  • Baltimore BG and Malkin R (1977) Appearance of membrane-bound iron-sulfur centers and the photosystem I reaction center during greening of barley. Plant Physiol 60: 76–80

    Article  PubMed  CAS  Google Scholar 

  • Berends T, Kubicek Q and Mullet JE (1986) Localization of the genes coding for the 51 kDa PSII chlorophyll apoprotein, apocytochrome b6, the 65–70 kDa PSI chlorophyll apoproteins and the 44 kDa PSII chlorophyll apoprotein in pea chloroplast DNA. Plant Mol Biol 6: 125–134

    Article  CAS  Google Scholar 

  • Bhaya D and Castelfranco PA (1986) Synthesis of a putative c-type cytochrome by intact, isolated pea chloroplasts. Plant Physiol 81: 960–964

    Article  PubMed  CAS  Google Scholar 

  • Clark RD and Hind G (1983) Isolation of a five-polypeptide cytochrome b-f complex from spinach chloroplasts. J Biol Chem 258: 10348–10354

    PubMed  CAS  Google Scholar 

  • Clark RD, Hawkesford MJ, Coughlan S J, Bennett J and Hind G (1984) Association of ferredoxin-NADP+ oxidoreductase with the chloroplast cytochrome b-f complex. FEBS Lett 174: 137–142

    Article  CAS  Google Scholar 

  • Courtice GRM, Bowman CM, Dyer TA and Gray JC (1985) Localisation of genes for components of photosystem II in chloroplast DNA from pea and wheat. Curr Genet 10: 329–333

    Article  CAS  Google Scholar 

  • Di Rago J-P, Perea X and Colson A-M (1986) DNA sequence analysis of diuron-resistant mutations in the mitochondrial cytochrome b gene of Saccharomyces cerevisiae. FEBS Lett 208: 208–210

    Article  PubMed  Google Scholar 

  • Doherty A and Gray JC (1979) Synthesis of cytochrome f by isolated pea chloroplasts. Eur J Biochem 98: 87–92

    Article  PubMed  CAS  Google Scholar 

  • Feierabend J (1979) Role of cytoplasmic protein synthesis and its coordination with the plastidic protein synthesis in the biogenesis of chloroplasts. Ber Deutsch Bot Ges 92: 553–574

    Google Scholar 

  • Fukuzawa H, Yoshida T, Kohchi T, Okumura T, Sawano Y and Ohyama K (1987) Splicing of group II introns in mRNAs coding for cytochrome b6 and subunit IV in the liverwort Marchantía polymorpha chloroplast genome: exon specifying a region coding for two genes with the spacer region. FEBS Lett 220: 61–66

    Article  CAS  Google Scholar 

  • Gounaris I, Michalowski CB, Bohnert H J and Price CA (1986) Restriction and gene maps of plastid DNA from Capsicum annuum (comparison of chloroplast and chromoplast DNA). Curr Genet 11: 7–16

    Article  CAS  Google Scholar 

  • Gray JC (1980) Maternal inheritance of cytochrome f in interspecific Nicotiana hybrids. Eur J Biochem 112: 39–46

    Article  PubMed  CAS  Google Scholar 

  • Gray JC, Phillips AL and Smith AG (1984) Protein synthesis by chloroplasts. In: Ellis RJ (ed) Chloroplast Biogenesis, pp 137–163. Cambridge: Cambridge University Press

    Google Scholar 

  • Gregory P and Bradbeer JW (1973) Plastid development in primary leaves of Phaseolus vulgaris: the light-induced development of the chloroplast cytochromes. Planta 109: 317–326

    Article  CAS  Google Scholar 

  • Hallier UW and Heber UW (1977) Cytochrome f deficient plastome mutants of Oenothera. In: Miyachi S, Katoh S, Fujita Y and Shibata K (eds) Photosynthetic Organelles, special issue of Plant and Cell Physiology, pp 257–273. Japan: Jap Soc Plant Physiol

    Google Scholar 

  • Heinemeyer W, Alt J and Herrmann RG (1984) Nucleotide sequence of the clustered genes for apocytochrome b6 and subunit 4 of the cytochrome b/f complex in the spinach plastid chromosome. Curr Genet 8: 543–549

    Article  CAS  Google Scholar 

  • Henningsen KW and Boardman NK (1973) Development of photochemical activity and the appearance of the high potential form of cytochrome b-559 in greening barley seedlings. Plant Physiol 51: 1117–1126

    Article  PubMed  CAS  Google Scholar 

  • Herrmann RG, Westhoff P, Alt J, Tittgen J and Nelson N (1985) Thylakoid membrane proteins and their genes. In: Vloten-Doting LV, Groot GSP and Hall TC (eds) Molecular Form and Function of the Plant Genome, pp 233–256, NATO ASI series. New York: Plenum Publishing Corporation

    Google Scholar 

  • Ho KK and Krogmann DW (1980) Cytochrome f from spinach and cyanobacteria. J Biol Chem 255: 3855–3861

    PubMed  CAS  Google Scholar 

  • Hurt E and Hauska G (1981) A cytochrome f/b6 complex of five polypeptides with plasto-quinol-plastocyanin oxidoreductase activity from spinach chloroplasts. Eur J Biochem 117: 591–599

    Article  PubMed  CAS  Google Scholar 

  • Hurt E and Hauska G (1982) Identification of the polypeptides in the cytochrome b6/f complex from spinach chloroplasts with redox-center-carrying subunits. J Bioenerg Bio-membr 14: 405–424

    Article  CAS  Google Scholar 

  • Jansen T, Rother C, Steppuhn J, Reinke H, Beyreuther K, Jansson C, Andersson B and Herrmann RG (1987) Nucleotide sequence of cDNA clones encoding the complete ‘23 kDa’ and ‘16 kDa’ precursor proteins associated with the photosynthetic oxygen-evolving complex from spinach. FEBS Lett 216: 234–240

    Article  CAS  Google Scholar 

  • Jansen RK and Palmer JD (1987) Chloroplast DNA from lettuce and Barnadesia (Ast-eraceae): structure, gene localization, and characterization of a large inversion. Curr Genet 11: 553–564

    Article  CAS  Google Scholar 

  • Karlin-Neumann GA and Tobin EM (1986) Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J 5: 9–13

    PubMed  CAS  Google Scholar 

  • Klein RR and Mullet JE (1986) Regulation of chloroplast-encoded chlorophyll-binding protein translation during plant chloroplast biogenesis. J Biol Chem 261: 11138–11145

    PubMed  CAS  Google Scholar 

  • Klein RR and Mullet JE (1987) Control of gene expression during higher plant chloroplast biogenesis: protein synthesis and transcript levels of psb A, psa A-psa B, and rbc L in dark-grown and illuminated barley seedlings. J Biol Chem 262: 4341–4348

    PubMed  CAS  Google Scholar 

  • Ko K, Straus NA and Williams JP (1984) The localization and orientation of specific genes in the chloroplast chromosome of Vicia faba. Curr Genet 8: 359–367

    Article  CAS  Google Scholar 

  • Ko K and Straus NA (1987) Sequence of the apocytochrome f gene encoded by the Vicia faba chloroplast genome. Nucl Acids Res 15: 2391

    Article  PubMed  CAS  Google Scholar 

  • Kyte J and Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132

    Article  PubMed  CAS  Google Scholar 

  • Lam E and Malkin R (1982) Ferredoxin-mediated reduction of cytochrome 6–563 in a chloroplast b-563/fcomplex. FEBS Lett 141: 98–101

    Article  CAS  Google Scholar 

  • Lam E and Malkin R (1985) Characterization of a photosynthetic mutant of Lemna lacking the cytochrome b6/f complex. Biochim Biophys Acta 810: 106–109

    Article  PubMed  CAS  Google Scholar 

  • Lin CM and Kung SD (1984) Nicotiana chloroplast genome 8. Localization of genes for subunits of ATP synthase, the cytochrome b-f complex and the 32 kD protein. Theor Applt Genet 68: 213–218

    Article  CAS  Google Scholar 

  • Malkin R and Posner HB (1978) On the site of function of the Rieske iron-sulfur center in the chloroplast electron transport chain. Biochim Biophys Acta 501: 552–554

    Article  PubMed  CAS  Google Scholar 

  • Mansfield RW and Anderson JM (1985) Transverse organization of components within the chloroplast cytochrome b-563/f complex. Biochim Biophys Acta 809: 435–444

    Article  CAS  Google Scholar 

  • Michalowski C, Breunig KD and Bohnert HJ (1987) Points of rearrangements between plastid chromosomes: location of protein coding regions on broad bean chloroplast DNA. Curr Genet 11: 265–274

    Article  CAS  Google Scholar 

  • Michel F and Dujon B (1983) Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J 2: 33–38

    PubMed  CAS  Google Scholar 

  • Miles D (1982) The use of mutations to probe photosynthesis in higher plants. In: Edelman M, Hallick RB and Chua N-H (eds) Methods in Chloroplast Molecular Biology, pp 75–107. Amsterdam: Elsevier Biomedical Press

    Google Scholar 

  • Nobrega FG and Tzagaloff A (1980) Assembly of the mitochondrial membrane. DNA sequence and organisation of the cytochrome b gene in Saccharomyces cerevisiae D273–10B. J Biol Chem 255: 9828–9837

    PubMed  CAS  Google Scholar 

  • Oettmeier W, Masson K, Soil H-J, Hurt E and Hauska G (1982) Photoaffinity labelling of plastoquinone binding sites in chloroplast cytochrome b6/f complex. FEBS Lett 144: 313–317

    Article  CAS  Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S-i, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantía polymorpha chloroplast DNA. Nature 322: 572–574

    Article  CAS  Google Scholar 

  • Oliver RP (1984) Location of the genes for cytochrome f, subunit IV of the b6/f complex, the α-subunit of CF1 ATP-synthase and subunit III of the CF0 ATP-synthase on the barley chloroplast genome. Carlsberg Res Commun 49: 555–557

    Article  CAS  Google Scholar 

  • Palmer JD (1985) Comparative organization of chloroplast genomes. Ann Rev Genet 19: 325–354

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD and Stein DB (1986) Conservation of chloroplast genome structure among vascular plants. Curr Genet 10: 823–833

    Article  CAS  Google Scholar 

  • Pfefferkorn B and Meyer HE (1986) N-terminal amino acid sequence of the Rieske iron-sulfur protein from the cytochrome b6/f-complex of spinach thylakoids. FEBS Lett 206: 233–237

    Article  CAS  Google Scholar 

  • Phillips AL (1985) Localisation of genes for chloroplast components in tomato plastid DNA. Curr Genet 10: 153–161

    Article  CAS  Google Scholar 

  • Phillips AL and Gray JC (1983) Isolation and characterization of a cytochrome b-f complex from pea chloroplasts. Eur J Biochem 137: 553–560

    Article  PubMed  CAS  Google Scholar 

  • Phillips AL and Gray JC (1984a) Synthesis of components of the cytochrome b/f complex by isolated pea chloroplasts. Eur J Biochem 138: 591–595

    Article  PubMed  CAS  Google Scholar 

  • Phillips AL and Gray JC (1984b) Location and nucleotide sequence of the gene for the 15.2 kDa polypeptide of the cytochrome b/f complex from pea chloroplasts. Mol Gen Genet 194: 477–484

    Article  CAS  Google Scholar 

  • Phillips AL and Gray JC (1984c) Synthesis of components of the cytochrome b-f complex. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol IV, pp 571–574. The Hague: Martinus Nijhoff/Dr W Junk Publishers

    Google Scholar 

  • Plesnicar M and Bendali DS (1973) The photochemical activities and electron carriers of developing barley leaves. Biochem J 136: 803–812

    PubMed  CAS  Google Scholar 

  • Rock CD, Barkan A and Taylor WC (1987) The maize plastid psb B-psb F-pet B-pet D gene cluster: spliced and unspliced pet B and pet D RNAs encode alternative products. Curr Genet 12: 69–77

    Article  PubMed  CAS  Google Scholar 

  • Rothstein SJ, Gatenby AA, Willey DL and Gray JC (1985) Binding of pea cytochrome f to the inner membrane of Escherichia coli requires the bacterial sec A gene product. Proc Natl Acad Sci USA 82: 7955–7959

    Article  PubMed  CAS  Google Scholar 

  • Schagger H, Borchart U, Machleidt W, Link TA and Von Jagow G (1987) Isolation and amino acid sequence of the ‘Rieske’ iron sulfur protein of beef heart ubiquinol:cytochrome c reductase. FEBS Lett 219: 161–168

    Article  PubMed  CAS  Google Scholar 

  • Shahak Y, Crowther D and Hind G (1981) The involvement of ferredoxin-NADP+ reductase in cyclic electron transport in chloroplasts. Biochim Biophys Acta 636: 234–243

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H and Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organisation and expression. EMBO J 5: 2043–2049

    PubMed  CAS  Google Scholar 

  • Singh GP, Wallen DG and Pillay DTN (1985) Positioning of protein-coding genes on the soybean chloroplast genome. Plant Mol Biol 4: 87–93

    Article  CAS  Google Scholar 

  • Smeekens S, de Groot M, van Binsbergen J and Weisbeek P (1985) Sequence of the precursor of the chloroplast thylakoid lumen protein plastocyanin. Nature 317: 456–458

    Article  CAS  Google Scholar 

  • Steppuhn J, Rother C, Hermans J, Jansen T, Salnikow J, Hauska G and Herrmann RG (1987) The complete amino-acid sequence of the Rieske FeS-precursor protein from spinach chloroplasts deduced from cDNA analysis. Mol Gen Genet 210: 171–177

    Article  CAS  Google Scholar 

  • Stubbe W and Herrmann RG (1982) Selection and maintenance of plastome mutants and interspecific genome/plastome hybrids from Oenothera. In: Edelman M, Hallick RB and Chua N-H (eds) Methods in Chloroplast Molecular Biology, pp 149–165. Amsterdam: Elsevier Biomedical Press

    Google Scholar 

  • Subik J and Takacsova G (1978) Genetic determination of ubiquinol-cytochrome c reductase. Mitochondrial locus much specifying resistance of Saccharomyces cerevisiae to mucidin. Mol Gen Genet 161: 99–108

    Article  PubMed  CAS  Google Scholar 

  • Takabe T, Takabe T and Akazawa T (1986) Biosynthesis of P700-chlorophyll a protein complex, plastocyanin, and cytochrome b6/f complex. Plant Physiol 81: 60–66

    Article  PubMed  CAS  Google Scholar 

  • Tittgen J, Hermans J, Steppuhn J, Jansen T, Jansson C, Andersson B, Nechushtai R, Nelson N and Herrmann RG (1986) Isolation of cDNA clones for fourteen nuclear-encoded thylakoid membrane proteins. Mol Gen Genet 204: 258–265

    Article  CAS  Google Scholar 

  • Tyagi AK and Herrmann RG (1986) Location and nucleotide sequence of the pre-apocytoch-rome f gene on the Oenothera hookeri plastid chromosome (Euoenothera plastome I). Curr Genet 10: 481–486

    Article  PubMed  CAS  Google Scholar 

  • Tyagi A, Hermans J, Steppuhn J, Jansson C, Vater F and Herrmann RG (1987) Nucleotide sequence of cDNA clones encoding the complete ‘33 kDa’ precursor protein associated with the photosynthetic oxygen-evolving complex from spinach. Mol Gen Genet 207: 288–293

    Article  CAS  Google Scholar 

  • Von Heijne G (1983) Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133: 17–21

    Article  Google Scholar 

  • Widger WR, Cramer WA, Herrmann RG and Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6/f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81: 674–678

    Article  PubMed  CAS  Google Scholar 

  • Willey DL, Huttly AK, Phillips AL and Gray JC (1983) Localization of the gene for cytochrome f in pea chloroplast DNA. Mol Gen Genet 189: 85–89

    Article  CAS  Google Scholar 

  • Willey DL, Auffret AD and Gray JC (1984a) Structure and topology of cytochrome f in pea chloroplast membranes. Cell 36: 555–562

    Article  PubMed  CAS  Google Scholar 

  • Willey DL, Howe CJ, Auffret AD, Bowman CM, Dyer TA and Gray JC (1984b) Location and nucleotide sequence of the gene for cytochrome f in wheat chloroplast DNA. Mol Gen Genet 194: 416–422

    Article  CAS  Google Scholar 

  • Wood PM and Bendall DS (1976) The reduction of plastocyanin by plastoquinol-1 in the presence of chloroplasts: a dark electron transfer reaction involving components between the two photosystems. Eur J Biochem 61: 337–344

    Article  PubMed  CAS  Google Scholar 

  • Wu N-h, Cote JC and Wu R (1986) Nucleotide sequence of the rice cytochrome f gene and the presence of sequence variation near this gene. Gene 50: 271–278

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Botany School, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK

    David L. Willey & John C. Gray

Authors
  1. David L. Willey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John C. Gray
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Illinois at Urbana, USA

    Govindjee (Editor-in-Chief) (Editor-in-Chief)

Rights and permissions

Reprints and permissions

Copyright information

© 1988 Kluwer Academic Publishers

About this chapter

Cite this chapter

Willey, D.L., Gray, J.C. (1988). Synthesis and assembly of the cytochrome b-f complex in higher plants. In: Govindjee (eds) Molecular Biology of Photosynthesis. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-2269-3_23

Download citation

  • DOI: https://doi.org/10.1007/978-94-009-2269-3_23

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-7517-6

  • Online ISBN: 978-94-009-2269-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation