Skip to main content

The chloroplast genes encoding subunits of the H+-ATP synthase

  • Chapter

Abstract

Three CF1 and three CF0 subunits of the chloroplast H+-ATP synthase are encoded on the chloroplast genome. The chloroplast atp genes are organized as two Operons in plants but not in the green alga, Chlamydomonas reinhardtii. The atpBE or β Operon shows a relatively simple organisation and transcription pattern, while the atpIHFA or α Operon is transcribed into a large variety of mRNAs. The atp genes are related to those of cyanobacteria and, more distantly, to those of non-photosynthetic bacteria such as E. coli, suggesting a common origin of most F1F0 ATP synthase subunits. Both the chloroplast and cyanobacterial ATP synthases have four F0 subunits, not three as in the E. coli complex. The proton pore of the CF0 is proposed to be formed by the interaction of subunits III and IV.

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

Buying options

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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akey CW, Crepean RH, Dunn SD, McCarty RE and Edelstein SJ (1983) Electron microscopy and single molecule averaging of subunit-deficient F1—ATPases from Escherichia coli and spinach chloroplasts. EMBO J 2: 1409–1413

    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 

  • Alt J, Winter P, Sebald W, Moser JG, Schedel R, Westhoff P and Herrmann RG (1983) Localization and nucleotide sequence of the gene for the ATP synthase proteolipid subunit on the spinach plastid chromosome. Curr Genet 7: 129–138

    Article  CAS  Google Scholar 

  • Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F and Young IG (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 156: 683–717

    Article  PubMed  CAS  Google Scholar 

  • Arana JL and Vallejos RH (1982) Involvement of sulfhydryl groups in the activation mechanism of the ATPase activity of chloroplast coupling factor 1. J Biol Chem 257: 1125–1127

    PubMed  CAS  Google Scholar 

  • Aris JP, Klionsky DJ and Simoni RD (1985) The F0 subunits of the Escherichia coli F1F0-ATP synthase are sufficient to form a functional proton pore. J Biol Chem 260: 11207–11215

    PubMed  CAS  Google Scholar 

  • Biekmann S and Feierabend J (1985) Synthesis and degradation of unassembled Polypeptides of the coupling factor of photophosphorylation CF1 in 70S ribosome-deficient rye leaves. Eur J Biochem 152: 529–535

    Article  PubMed  CAS  Google Scholar 

  • Biketov SF, Kasho VN, Kozlov IA, Mileykovskaya YI, Ostrovsky DN, Skulachev VP, Tikhonova GV and Tsuprun VL (1982) F1-like ATPase from anaerobic bacterium Lactobacillus casei contains six similar subunits. Eur J Biochem 129: 241–250

    Article  PubMed  CAS  Google Scholar 

  • Bird CR, Koller B, Auffret AD, Huttly AK, Howe CJ, Dyer TA and Gray JC (1985) The wheat chloroplast gene for CF0 subunit I of ATP synthase contains a large intron. EMBO J 4: 1381–1388

    PubMed  CAS  Google Scholar 

  • Bradley D and Gatenby AA (1985) Mutational analysis of the maize chloroplast ATPase-β subunit gene promoter: the isolation of promoter mutants in E. coli and their characterization in a chloroplast in vitro transcription system. EMBO J 4: 3641–3648

    PubMed  CAS  Google Scholar 

  • Cain BD and Simoni RD (1986) Impaired proton conductivity resulting from mutations in the a subunit of F1F0 ATPase in Escherichia coli. J Biol Chem 261: 10043–10050

    PubMed  CAS  Google Scholar 

  • Clarke DJ, Fuller FM and Morris JG (1979) The proton-translocating adenosine triphosphatase of the obligately anaerobic bacterium Clostridium pasteurianum. 1. ATP phosphohydralase activity. Eur J Biochem 9: 597–612

    Article  Google Scholar 

  • Cox GB, Downie JA, Langman L, Senior AE, Ash G, Fayle DRH and Gibson F (1981) Assembly of the adenosine triphosphatase complex in Escherichia coli: assembly of F0 is dependent on the formation of specific F, subunits. J Bact 148: 30–42

    PubMed  CAS  Google Scholar 

  • Cox GB, Fimmel AL, Gibson F and Hatch L (1986) The mechanism of ATP synthase: a reassessment of the functions of the b-and a-subunits. Biochim Biophys Acta 849: 62–69

    Article  PubMed  CAS  Google Scholar 

  • Cox GB, Hatch L, Webb D, Fimmel AL, Lin Z-H, Senior AE and Gibson F (1987) Amino acid substitutions in the 6-subunit of the F1F0-ATPase of Escherichia coli. Biochim Biophys Acta 890: 195–204

    Article  PubMed  CAS  Google Scholar 

  • Cozens AL and Walker JE (1987) The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301. Support for an endosymbiont origin of chloroplasts. J Mol Biol 194: 359–383

    Article  PubMed  CAS  Google Scholar 

  • Cozens AL, Walker JE, Phillips AL, Huttly AK and Gray JC (1986) A sixth subunit of ATP synthase, an F0 component, is encoded in the pea chloroplast genome. EMBO J 5: 217–222

    PubMed  CAS  Google Scholar 

  • Cross RL (1981) The mechanism and regulation of ATP synthesis by F,-ATPases. Ann Rev Biochem 50: 681–714

    Article  PubMed  CAS  Google Scholar 

  • De Heij HT, Jochemsen A-G, Willemsen PTJ and Groot GSP (1984) Protein synthesis during chloroplast development in Spirodela oligorhiza. Coordinated synthesis of chloroplast-encoded and nuclear-encoded subunits of ATPase and ribulose-1,5-bisphosphate carboxylase. Eur J Biochem 138: 161–168

    Article  PubMed  Google Scholar 

  • Deng X-W and Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49: 379–387

    Article  PubMed  CAS  Google Scholar 

  • Deno H, Shinozaki K and Suguira M (1983) Nucleotide sequence of tobacco chloroplast gene for the a subunit of proton-translocating ATPase. Nucleic Acids Res 10: 7511–7520

    Article  Google Scholar 

  • Deno H, Shinozaki K and Sugiura M (1984) Nucleotide sequence and transcription of tobacco chloroplast genes for CF0 subunits of proton-translocating ATPase. Gene 32: 195–201

    Article  CAS  Google Scholar 

  • Dunn SD and Heppel LA (1981) Properties and functions of the subunits of the Escherichia coli coupling factor ATPase. Arch Biochem Biophys 210: 421–436

    Article  PubMed  CAS  Google Scholar 

  • Echt CS, Polacco ML and Neuffer MG (1987) A nuclear encoded chloroplast ATP synthase mutant of Zea mays L. Mol Gen Genet 208: 230–234

    Article  CAS  Google Scholar 

  • Filiingame RH (1981) Biochemistry and genetics of bacterial H+-translocating ATPases. Curr Topics Bioenerg 11: 35–106

    Google Scholar 

  • Finel M, Rubinstein M and Pick U (1984) Preparation of an e-deficient chloroplast coupling factor 1 having a high ATPase activity. FEBS Lett 166: 85–89

    Article  CAS  Google Scholar 

  • Foster DL and Filiingame RH (1982) Stoichiometry of subunits in the H+-ATPase complex of Escherichia coli. J Biol Chem 257: 2009–2015

    PubMed  CAS  Google Scholar 

  • Fromme P, Gräber P and Salnikow J (1987) Isolation and identification of a fourth subunit in the membrane part of the chloroplast ATP-synthase. FEBS Lett 218: 27–30

    Article  CAS  Google Scholar 

  • Futai M and Kanazawa H (1980) Role of subunits in proton-translocating ATPase (F0-F1). Curr Topics Bioenerg 10: 181–215

    CAS  Google Scholar 

  • Gray MW and Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Micro Rev 46: 1–42

    CAS  Google Scholar 

  • Gruissem W and Zurawski G (1985) Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes. EMBO J 4: 3375–3383

    PubMed  CAS  Google Scholar 

  • Hanley-Bowdoin L and Chua N-H (1987) Chloroplast promoters. Trends in Biochem Sci 12: 67–70

    Article  CAS  Google Scholar 

  • Hennig J and Herrmann RG (1986) Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203: 117–128

    Article  CAS  Google Scholar 

  • Herrmann RG, Westhoff P, Alt J, Tittgen J and Nelson N (1985) Thylakoid membranes and their genes. In: Van Vloten-Doting L, Grott GSP and Hall TC (eds) Molecular Form and Function of the Plant Genome. New York: Plenum Press

    Google Scholar 

  • Hoppe J and Sebald W (1984) The proton conducting F0-part of bacterial ATP synthases. Biochim Biophys Acta 768: 1–27

    PubMed  CAS  Google Scholar 

  • Howe CJ, Auffret AD, Doherty A, Bowman CM, Dyer TA and Gray JC (1982) Location and nucleotide sequence of the gene for the proton-translocating subunit of wheat chloroplast ATP synthase. Proc Natl Acad Sci USA 79: 6903–6907

    Article  PubMed  CAS  Google Scholar 

  • Howe CJ, Bowman CM, Dyer TA and Gray JC (1983) The genes for the alpha and proton-translocating subunits of wheat chloroplast ATP synthase are close together on the same strand of chloroplast DNA. Mol Gen Genet 190: 51–55

    Article  CAS  Google Scholar 

  • Howe CJ, Fearnley IM, Walker JE, Dyer TA and Gray JC (1985) Nucleotide sequences of the genes for the alpha, beta and epsilon subunits of wheat chloroplast ATP synthase. Plant Mol Biol 4: 333–345

    Article  CAS  Google Scholar 

  • Hudson GS, Mason JG, Holton TA, Koller B, Cox G, Whitfeld PR and Bottomley W (1987) A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and three CF0 subunits of the H+-ATP synthase complex and the ribosomal protein S2. J Mol Biol 196: 283–298

    Article  PubMed  CAS  Google Scholar 

  • Hudson GS, Holton TA, Whitfeld PR and Bottomley W (1988) The spinach chloroplast rpoBC genes encode three subunits of the chloroplast RNA Polymerase. J Mol Biol, in press

    Google Scholar 

  • Kanazawa H and Futai M (1982) Structure and function of H+-ATPase: What we have learned from E. coli H+-ATPase. Ann NY Acad Sci 402: 45–64

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ, Brusilow WSA and Simoni RD (1984) In vivo evidence for the role of the s subunit as an inhibitor of the proton-translocating ATPase of Escherichia coli. J Bact 160: 1055–1060

    PubMed  CAS  Google Scholar 

  • Kobayashi K, Nakamura K and Asahi T (1987) CF1 ATPase β-and ε-subunit genes are separated in the sweet potato chloroplast genome. Nucleic Acids Res 15: 7177

    Article  PubMed  CAS  Google Scholar 

  • Krebbers ET, Larrinua IM, McIntosh L and Bogorad L (1982) The maize chloroplast genes for the β and e subunits of the photosynthetic coupling factor CF1 are fused. Nucleic Acids Res 10: 4985–5002

    Article  PubMed  CAS  Google Scholar 

  • McCarthy JEG, Schairer HU and Sebald W (1985) Translation initiation frequency of atp genes from Escherichia coli: identification of an intercistronic sequence that enhances translation. EMBO J. 4: 519–526

    PubMed  CAS  Google Scholar 

  • Merchant S and Selman BR (1985) Photosynthetic ATPases: purification, properties, subunit isolation and function. Photosynth Res 6: 3–31

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mileykovskaya EI, Abuladze AN and Ostrovsky DN (1987) Subunit composition of the H+-ATPase complex from anaerobic bacterium Lactobacillus casei. Eur J Biochem 168: 703–708

    Article  PubMed  CAS  Google Scholar 

  • Mullet JE, Orozco EM JR and Chua N-H (1985) Multiple transcripts for higher plant rbcL and atpB genes and localization of the transcription initiation site of the rbclL gene. Plant Mol Biol 4: 39–54

    Article  CAS  Google Scholar 

  • Nalin CM and McCarty RE (1984) Role of a disulphide bond in the y subunit in activation of the ATPase of chloroplast coupling factor 1. J Biol Chem 259: 7275–7280

    PubMed  CAS  Google Scholar 

  • Nelson N (1981) Proton-ATPase of chloroplasts. Curr Topics Bioenerg 11: 1–33

    CAS  Google Scholar 

  • Nelson N, Nelson H and Schatz G (1980) Biosynthesis and assembly of the proton-translocating adenosine triphosphatase complex from chloroplasts. Proc Natl Acad Sci USA 77: 1361–1364

    Article  PubMed  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, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchanda polymorpha chloroplast DNA. Nature 322: 572–574

    Article  CAS  Google Scholar 

  • Orozco EM Jr, Mullet JE and Chua N-H (1985) An in vitro system for accurate transcription initiation of chloroplast protein genes. Nucleic Acids Res 13: 1283–1302

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Patrie WJ and McCarty RE (1984) Specific binding of coupling factor 1 lacking the δ and ε subunits to thylakoids. J Biol Chem 259: 11121–11128

    PubMed  CAS  Google Scholar 

  • Perlin DS, Cox DN and Senior AE (1983) Integration of F1 and the membrane sector of the proton-ATPase of Escherichia coli. J Biol Chem 258: 9793–9800

    PubMed  CAS  Google Scholar 

  • Pick U and Racker E (1979) Purification and reconstitution of the N, N’-dicyclohexylcarbodiimide-sensitive ATPase complex from spinach chloroplasts. J Biol Chem 254: 2793–2799

    PubMed  CAS  Google Scholar 

  • Richter ML, Patrie WJ and McCarty RE (1984) Preparation of the e subunit and e subunit-deficient chloroplast coupling factor 1 in reconstitutively active forms. J Biol Chem 259: 7371–7373

    PubMed  CAS  Google Scholar 

  • Rodermel SR and Bogorad L (1987) Molecular evolution and nucleotide sequences of the maize plastid genes for the α subunit of CF1 (atpA) and the proteolipid subunit of CF0 (atpH). Genetics 116: 127–139

    PubMed  CAS  Google Scholar 

  • Sears B and Herrmann RG (1985) Plastome mutation affecting the chloroplast ATP synthase involves a post-transcriptional defect. Curr Genet 9: 521–528

    Article  PubMed  CAS  Google Scholar 

  • Sebald W and Hoppe J (1981) On the structure and genetics of the proteolipid subunit of the ATP synthase complex. Curr Topics Bioenerg 12: 1–60

    CAS  Google Scholar 

  • Sebald W and Wachter E (1980) Amino acid sequence of the proteolipid subunit of the ATP synthase from spinach chloroplasts. FEBS Lett 122: 307–311

    Article  CAS  Google Scholar 

  • Senior AE and Wise JG (1983) The proton-ATPase of bacteria and mitochondria. J Membrane Biol 73: 105–124

    Article  CAS  Google Scholar 

  • Shavit N (1980) Energy transduction in chloroplasts: structure and function of the ATPase complex. Ann Rev Biochem 49: 111–138

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Deno H, Kato A and Sugiura M (1983) Overlap and cotranscription of the genes for the beta and epsilon subunits of tobacco chloroplast ATPase. Gene 32: 195–201

    Google Scholar 

  • Shinozaki K, Deno H, Wakasugi T and Sugiura M (1986a) Tobacco chloroplast gene coding for subunit I of proton-translocating ATPase: comparison with the wheat subunit I and E. coli subunit b. Curr Genet 10: 421–423

    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 (1986b) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049

    PubMed  CAS  Google Scholar 

  • Strotmann H and Bickel-Sandkötter S (1984) Structure, function, and regulation of chloroplast ATPase. Ann Rev Plant Physiol 35: 97–120

    Article  CAS  Google Scholar 

  • Süss K-H (1980) Identification of chloroplast thylakoid membrane Polypeptides. ATPase complex (CF1-CF0) and light-harvesting chlorophyll a/b-protein (LHCP) complex. FEBS Lett 112: 255–259

    Article  Google Scholar 

  • Süss K-H and Schmidt O (1982) Evidence for an α3, β 3 , γ, δ, I, II, ε, III5 subunit stoichiometry of chloroplast ATP synthetase complex (CF1-CF0). FEBS Lett. 144: 213–218

    Article  Google Scholar 

  • Tittgen J, Hermans J, Steppuhn J, Jansen T, Jansson C, Andersson B, Neuchushtai 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 

  • Walker JE, Saraste M and Gay NJ (1984) The unc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta 768: 164–200

    PubMed  CAS  Google Scholar 

  • Walker JE, Fearnley IM, Gay NJ, Gibson BW, Northrop FD, Powell SJ, Runswick MJ, Saraste M and Tybulewicz VLJ (1985) Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J Mol Biol 184: 677–701

    Article  PubMed  CAS  Google Scholar 

  • Walker JE, Runswick MJ and Poulter L (1987) ATP synthase from bovine mitochondria. The characterization and sequence analysis of two membrane-associated sub-units and of the corresponding cDNAs. J Mol Biol 197: 89–100

    Article  PubMed  CAS  Google Scholar 

  • Watanabe A and Price CA (1982) Translation of mRNAs for subunits of chloroplast coupling factor 1 in spinach. Proc Natl Acad Sci USA 79: 6304–6308

    Article  PubMed  CAS  Google Scholar 

  • Westhoff P, Nelson N, Bunemann H and Herrmann RG (1981) Localization of genes for coupling factor subunits on the spinach plastid chromosome. Curr Genet 4: 109–120

    Article  CAS  Google Scholar 

  • Westhoff P, Alt J, Nelson N and Herrmann RG (1985) Genes and transcripts for the ATP synthase CF0 subunits I and II from spinach thylakoid membranes. Mol Gen Genet 199: 290–299

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Micro Rev 51: 221–271

    CAS  Google Scholar 

  • Woessner JP, Gillham NW and Boynton JE (1987) Chloroplast genes encoding subunits of the H+-ATPase complex of Chlamydomonas reinhardtii are rearranged compared to higher plants: sequence of the atpE gene and location of the atpF and atpI genes. Plant Mol Biol 8: 151–158

    Article  CAS  Google Scholar 

  • Zurawski G and Clegg MT (1984) The barley chloroplast DNA atpBE, trnM2, and trnV1 loci. Nucleic Acids Res 12: 2549–2559

    Article  PubMed  CAS  Google Scholar 

  • Zurawski G and Clegg MT (1987) Evolution of higher-plant chloroplast DNA-encoded genes: implications for structure-function and phylogenetic studies. Ann Rev Plant Physiol 38: 391–418

    Article  CAS  Google Scholar 

  • Zurawski G, Bottomley W and Whitfeld PR (1982) Structures of the genes for the β and ε subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79: 6260–6264

    Article  PubMed  CAS  Google Scholar 

  • Zurawski G, Bottomley W and Whitfeld PR (1986) Sequence of the genes for the β and ε subunits of ATP synthase from pea chloroplasts. Nucleic Acids Res 14: 3974

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1988 Kluwer Academic Publishers

About this chapter

Cite this chapter

Hudson, G.S., Mason, J.G. (1988). The chloroplast genes encoding subunits of the H+-ATP synthase. In: Govindjee (eds) Molecular Biology of Photosynthesis. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-2269-3_26

Download citation

  • DOI: https://doi.org/10.1007/978-94-009-2269-3_26

  • 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