SpringerLink
Log in

Genes and transcripts for the ATP synthase CF0 subunits I and II from spinach thylakoid membranes

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

Subunits I and II of the ATP synthase CF0 in spinach are encoded by plastid and nuclear genes, respectively. Using hybrid selection translation, cell-free transcription-translation of cloned restriction fragments and an appropriate antiserum, a single gene for subunit I has been located on the circular plastid chromosome between the genes for the ATP synthase proteolipid and subunit alpha. This finding implies that the five plastome-coded ATP synthase subunits in spinach are arranged in two clusters which are separated by approximately 40 kilobase pairs of DNA. The genes of each cluster appear to be transcribed into large RNA species. The analysis indicates that the putative polycistronic proteolipid/CF0-I/alpha transcript is post-transcriptionally modified. The previous assumption that the structural gene for subunit I is split has not been excluded.-The transcript for subunit II has been found in the cytosolic RNA fraction. It lacks complementarity to plastid DNA and appears to be decoded into a protein precursor.-Evidence is presented that spinach chloroplast ATP synthase contains more than eight subunits.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ptDNA:

plastid DNA

bp:

base pairs

kbp:

kilobase pairs

References

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

    Google Scholar 

  • Alt J, Morris J, Westhoff P, Herrmann RG (1984) Nucleotide sequence of the clustered genes for the 44 kd chlorophyll a apoprotein and the “32 kd”-like protein of the photosystem II reaction center in the spinach plastid chromsome. Curr Genet 8:597–606

    Google Scholar 

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

    Google Scholar 

  • Alt J, Westhoff P, Sears BB, Nelson N, Hurt E, Hauska G, Herrmann RG (1983b) Genes and transcripts for the polypeptides of the cytochrome b 6/f complex from spinach thylakoid membranes. EMBO J 2:979–986

    Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Google Scholar 

  • Bossi L, Roth JE (1980) The influence of codon context on genetic code translation. Nature 286:123–127

    Google Scholar 

  • Bünemann H, Westhoff P, Herrmann RG (1982) Immobilization of denatured DNA to macroporous supports: I. Efficiency of different coupling procedures. Nucleic Acids Res 10:7163–7180

    Google Scholar 

  • Chua N-H, Schmidt GW (1979) Transport of proteins into mitochondria and chloroplasts. J Cell Biol 81:461–483

    Google Scholar 

  • Crouse EJ, Schmitt JM, Bohnert HJ, Gordon K, Driesel AJ, Herrmann RG (1978) Intramolecular compositional heterogeneity of Spinacia and Euglena chloroplast DNAs. In: Akoyunoglou, G. Argyroudi-Akoyunoglou JH (eds) Chloroplast development. Elsevier/North-Holland Press, Amsterdam, pp 565–572

    Google Scholar 

  • De Heij HT, Lustig H, Moeskops DJM, Bovenberg WA, Bisanz C, Groot GSP (1983) Chloroplast DNAs of Spinacia, Petunia and Spirodela have a similar gene organization. Curr Genet 7:1–6

    Google Scholar 

  • Deno H, Shinozaki K, Sugiura M (1983) Nucleotide sequence of tobacco chloroplast gene for the α-subunit of proton-translocating ATPase. Nucleic Acids Res 11:2185–2191

    Google Scholar 

  • Driesel AJ, Crouse EJ, Gordon K, Bohnert HJ, Herrmann RG, Steinmetz A, Mubumbila M, Keller M, Burkhard G, Weil JH (1979) Fractionation and identification of spinach chloroplast transfer RNAs and map** of their genes on the restriction map of chloroplast DNA. Gene 6:285–306

    Google Scholar 

  • Driesel AJ, Speirs J, Bohnert HJ (1980) Spinach chloroplast mRNA for a 32 000 Dalton polypeptide. Size and localization on the physical map of the chloroplast DNA. Biochim Biophys Acta 610:297–310

    Google Scholar 

  • Gay NJ, Walker JE (1981a) The atp operon: nucleotide sequence of the region encoding the α-subunit of Escherichia coli ATP synthase. Nucleic Acids Res 9:2187–2194

    Google Scholar 

  • Gay NJ, Walker JE (1981b) The atp operon: nucleotide sequence of the promoter and the genes for the membrane proteins, and the δ-subunit of Escherichia coli ATP synthase. Nucleic Acids Res 9:3919–3926

    Google Scholar 

  • Goldberg ML, Steitz JA (1974) Cistron specificity of 30S ribosomes heterologously reconstituted with components from Escherichia coli and Bacillus stearothermophilus. Biochemistry 13:2123–2129

    Google Scholar 

  • Grunstein M, Wallis J (1979) Colony hybridization. In: Colowick SP, Kaplan NO (eds) Methods Enzymol 68:379–389

  • Heinemeyer W, Alt J, Herrmann RG (1984) Nucleotide sequence of the clustered genes for apocytochrome b 6 and subunit 4 of the cytochrome b/f complex in the spinach plastid chromosome. Curr Genet 8:543–549

    Google Scholar 

  • herrmann RG, Possingham JV (1980) Plastid DNA-the plastome. In: Reinert J (ed) Results and problems in cell differentiation, vol 10. Springer, Berlin Heidelberg New York, pp 45–96

    Google Scholar 

  • Herrmann RG, Whitfeld PR, Bottomley W (1980a) Construction of a SalI/PstI restriction map of spinach chloroplast DNA using low-gelling-temperature-agarose electrophoresis. Gene 8:179–191

    Google Scholar 

  • Herrmann RG, Seyer P, Schedel R, Gordon K, Bisanz C, Winter P, Hildebrandt JW, Wlaschek M, Alt J, Driesel AJ, Sears BB (1980b) The plastid chromosomes of several dicotyledons. In: Bücher Th, Sebald W, Weiss H (eds) Biological chemistry of organelle formation. Springer, Berlin Heidelberg New York, pp 97–112

    Google Scholar 

  • Herrmann RG, Westhoff P, Alt J, Winter P, Tittgen J, Bisanz C, Sears BB, Nelson N, Hurt E, Hauska G, Viebrock A, Sebald W (1983) Identification and characterization of genes for polypeptides of the thylakoid membrane. In: Cifferi O, Dure L III (eds) Structure and function of plant genomes. Plenum Publ Corp, Life Sci 63:143–154

  • Howe CJ, Auffret AD, Doherty A, Bowman CM, Dyer TA, Gray JC (1982a) 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

    Google Scholar 

  • Howe CJ, Bowman CM, Dyer TA, Gray JC (1982b) Localization of wheat chloroplast genes for the beta and epsilon subunits of ATP synthase. Mol Gen Genet 186:525–530

    Google Scholar 

  • Howe CJ, Bowman CM, Dyer TA, 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

    Google Scholar 

  • Huttly AK, Gray JC (1984) Localization of genes for four ATP synthase subunits in pea chloroplast DNA. Mol Gen Genet 194:402–409

    Google Scholar 

  • Katz L, Kingsbury DT, Helinski DR (1973) Stimulation by cyclic adenosine monophosphate of plasmid deoxyribonucleic acid replication anc catabolite repression of the plasmid deoxyribonucleic acid-protein relaxation complex. J Bacteriol 114:577–591

    Google Scholar 

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

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Leaver CJ, Gray MW (1982) Mitochondrial genome organization and expression in higher plants. Ann Rev Plant Physiol 33:373–402

    Google Scholar 

  • McMaster GK, Carmichael GG (1977) Analysis of single- and double-stranded nucleic acids in polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74:4835–4838

    Google Scholar 

  • Mendiola-Morgenthaler LR, Morgenthaler JJ, Price CA (1976) Synthesis of coupling factor CF1 protein by isolated spinach chloroplasts. FEBS Slett 62:96–100

    Google Scholar 

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

    Google Scholar 

  • Morris J, Herrmann RG (1984) Nucleotide sequence of the gene for the P680 chlorophyll a apoprotein of the photosystem II reaction center from spinach. Nucleic Acids Res 12:2837–2850

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Nielsen J, Hansen FG, Hoppe J, Friedl P, von Meyenburg K (1981) The nucleotide sequence of the atp genes coding for the F0 subunits a, b, c and the F1 subunit δ of the membrane bound ATP synthase of Escherichia coli. Mol Gen Genet 184:33–39

    Google Scholar 

  • Ovchinnikov YA, Modyanov NN, Grinkevich VA, Aldanova NA, Trubetskaya OE, Nazimov IV, Hundal T, Ernster L (1984) Amino acid sequence of the oligomycin sensitivity-conferring protein (OSCP) of beef-heart mitochondria and its homology with the δ-subunit of the F1-ATPase of Escherichia coli. FEBS Lett 166:19–22

    Google Scholar 

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

    Google Scholar 

  • Rigby PWJ, Dieckmann M, Rhodes C, Berg P (1977) Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol 113:237–251

    Google Scholar 

  • Saraste M, Gay NJ, Eberle A, Runswick MJ, Walker JE (1981) The atp operon: nucleotide sequence of the genes for the γ, β and ε subunits of Escherichia coli ATP synthase. Nucleic Acids Res 9:5287–5296

    Google Scholar 

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

    Google Scholar 

  • Towbin H, Staehelin I, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets-procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Velours J, Esparza M, Hoppe J, Sebald W, Guerin B (1984) Amino acid sequence of a new mitochondrially synthesized proteolipid of the ATP synthase of Saccharomyces cerevisiae. EMBO J 3:207–212

    Google Scholar 

  • Walker JE, Runswick MJ, Saraste M (1982) Subunit equivalence in Escherichia coli and bovine heart mitochondrial F1F0 ATPases. FEBS Lett 146:393–396

    Google Scholar 

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

    Google Scholar 

  • Westhoff P, Alt J, Nelson N, Bottomley W, Bünemann H, Herrmann RG (1983a) Genes and transcripts for the P700 chlorophyll a apoprotein and subunit 2 of the photosystem I reaction center complex from spinach thylakoid membranes. Plant Mol Biol 2:95–107

    Google Scholar 

  • Westhoff P, Alt J, Herrmann RG (1983b) Localization of the genes for the two chlorophyll a-conjugated polypeptides (mol.wt.51 and 44 kd) of the photosystem II reaction center on the spinach plastid chromosome. EMBO J 2:2229–2237

    Google Scholar 

  • Westhoff P, Alt J, Widger WR, Cramer WA, Herrmann RG (1985a) Localization of the gene for apocytochrome b-559 on the plastid chromosome of spinach. Plant Mol Biol 4:103–110

    Google Scholar 

  • Westhoff P, Jansson C, Klein-Hitpaß L, Berzborn R, Larsson C, Bartlett SG (1985b) Intracellular coding sites of polypeptides associated with photosynthetic oxygen evolution of photosystem II. Plant Mol Biol 4:137–146

    Google Scholar 

  • Whitfeld PR, Bottomley W (1980) Map** of the gene for the large subunit of ribulose bisphosphate carboxylase on spinach chloroplast DNA. Biochem Internat 1:172–178

    Google Scholar 

  • Whitfeld PR, Herrmann RG, Bottomley W (1978) Map** of ribosomal RNA genes on spinach chloroplast DNA. Nucleic Acids Res 5:1741–1751

    Google Scholar 

  • Whitfeld PR, Zurawski G, Bottomley W (1983) Organization and structure of the genes for the β and ε subunits of spinach and pea chloroplast ATPase. In: Cifferi O, Dure III L (eds) Structure and Function of Plant Genomes. Life Sci 63:143–198

  • Widger WR, Cramer WA, Herrmann RG, Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b 6/f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81:674–678

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Botanisches Institut der Universität, Universitätsstrasse 1, D-4000, Düsseldorf 1, Federal Republic of Germany

    Peter Westhoff, Juliane Alt & Reinhold G. Herrmann

  2. Department of Biology, Technion, Haifa, Israel

    Nathan Nelson

Authors
  1. Peter Westhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juliane Alt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nathan Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reinhold G. Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. Schell

Dedicated to Professor Georg Melchers to celebrate his 50-year association with the journal

Rights and permissions

Reprints and permissions

About this article

Cite this article

Westhoff, P., Alt, J., Nelson, N. et al. Genes and transcripts for the ATP synthase CF0 subunits I and II from spinach thylakoid membranes. Molec Gen Genet 199, 290–299 (1985). https://doi.org/10.1007/BF00330271

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00330271

Keywords

Search

Navigation