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. 1986 Feb;5(2):217–222. doi: 10.1002/j.1460-2075.1986.tb04201.x

A sixth subunit of ATP synthase, an F0 component, is encoded in the pea chloroplast genome

Alison L Cozens 1, John E Walker 1, Andrew L Phillips 1,2, Alison K Huttly 1,3, John C Gray 1
PMCID: PMC1166721  PMID: 16453667

Abstract

DNA from pea and tobacco chloroplasts hybridizes specifically with probes derived from the gene for a membrane component, the a subunit of ATP synthase of the cyanobacterium, Synechococcus 6301. DNA sequence of the hybridizing region of the pea plastid DNA has revealed that it encodes a protein of 247 amino acids related in sequence to the a subunits of ATP synthase of Escherichia coli, Synechococcus and mitochondria. This is the sixth component of chloroplast ATP synthase that is plastid coded. The gene is located upstream from the genes for three other ATP synthase subunits and a transcript of 6 kb contains coding sequences from each of these genes. Thus the subunit a gene is part of a co-transcribed cluster of four ATP synthase genes arranged in the order a:c(or III):b(or I):α. Two other ATP synthase genes, those for β and ε subunits, are known to form a separate cluster. These gene arrangements are most closely related to those found in the cyanobacterium, Synechococcus 6301. Hence, this finding provides strong evidence for a common origin for cyanobacteria and plant chloroplasts.

Keywords: chloroplast, ATP synthase, F0 subunit, plastid coded

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  2. Biggin M. D., Gibson T. J., Hong G. F. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. doi: 10.1073/pnas.80.13.3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bird C. R., Koller B., Auffret A. D., Huttly A. K., Howe C. J., Dyer T. A., Gray J. C. The wheat chloroplast gene for CF(0) subunit I of ATP synthase contains a large intron. EMBO J. 1985 Jun;4(6):1381–1388. doi: 10.1002/j.1460-2075.1985.tb03790.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Falk G., Hampe A., Walker J. E. Nucleotide sequence of the Rhodospirillum rubrum atp operon. Biochem J. 1985 Jun 1;228(2):391–407. doi: 10.1042/bj2280391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Gay N. J., Walker J. E. The atp operon: nucleotide sequence of the promoter and the genes for the membrane proteins, and the delta subunit of Escherichia coli ATP-synthase. Nucleic Acids Res. 1981 Aug 25;9(16):3919–3926. doi: 10.1093/nar/9.16.3919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Herrmann R. G., Possingham J. V. Plastid DNA-the plastome. Results Probl Cell Differ. 1980;10:45–96. doi: 10.1007/978-3-540-38255-3_3. [DOI] [PubMed] [Google Scholar]
  7. Howe C. J., Auffret A. D., Doherty A., Bowman C. M., Dyer T. A., Gray J. C. Location and nucleotide sequence of the gene for the proton-translocating subunit of wheat chloroplast ATP synthase. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6903–6907. doi: 10.1073/pnas.79.22.6903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Klionsky D. J., Brusilow W. S., Simoni R. D. Assembly of a functional F0 of the proton-translocating ATPase of Escherichia coli. J Biol Chem. 1983 Aug 25;258(16):10136–10143. [PubMed] [Google Scholar]
  9. Koller B., Delius H., Dyer T. A. The organization of the chloroplast DNA in wheat and maize in the region containing the LS gene. Eur J Biochem. 1982 Feb;122(1):17–23. doi: 10.1111/j.1432-1033.1982.tb05842.x. [DOI] [PubMed] [Google Scholar]
  10. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  11. Nelson N., Nelson H., Schatz G. Biosynthesis and assembly of the proton-translocating adenosine triphosphatase complex from chloroplasts. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1361–1364. doi: 10.1073/pnas.77.3.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Oishi K. K., Tewari K. K. Characterization of the gene and mRNA of the large subunit of ribulose-1,5-bisphosphate carboxylase in pea plants. Mol Cell Biol. 1983 Apr;3(4):587–595. doi: 10.1128/mcb.3.4.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Palmer J. D., Thompson W. F. Rearrangements in the chloroplast genomes of mung bean and pea. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5533–5537. doi: 10.1073/pnas.78.9.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pick U., Racker E. Purification and reconstitution of the N,N'-dicyclohexylcarbodiimide-sensitive ATPase complex from spinach chloroplasts. J Biol Chem. 1979 Apr 25;254(8):2793–2799. [PubMed] [Google Scholar]
  15. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schneider E., Altendorf K. All three subunits are required for the reconstitution of an active proton channel (F0) of Escherichia coli ATP synthase (F1F0). EMBO J. 1985 Feb;4(2):515–518. doi: 10.1002/j.1460-2075.1985.tb03658.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  18. Staden R. An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res. 1982 May 11;10(9):2951–2961. doi: 10.1093/nar/10.9.2951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Staden R. Graphic methods to determine the function of nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):521–538. doi: 10.1093/nar/12.1part2.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tybulewicz V. L., Falk G., Walker J. E. Rhodopseudomonas blastica atp operon. Nucleotide sequence and transcription. J Mol Biol. 1984 Oct 25;179(2):185–214. doi: 10.1016/0022-2836(84)90465-0. [DOI] [PubMed] [Google Scholar]
  23. Walker J. E., Saraste M., Gay N. J. The unc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta. 1984 Sep 6;768(2):164–200. doi: 10.1016/0304-4173(84)90003-x. [DOI] [PubMed] [Google Scholar]
  24. Wieslander L. A simple method to recover intact high molecular weight RNA and DNA after electrophoretic separation in low gelling temperature agarose gels. Anal Biochem. 1979 Oct 1;98(2):305–309. doi: 10.1016/0003-2697(79)90145-3. [DOI] [PubMed] [Google Scholar]
  25. von Meyenburg K., Jørgensen B. B., Michelsen O., Sørensen L., McCarthy J. E. Proton conduction by subunit a of the membrane-bound ATP synthase of Escherichia coli revealed after induced overproduction. EMBO J. 1985 Sep;4(9):2357–2363. doi: 10.1002/j.1460-2075.1985.tb03939.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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