Skip to main content
SpringerLink
Log in

Molecular and genetic analysis of the chloroplast ATPase of chlamydomonas

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

An Erratum to this article was published on 01 January 1985

Summary

We have carried out a molecular and genetic analysis of the chloroplast ATPase in Chlamydomonas reinhardtii. Recombination and complementation studies on 16 independently isolated chloroplast mutations affecting this complex demonstrated that they represent alleles in five distinct chloroplast genes. One of these five, the ac-u-c locus, has been positioned on the physical map of the chloroplast DNA by deletion mutations. The use of cloned spinach chloroplast ATPase genes in heterologous hybridizations to Chlamydomonas chloroplast DNA has allowed us to localize three or possibly four of the ATPase genes on the physical map. The beta and probably the epsilon subunit genes of Chlamydomonas CF1 lie within the same region of chloroplast DNA as the ac-u-c locus, while the alpha and proteolipid subunit genes appear to map adjacent to one another approximately 20 kbp away. Unlike the arrangement in higher plants, these two pairs of genes are separated from each other by an inverted repeat.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    Google Scholar 

  2. Bennoun P, Chua N-H: Methods for the detection and characterization of photosynthetic mutants in Chlamydomonas reinhardi. In: Bücher Th, Neupert W, Sebald W, Werner S (eds) Genetics and biogenesis of chloroplasts and mitochondria. Elsevier/North Holland Biomedical Press, Amsterdam, 1976, pp 33–39.

    Google Scholar 

  3. Bennoun P, Delepelaire P: Isolation of photosynthesis mutants in Chlamydomonas. In: Edelman M, Hallick RB, Chua N-H (eds) Methods in chloroplast molecular biology. Elsever/North Holland Biomedical Press, Amsterdam, 1982. pp 25–38.

    Google Scholar 

  4. Bennoun P, Masson A, Delosme M: A method for complementation analysis of nuclear and chloroplast mutants of photosynthesis in Chlamydomonas. Genetics 95:39–47, 1980.

    Google Scholar 

  5. Bennoun P, Masson A, Piccioni R, Chua N-H: Uniparental mutants of Chlamydomonas reinhardi defective in photosynthesis. In: Akoyunoglou G, Argyroudi-Akoyunoglou JH (eds) Chloroplast development. Elsevier/North Holland Biomedical Press, Amsterdam, 1978, pp 721–726.

    Google Scholar 

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

    Google Scholar 

  7. Chua NH, Bennoun P: Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: Wild-type and mutant strains deficient in photosystem II reaction center. Proc Natl Acad Sci USA 72:2175–2179, 1975.

    Google Scholar 

  8. Chua N-H, Gillham NW: The sites of synthesis of the principal thylakoid membrane polypeptides in Chlamydomonas reinhardtii. J Cell Biol 74:441–452, 1977.

    Google Scholar 

  9. Cone KC, Sellitti MA, Steege DA: Lac repressor mRNA transcription terminates in vivo in the lac contol region. J Biol Chem 258:11296–11304, 1983.

    Google Scholar 

  10. deHeij HT, Lustig H, Moeskops D-JM, Bovenberg WA, Bisanz C, Groot GSP: Chloroplast DNAs of Spinacia, Petunia, and Spirodela have a similar gene organization. Curr Genet 7:1–6, 1983.

    Google Scholar 

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

    Google Scholar 

  12. Dron M, Rahire M, Rochaix J-D: Sequence of the chloroplast DNA region of Chlamydomonas reinhardii containing the gene of the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162:775–793, 1982.

    Google Scholar 

  13. Gillham NW, Boynton JE, Grant DM, Shepherd HS, Wurtz EA: Genetic analysis of chloroplast DNA function. In: Cummings D, Borst P, Dawid I, Weissman S, Fox CF (eds) Extrachromosomal DNA, volume 15 of the ICN-UCLA Symposia on Molecular and Cellular Biology. Academic Press, New York, 1979, pp. 75–96.

    Google Scholar 

  14. Gorman DS, Levine RP: Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 54:1665–1669, 1965.

    Google Scholar 

  15. Grant DM, Gillham NW, Boynton JE: Inheritance of chloroplast DNA in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 77:6067–6071, 1980.

    Google Scholar 

  16. Harris DA: The coupling ATPase complex: an evolutionary view. Biosystems 14:113–121, 1981.

    Google Scholar 

  17. Harris EH, Boynton JE, Gillham NW: Chloroplast ribosome biogenesis in Chlamydomonas. Selection and characterization of mutants blocked in ribosome formation. J Cell Biol 63:160–179, 1974.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  20. Hudock MO, Togasaki RK, Lien SH, Hasek M, San Pietro A: A uniparentally inherited mutation affecting photophosphorylation in Chlamydomonas reinhardi. Biochem Biophys Res Commun 87:66–71, 1979.

    Google Scholar 

  21. Kanazawa H, Kayano T, Kinyasu T, Futai M: Nucleotide sequence of the genes for beta and epsilon subunits of proton-translocating ATPase from Escherichia coli. Biochem Biophys Res Commun 105:1257–1264, 1982.

    Google Scholar 

  22. Krebbers ET, Larrinua IM, McIntosh L, Bogorad L: The maize chloroplast genes for the beta and epsilon subunits of the photosynthetic coupling factor CF1 are fused. Nucleic Acids Res 10:568–575, 1982.

    Google Scholar 

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

    Google Scholar 

  24. Lennox ES: Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1:190–206, 1955.

    Google Scholar 

  25. Levine RP, Goodenough UW: The genetics of photosynthesis and the chloroplast in Chlamydomonas reinhardi. Ann Rev Genet 4:397–408, 1970.

    Google Scholar 

  26. Mandel M, Higa A: Calcium dependent bacteriophage DNA infection. J Mol Biol 53:159–162, 1970.

    Google Scholar 

  27. Merchant S, Selman BR: Identification of the alpha and beta subunits of the chloroplast coupling factor one in Chlamydomonas reinhardi. Eur J Biochem 137:373–376, 1983.

    Google Scholar 

  28. Myers AM, Grant DM, Rabert DK, Harris EH, Boynton JE, Gillham NW: Mutants of Chlamydomonas reinhardtii with physical alterations in their chloroplast DNA. Plasmid 7:133–151, 1982.

    Google Scholar 

  29. Nelson N: Structure and function of CF0. In: Selman BR, Selman-Reimer S (eds) Energy coupling in photosynthesis. Elsevier North Holland, 1981, pp 261–268

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

    Google Scholar 

  31. Piccioni RG, Bennoun P, Chua N-H: A nuclear mutant of Chlamydomonas reinhardtii defective in photosynthetic photophosphorylation. Characterization of the algal coupling factor ATPase. Eur J Biochem 117:93–102, 1981.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  34. Rochaix JD: Restriction endonuclease map of the chloroplast DNA of Chlamydomonas reinhardii. J Mol Biol 126:597–617, 1978.

    Google Scholar 

  35. Rochaix JD: Organization, function and expression of the chloroplast DNA of Chlamydomonas reinhardii. Experientia 37:323–332, 1981.

    Google Scholar 

  36. Sancar A, Hack AM, Rupp WD: Simple method for identification of plasmid-coded proteins. J Bacteriol 137:692–693, 1979.

    Google Scholar 

  37. Schmidt GW, Matlin KS, Chua N-H: A rapid procedure for selective enrichment of photosynthetic electron transport mutants. Proc Natl Acad Sci USA 74:610–614, 1977.

    Google Scholar 

  38. Schmidt RJ, Myers AM, Gillham NW, Boynton JE: Chloroplast ribosomal proteins of Chlamydomonas synthesized in the cytoplasm are made as precursors. J Cell Biol, 1984, in press.

  39. Selman-Reimer S, Merchant S, Selman BR: Isolation and characterization of the chloroplast coupling factor 1 from wild-type Chlamydomonas reinhardi. In: Selman BR, Selman-Reimer S (eds) Energy coupling in photosynthesis. El-sevier North Holland, 1981, pp 341–352.

    Google Scholar 

  40. Shepherd HS, Boynton JE, Gillham NW: Mutations in nine chloroplast loci of Chlamydomonas affecting different photosynthetic functions. Proc Natl Acad Sci USA 76: 1353–1357, 1979.

    Google Scholar 

  41. Shinozaki K, Deno H, Kato A, Sugiura M: Overlap and cotranscription of the genes for the beta and epsilon subunits of tobacco chloroplast ATPase. Gene 24:147–155, 1983.

    Google Scholar 

  42. Shinozaki K, Sugiura M: Sequence of the intercistronic region between the ribulose-bisphosphate carboxylase-oxygenase large subunit and the coupling factor beta subunit gene. Nucleic Acids Res 10:4923–4934, 1982.

    Google Scholar 

  43. Southern EM: Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517, 1975.

    Google Scholar 

  44. Sueoka N: Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc Natl Acad Sci USA 46: 83–91, 1960.

    Google Scholar 

  45. Vieira J, Messing J: The pUC plasmids, an M13 mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268, 1982.

    Google Scholar 

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

    Google Scholar 

  47. Zurawski G, Bottomley W, Whitfield PR: Structures of the genes for the beta and epsilon subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79:6260–6264, 1982.

    Google Scholar 

  48. Fluhr R, Fromn H, Edelman M: Clone bank of Nicotiana tabacum chloroplast DNA: mapping of the alpha, beta and epsilan subunits of the ATPase coupling factor, the large subunit of ribulosebisphosphate carboxylase and the 32-k Dal membrane protein. Gene 25:271–280, 1983.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Duke University, 27706, Durham, NC, U.S.A.

    Jeffrey P. Woessner & Nicholas W. Gillham

  2. Department of Botany, Duke University, 27706, Durham, NC, U.S.A.

    Elizabeth H. Harris & John E. Boynton

  3. Institut de Biologie Physico-Chimique, 13 Rue Pierre et Marie Curie, 75005, Paris, France

    Arlette Masson & Pierre Bennoun

Authors
  1. Jeffrey P. Woessner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arlette Masson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth H. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Bennoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicholas W. Gillham
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John E. Boynton
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/BF02498716.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Woessner, J.P., Masson, A., Harris, E.H. et al. Molecular and genetic analysis of the chloroplast ATPase of chlamydomonas. Plant Mol Biol 3, 177–190 (1984). https://doi.org/10.1007/BF00016065

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00016065

Keywords

Search

Navigation