Skip to main content
SpringerLink
Log in

Expression of photosynthesis genes in the cyanobacteriumSynechocystis sp. PCC 6803:psaA-psaB andpsbA transcripts accumulate in dark-grown cells

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have cloned and sequenced thepsaA andpsaB genes from the unicellular cyanobacteriumSynechocystis sp. PCC 6803. These genes are arranged in tandem, are co-transcribed, and are highly homologous to thepsaA andpsaB genes previously characterized. RNA was isolated from light-grown cells, from cells put in total darkness with and without glucose, and from cells grown under light-activated heterotrophic growth (LAHG) conditions. Quantitation of hybridization to northern blots revealed only a slight decrease in the accumulation of thepsaA-psaB transcript in cells grown in complete darkness with glucose and in LAHG cells, relative to light-grown cells. Accumulation of thepsbA transcript steadily declines through dark incubation, with a steady-state level in LAHG cells 28% of that in light-grown cells. Transcripts frompsbD, psaD, andrbcLS accumulate in cells grown in complete darkness and in LAHG cells to approximately the same levels as in light-grown cells. Photosynthesis gene transcripts in cells grown in the dark without glucose were detected, but were highly degraded. Our data prove that transcripts from photosynthesis genes do accumulate in dark-grownSynechocystis 6803, which may allow for synthesis and assembly of photosystem (PS) I and PS II in the dark.

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. Anderson SL, McIntosh L: Light-activated heterotrophic growth of the cyanobacteriumSynechocystis sp. PCC 6803: a blue-light-requiring process. J Bact 173: 2761–2767 (1991).

    Google Scholar 

  2. Bengis C, Nelson N: Subunit structure of chloroplast photosystem I reaction center. J Biol Chem 252: 4564–4569 (1977).

    Google Scholar 

  3. Boyer HW, Roulland-Dussoix D: A complementation analysis of the restriction and modification of DNA inEscherichia coli. J Mol Biol 41: 459–472 (1969).

    Google Scholar 

  4. Bustos SA, Schaefer MR, Golden SS: Different and rapid responses of four cyanobacterialpsbA transcripts to changes in light intensity. J Bact 172: 1998–2004 (1990).

    Google Scholar 

  5. Cantrell A, Bryant DA: Molecular cloning and nucleotide sequence of thepsaA andpsaB genes of the cyanobacteriumSynechococcus sp. PCC 7002. Plant Mol Biol 9: 453–468 (1987).

    Google Scholar 

  6. Chen S-CG, Cheng M-C, Chen J, Hwang L-Y: Organization of the rice chloroplastpsaA-psaB-rps14 gene and the presence of sequence heterogeneity in this gene cluster. Plant Sci 68: 213–221 (1990).

    Google Scholar 

  7. Chitnis PR, Reilly PA, Miedel MC, Nelson N: Structure and targeted mutagenesis of the gene encoding 8-kDa subunit of photosystem I from the cyanobacteriumSynechecystis sp. PCC 6803. J Biol Chem 264: 18374–18380 (1989).

    Google Scholar 

  8. Chitnis PR, Reilly PA, Nelson N: Insertional inactivation of the gene encoding subunit II of photosystem I from the cyanobacteriumSynechocystis sp. PCC 6803. J Biol Chem 264: 18381–18385 (1989).

    Google Scholar 

  9. Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kück U, Bennoun P, Rochaix J-D: Mutant phenotypes support atrans-splicing mechanism for the expression of the tripartitepsaA gene in theC. reinhardtii chloroplast. Cell 52: 903–913 (1988).

    Google Scholar 

  10. Cushman JC, Hallick RB, Price CA: The gene for the P700-chlorophylla protein inEuglena gracilis is interrupted by three introns. In: Biggens J (ed) Progress in Photosynthesis Research, pp. 667–670. Martinus Nijhoff Publishers, Dordrecht, Netherlands (1987).

    Google Scholar 

  11. Debus RJ, Barry BA, Babcock GT, McIntosh L: Sitedirected mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 85: 427–430 (1988).

    Google Scholar 

  12. Feinberg AP, Vogelstein B: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    Google Scholar 

  13. Fish LE, Kück U, Bogorad L: Two partially homologous adjacent light-inducible maize chloroplast genes encoding polypeptides of the P700 chlorophylla-protein complex of photosystem I. J Biol Chem 260: 1413–1421 (1985).

    Google Scholar 

  14. Golbeck JH: Structure, function, and organization of the photosystem I reaction center complex. Biochim Biophys Acta 895: 167–204 (1989).

    Google Scholar 

  15. Golbeck JH, Bryant DA: Photosystem I. Current Topics in Bioenergetics (1991),(in press).

  16. Golbeck JH, Parrett KG, Mehari T, Jones KL, Brand JJ: Isolation of the intact photosystem I reaction center core containing P700 and iron-sulfur center Fx. FEBS Lett 228: 268–272 (1988).

    Google Scholar 

  17. Golden SS, Brusslan J, Haselkorn R: Genetic engineering of the cyanobacterial chromosome. Meth Enzymol 153: 215–231 (1987).

    Google Scholar 

  18. Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y, Rochaix J-D:Trans-splicing mutants ofChlamydomonas reinhardtii. Mol Gen Genet 223: 417–425 (1990).

    Google Scholar 

  19. Grunstein M, Hogness DS: Colony hybridization: A method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci USA 72: 3961–3965 (1975).

    Google Scholar 

  20. Hawley DK, McClure WR: Compilation and analysis ofEscherichia coli promoter DNA sequences. Nucl Acids Res 11: 2237–2255 (1983).

    Google Scholar 

  21. Henikoff S: Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351–359 (1984).

    Google Scholar 

  22. Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun C-R, Meng B-Y, Li Y-Q, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M: The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194 (1989).

    Google Scholar 

  23. Ho KK, Krogmann DW: Photosynthesis. In: Carr NG, Whitton BA (eds) The Biology of Cyanobacteria, pp. 191–214. University of California Press, Los Angeles (1982).

    Google Scholar 

  24. Høj PB, Svendsen I, Scheller HV, Møller BL: Identification of a chloroplast-encoded 9-kDa polypeptide as a 2[4Fe-4S] protein carrying centers A and B of photosystem I. J Biol Chem 262: 12676–12684 (1987).

    Google Scholar 

  25. Jansson C, Debus RJ, Osiewacz HD, Gurevitz M, McIntosh L: Construction of an obligate photoheterotrophic mutant of the cyanobacteriumSynechocystis 6803 Plant Physiol 85: 1021–1025 (1987).

    Google Scholar 

  26. Kirsch W, Seyer P, Herrmann RG: Nucleotide sequence of the clustered genes for two P700 chlorophylla apoproteins of the photosystem I reaction center and the ribosomal protein S14 of the spinach plastid chromosome. Curr Genet 10: 843–855 (1986).

    Google Scholar 

  27. Kössel H, Döry I, Igloi G, Maier R: A leucine-zipper motif in photosystem I. Plant Mol Biol 15: 497–499 (1990).

    Google Scholar 

  28. Kück U, Choquet Y, Schneider M, Dron M, Bennoun P: Structural and transcriptional analysis of two homologous genes for the P700 chlorophylla-apoproteins inChlamydomonas reinhardii: evidence forin vivo trans-splicing. EMBO J 6: 2185–2195 (1987).

    Google Scholar 

  29. Lehmbeck J, Rasmussen OF, Bookjans GB, Jepsen BR, Stummann BM, Henningsen KW: Sequence of two genes in pea chloroplast DNA coding for 84 and 82 kDa polypeptides of the photosystem I complex. Plant Mol Biol 7: 3–10 (1986).

    Google Scholar 

  30. Lönneborg A, Kalla SR, Samuelsson G, Öquist G: Light-regulated expression of thepsbA transcript in the cyanobacteriumAnacystis nidulans. FEBS Lett 240: 110–114 (1988).

    Google Scholar 

  31. Lundell DJ, Glazer AN, Melis A, Malkin R: Characterization of a cyanobacterial photosystem I complex. J Biol Chem 260: 646–654 (1985).

    Google Scholar 

  32. Meng BY, Tanaka M, Wakasugi T, Ohme M, Shinozaki K, Sugiura M: Co-transcription of the genes encoding two P700 chlorophylla apoproteins with the gene for ribosomal protein CS14: determination of the transcriptional initiation site byin vitro capping. Curr Genet 14: 395–400 (1988).

    Google Scholar 

  33. Metz J, Nixon P, Diner B: Nucleotide sequence of thepsbA3 gene from the cyanobacteriumSynechocystis PCC 6803. Nucl Acids Res 18: 6715 (1990).

    Google Scholar 

  34. Mohamed A, Jansson C: Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacteriumSynechocystis 6803. Plant Mol Biol 13: 693–700 (1989).

    Google Scholar 

  35. Mullet JE: Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39: 475–502 (1988).

    Google Scholar 

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

    Google Scholar 

  37. Osiewacz HD, McIntosh L: Nucleotide sequence of a member of thepsbA multigene family from the unicellular cyanobacteriumSynechocystis 6803. Nucl Acids Res 15: 10585 (1987).

    Google Scholar 

  38. Reilly P, Hulmes JD, Pan YCE, Nelson N: Molecular cloning and sequencing of thepsaD gene encoding subunit II of Photosystem I from the cyanobacterium,Synechocystis sp. PCC 6803. J Biol Chem 263: 17658–17662 (1988).

    Google Scholar 

  39. Rodermel SR, Bogorad L: Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development. J Cell Biol 100: 463–476 (1985).

    Google Scholar 

  40. Rosenberg M, Court D: Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet 13: 319–353 (1979).

    Google Scholar 

  41. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989)

    Google Scholar 

  42. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    Google Scholar 

  43. Schaefer MR, Golden SS: Differential expression of members of a cyanobacterialpsbA gene family in response to light. J Bact 171: 3973–3981 (1989).

    Google Scholar 

  44. Schaefer MR, Golden SS: Light availability influences the ratio of two forms of D1 in cyanobacterial thylakoids. J Biol Chem 264: 7412–7417 (1989).

    Google Scholar 

  45. Shine J, Dalgarno L: The 3-terminal sequence ofEscherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342–1346 (1974).

    Google Scholar 

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

    Google Scholar 

  47. Tomioka N, Shinozaki K, Sugiura M: Molecular cloning and characterization of ribosomal RNA genes from a blue-green alga,Anacystis nidulans. Mol Gen Genet 184: 359–363 (1981).

    Google Scholar 

  48. Vieira J, Messing J: Production of single-stranded plasmid DNA. Meth Enzymol 153: 3–11 (1987).

    Google Scholar 

  49. Webber AN, Malkin R: Photosystem I reaction-centre proteins contain leucine zipper motifs: A proposed role in dimer formation. FEBS Lett 264: 1–4 (1990).

    Google Scholar 

  50. Williams JGK: Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods inSynechocystis 6803. Meth Enzymol 167: 766–778 (1988).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. M.S.U.-D.O.E. Plant Research Lab, Michigan State University, 48824, East Lansing, MI, USA

    Lawrence B. Smart & Lee McIntosh

  2. Genetics Program, Michigan State University, 48824, East Lansing, MI, USA

    Lawrence B. Smart & Lee McIntosh

  3. Department of Biochemistry, Michigan State University, 48824, East Lansing, MI, USA

    Lawrence B. Smart & Lee McIntosh

Authors
  1. Lawrence B. Smart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lee McIntosh
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smart, L.B., McIntosh, L. Expression of photosynthesis genes in the cyanobacteriumSynechocystis sp. PCC 6803:psaA-psaB andpsbA transcripts accumulate in dark-grown cells. Plant Mol Biol 17, 959–971 (1991). https://doi.org/10.1007/BF00037136

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00037136

Key words

Search

Navigation