Log in

Organization and expression of a phycobiliprotein gene cluster from the unicellular red alga Cyanidium caldarium

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have sequenced a plastid gene cluster from the unicellular red alga Cyanidium caldarium which is located downstream from the psbA gene and contains, in the following order, genes for a β-allophycocyanin-like protein (apcB′), a putative 9.5 kDa allophycocyanin linker protein (apcL 9.5) and a putative 29 kDa phycocyanin linker protein (cpcL 29). The apcB′ and apcL 9.5 genes are organized in the form of an operon. The cpcL 29 gene is transcribed monocistronically from the opposite strand of DNA. Both transcription units are probably terminated at a 25 bp inverted repeat 3 and 5 bp downstream of the stop codons of the apcL 9.5 and cpcL 29 genes, respectively. The levels of both transcripts are greatly reduced in the dark as is the psbA transcript. Downstream from the phycobiliprotein gene cluster two open reading frames (ORFs) were found which are homologous to ORFs from plastid DNAs and cyanelle DNA of Cyanophora paradoxa. Sequence homologies between genes analysed in this study and corresponding genes from cyanobacteria, chlorophytic plastids and cyanelles point to a large phylogenetic distance between the plastids of Cyanidium and cyanobacteria and other plastid types.

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

Access this article

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.

Similar content being viewed by others

References

  1. Belford HS, Offner GD, Troxler RF: Phycobiliprotein synthesis in the unicellular Rhodophyte, Cyanidium caldarium. J Biol Chem 258: 4503–4510 (1983).

    Google Scholar 

  2. Belknap WR, Haselkorn R: Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena. EMBO J 6: 871–884 (1987).

    Google Scholar 

  3. Bryant DA, deLorimier R, Lambert DH, Dubbs JM, Stirewalt VL, Stevens SEJr., Porter RP, Tam J, Jay E: Molecular cloning and nucleotide sequence of the α and β subunits of allophycocyanin from the cyanelle genome of Cyanophora paradoxa. Proc Natl Acad Sci USA 82: 3242–3246 (1985).

    Google Scholar 

  4. Bryant DA: Genetic analysis of phycobilisome biosynthesis, assembly, structure and function in the cyanobacterium Synechococcus sp. 7002. In: StevensJr SE, Bryant DA (eds) Light Energy Transduction in Photosynthesis: Higher Plant and Bacterial Models, pp. 62–90. American Society of Plant Physiologists, Rockville, MA (1988).

    Google Scholar 

  5. Conley PB, Lemaux PG, Lomax TL, Grossmann AR: Genes encoding major light-harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc Natl Acad Sci USA 83: 3924–3928 (1986).

    Google Scholar 

  6. Conley PB, Lemaux PG, Grossman A: Molecular characterization and evolution of sequences encoding light-harvesting components in the chromaticaliy adapting cyanobacterium Fremyella diplosiphon. J Mol Biol 199: 447–465 (1988).

    Google Scholar 

  7. Davis LC, Dibner MD, Battey JF: Basic Methods in Molecular Biology. Elsevier Science Publishers, Amsterdam (1986).

    Google Scholar 

  8. DeLange RJ, Williams LC, Glazer AN: The amino acid sequence of the β subunit of allophycocyanin. J Biol Chem 256: 9558–9566 (1981).

    Google Scholar 

  9. Egelhoff T, Grossmann A: Cytoplasmatic and chloroplast synthesis of phycobilisome polypeptides. Proc Natl Acad Sci USA 80: 3339–3343 (1983).

    Google Scholar 

  10. Evrard J-L, Weil J-H, Kuntz M: An ORF potentially encoding a 6.5 kDa hydrophobic protein in chloroplasts is also present in the cyanellar genome of Cyanophora paradoxa. Plant Mol Biol 15: 779–781 (1990).

    Google Scholar 

  11. Federspiel NA, Grossmann AR: Characterization of the light regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bact 172: 4072–4081 (1990).

    Google Scholar 

  12. Flueglistaller P, Ruembeli R, Suter F, Zuber H: Minor polypeptides from the phycobilisome of the cyanobacterium Mastigocladus laminosus. Hoppe-Seylers Z Physiol Chem 365: 1085–1096 (1984).

    Google Scholar 

  13. Flueglistaller P, Suter F, Zuber H: Linker polypeptides of the phycobilisome from the cyanobacterium Mastigocladus laminosus: Amino-acid sequences and relationships. Biol Chem Hoppe Seyler 366: 993–1001 (1985).

    Google Scholar 

  14. Flueglistaller P, Mimuro M, Suter F, Zuber H: Allophycocyanin complexes of the phycobilisome from Mastigocladus laminosus—influence of the linker polypeptide Lc8.9 on the spectral properties of the phycobilisome subunit. Biol Chem Hoppe-Seyler 368: 353–367 (1987).

    Google Scholar 

  15. Glazer AN: Phycobilisome — a macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 786: 29–51 (1984).

    Google Scholar 

  16. Glazer AN, Clark JH: Phycobilisomes — macromolecular structure and energy flow dynamics. Biophys J 49: 115–116 (1986).

    Google Scholar 

  17. Gruissem W: Chloroplast gene expression: How plants turn their genes on. Cell 56: 161–170 (1989).

    Google Scholar 

  18. Higgins DG, Sharp PM. CLUSTAL: a package for performing multiple sequence alignments on a microcomputer. Gene 73: 237–244 (1988).

    Google Scholar 

  19. 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 S: The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes account for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194 (1989).

    Google Scholar 

  20. Houmard J, Capuano V, Coursin T, TandeaudeMarsac N: Genes encoding core components of the phycobilisome in the Cyanobacterium Calothrix sp. Strain PCC 7601: occurrence of a multigene family. J Bact 170: 5512–5521 (1988).

    Google Scholar 

  21. Houmard J, Mazel D, Moguet C, Bryant DA, TandeaudeMarsac N: Organization and nucleotide sequence of genes encoding core components of the phycobilisomes from Synechococcus 6301. Mol Gen Genet 205: 404–410 (1986).

    Google Scholar 

  22. Johnson TR, HaynesII JI, Wealand JL, Yarbrough LR, Hirschberg R: Structure and regulation of genes encoding phycocyanin and allophycocyanin from Anabaena variabilis ATCC 29413. J Bact 170: 1858–1865 (1988).

    Google Scholar 

  23. Lemaux PG, Grossmann AR: Major light-harvesting polypeptides encoded in polycistronic transcripts in a eucaryotic alga. EMBO J 4: 1911–1919 (1985).

    Google Scholar 

  24. Lomax TL, Conley PB, Schilling J, Grossmann AR: Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA. J Bact 169: 2675–2684 (1987).

    Google Scholar 

  25. deLorimier D, Bryant DA, Porter RD, Liu WY, Jay E, StevensJr SE: Genes for the α and β subunits of phycocyanin. Proc Natl Acad Sci USA 81: 7946–7950 (1984).

    Google Scholar 

  26. deLorimier R, Bryant DA, StevensJr SE: Genetic analysis of a 9 kDa phycocyanin-associated linker polypeptide. Biochim Biophys Acta 1019: 29–41 (1990).

    Google Scholar 

  27. Lundell DJ, Glazer AN: Molecular architecture of a light-harvesting antenna. Core substructure in Synechococcus 6301 Phycobilisomes: Two new allophycocyanin and allophycocyanin B complexes. J Biol Chem 258: 902–908 (1983).

    Google Scholar 

  28. Maid U, Valentin K, Zetsche K: The psbA-gene from a red alga resembles those from cyanobacteria and cyanelles. Curr Genet 17: 255–259 (1990).

    Google Scholar 

  29. Maid U, Zetsche K: Structural features of the plastid ribosomal RNA operons of two red algae: Antithamnion sp. and Cyanidium caldarium. Plant Mol Biol 16: 537–546 (1991).

    Google Scholar 

  30. Mazel D, Marliere P: Adaptive eradication of methionine and cysteine from cyanobacterial light-harvesting proteins. Nature 341: 245–248 (1989).

    Google Scholar 

  31. Minami Y, Yamada F, Hase T, Matsubara H, Murakami A, Fujita Y, Takao T, Shimonishi Y: Amino acid sequences of allophycocyanin α- and β-subunits isolated from Anabaena cylindrica. FEBS Lett 191: 216–220 (1985).

    Google Scholar 

  32. Merola A, Astaldo R, Deluca P, Gombardella R, Musaccio A, Taddei R: Revision of Cyanidium caldarium. Three species of acidophilic algae. Giorn Bot Ital 115: 189–195 (1981).

    Google Scholar 

  33. Moerschel E, Rhiel E: Phycobilisomes and Thylakoids: The light-harvesting system of cyanobacteria and red algae. In: Harries JR, Horne RW (eds.) Electron Microscopy of Proteins, Vol. 6. Membranous Structures, pp. 209–254. Academic Press, London (1987).

    Google Scholar 

  34. Offner GD, Troxler RF: Primary structure of allophycocyanin from the unicellular Rhodophyte, Cyanidium caldarium. J Biol Chem 258: 9931–9940 (1983).

    Google Scholar 

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

    Google Scholar 

  36. Pilot TJ, Fox JL: Cloning and sequencing of the genes encoding the α and β subunits of C-phycocyanin from the cyanobacterium Agmellum quadruplicatum. Proc Natl Acad Sci USA 81: 6983–6987 (1984).

    Google Scholar 

  37. Ruembeli R, Wirth M, Suter F, Zuber H: The phycobiliprotein β16.2 of the allophycocyanin core from the cyanobacterium Mastigocladus laminosus. Biol Chem Hoppe-Seyler 368: 1–9 (1987).

    Google Scholar 

  38. Reuter W, Nickel C, Wehrmeyer W: Isolation of allophycocyanin B from Rhodella violacea results in a model of the core from the hemidiscoidal phycobilisomes of rhodophyceae. FEBS Lett 273: 155–158 (1990).

    Google Scholar 

  39. Reuter W, Wehrmeyer W: Core substructure in Mastigocladus laminosus phycobilisomes. II. The central part of the tri-cylindrical core-APcm-contains the ‘anchor’ polypeptide and no allophycocyanin B. Arch Microbiol 153: 111–117 (1990).

    Google Scholar 

  40. Schirmer T, Bode W, Huber R: X-ray crystallographic structure of the light-harvesting biliprotein C-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures. J Mol Biol 184: 257–277 (1985).

    Google Scholar 

  41. Schneider W: Einfluss von Licht und Acetat auf den Plastiden-DNA-Gehalt und die Transkript-Konzentrationen von Kern- und Organellcodierten Plastidenproteinen bei Chlorogonium elongatum. Thesis, University of Giessen, FRG (1989).

  42. Shinozaki K, Ohme M, Wagasuki T, Hayashida N, Matsubayashi T, Zaita N, Chungwongse J, Obokata J, Yamagushi-Shinozaki K, Ohto C, Torozawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugita M: The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049 (1986).

    Google Scholar 

  43. Shivji MS: Organization of the chloroplast genome in the red alga Porphyra yezoensis. Curr Genet 19: 49–54 (1991).

    Google Scholar 

  44. Sidler WG, Gysi J, Isker E, Zuber H: The complete amino acid sequence of both subunits of allophycocyanin, a light-harvesting protein-pigment complex from the cyanobacterium Mastigocladus laminosus. Hoppe Seylers Z Physiol Chem 352: 611–628 (1981).

    Google Scholar 

  45. Sidler W, Nutt H, Klumpf B, Frank G, Suter F, Brenzel A, Wehrmeyer W, Zuber H: The complete amino-acid sequence and the phylogenetic origin of Phycoerythrin-654 from the cryptophytan alga Chroomonas sp. Biol Chem Hoppe-Seyler 371: 537–547 (1990).

    Google Scholar 

  46. Steinmueller K, Kaling M, Zetsche K: In vitro synthesis of phycobiliproteins and ribulose-1,5-bisphosphate carboxylase by non-polyadenylated-RNA. Planta 159: 308–313 (1983).

    Google Scholar 

  47. Valentin K, Zetsche K: Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: Evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222: 425–430 (1990).

    Google Scholar 

  48. Valentin K, Zetsche K: Rubisco genes indicate a close phylogenetic relationship between plastids of Chromophyta and Rhodophyta. Plant Mol Biol 15: 575–584 (1990).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valentin, K., Maid, U., Emich, A. et al. Organization and expression of a phycobiliprotein gene cluster from the unicellular red alga Cyanidium caldarium . Plant Mol Biol 20, 267–276 (1992). https://doi.org/10.1007/BF00014494

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00014494

Key words

Navigation