Plant Molecular Biology

, Volume 21, Issue 1, pp 27–38

Characterization and transcript analysis of the major phycobiliprotein subunit genes from Aglaothamnion neglectum (Rhodophyta)

  • Kirk E. Apt
  • Arthur R. Grossman
Research Article

Abstract

The genes encoding the α and β subunits of allophycocyanin, phycocyanin and phycoerythrin from the red alga Aglaothamnion neglectum were isolated and characterized. While the operons containing the different phycobiliprotein genes are dispersed on the plastid genome, the genes encoding the α and β subunits for each phycobiliprotein are contiguous. The β subunit gene is 5′ for both the phycocyanin and phycoerythrin operons, while the α subunit gene is 5′ for the allophycocyanin operon. The amino acid sequences of A. neglectum phycobiliproteins, as deduced from the nucleotide sequences of the genes, are 65–85% identical to analogous proteins from other red algae and cyanobacteria. The conserved nature of the plastid-encoded red algal and cyanobacterial phycobiliprotein genes supports the proposed origin of red algal plastids from cyanobacterial endosymbionts.

Many environmental factors effect phycobilisome biosynthesis. The effect of both nutrient availability and light quantity on the level of A. neglectum phycobiliprotein subunits and the mRNA species encoding those subunits is described.

Key words

allophycocyanin phycobilisome phycocyanin phycoerythrin plastid red algae 

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References

  1. 1.
    Anderson LK, Grossman AR: Genes for phycocyanin subunits in Synechocystis sp. strain PCC 6701 and assembly mutant UV16. J Bact 172: 1289–1296 (1990).PubMedGoogle Scholar
  2. 2.
    Anderson LK, Grossman AR: Structure and light-regulated expression of phycoerythrin genes in wild-type and phycobilisome assembly mutants of Synechocystis sp. strain PCC 6701. J Bact 172: 1297–1305 (1990).PubMedGoogle Scholar
  3. 3.
    Boczar BA, Delaney TP, Cattolico RA: Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemotropic bacterium. Proc Natl Acad Sci USA 86: 4996–4999 (1989).PubMedGoogle Scholar
  4. 4.
    Bryant D: Cyanobacterial phycobilisomes: Progress to-wards a complete structural and functional analysis via molecular genetics. In: Bogorad L, Vasil IK (eds) The Molecular Biology of Plastids and Mitochondria, pp. 255–298. Academic Press, New York (1991).Google Scholar
  5. 5.
    Capuano V, Braux A-S, Tandeau de Marsac N, Houmard J: The ‘anchor polypeptide’ of cyanobacterial phycobilisomes, molecular characterization of the Synechococcus sp. PCC 6301 apcE gene. J Biol Chem 266: 7239–7247 (1991).PubMedGoogle Scholar
  6. 6.
    Conley PB, Lemaux PG, Grossman AR: Molecular characterization and evolution of sequences encoding light harvesting components in the chromatically adapting cyanobacterium Fremyella diplosiphon. J Mol Biol 199: 447–465 (1988).PubMedGoogle Scholar
  7. 7.
    Egelhoff T, Grossman AR: Cytoplasmic and chloroplast synthesis of phycobilisome polypeptides. Proc Natl Acad Sci USA 80: 3339–3343 (1983).Google Scholar
  8. 8.
    Federspiel NA, Grossman AR: Characterization of the light-regualted operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bact 172: 4072–4081 (1990).PubMedGoogle Scholar
  9. 9.
    Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137: 266–267 (1984).PubMedGoogle Scholar
  10. 10.
    Gantt E: Phycobilisomes. Annu Rev Plant Physiol 32: 327–347 (1981).CrossRefGoogle Scholar
  11. 11.
    Goff LJ, Coleman AW: The use of plastid DNA restriction endonuclease patterns in delineating red algal species and populations. J Phycol 24: 357–368 (1988).Google Scholar
  12. 12.
    Golden S, Stearns GW: Nucleotide sequence and transcript analysis of three photosystem II genes from the cyanobacterium Synechococcus sp. PCC 7942. Gene 67: 85–96 (1988).CrossRefPubMedGoogle Scholar
  13. 13.
    Glazer AN: Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14: 47–77 (1985).CrossRefPubMedGoogle Scholar
  14. 14.
    Glazer AN: Phycobilisomes: assembly and attachment. In: Fay P, Van Baalen C (eds) The Cyanobacteria, pp. 69–94. Elsevier Biomedical, Amsterdam (1987).Google Scholar
  15. 15.
    Glazer AN: Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264: 1–4 (1989).PubMedGoogle Scholar
  16. 16.
    Glazer AN, Melis A: Photochemical reaction centers; structure, organization and function. Annu Rev Plant Physiol 38: 11–45 (1987).Google Scholar
  17. 17.
    Gray MW: The evolutionary origins of organelles. Trends Genet 5: 294–299 (1989).CrossRefPubMedGoogle Scholar
  18. 18.
    Grossman AR, Lemaux PG, Conley PB, Bruns BU, Anderson LK: Characterization of phycobiliprotein and linker polypeptide genes in Fremyella diplosiphon and their regulated expression during complementary chromatic adaptation. Photosyn Res 17: 25–56 (1988).Google Scholar
  19. 19.
    Hawley DK, McClure WR: Compilation and analysis of Escherichia coli promoter DNA sequences. Nucl Acids Res 11: 2237–2255 (1983).PubMedGoogle Scholar
  20. 20.
    Hwang S-R, Tabia FR: Cloning and expression of the chloroplast-encoded rbcL and rbsS genes from the marine diatom Cylindrotheca sp. strain N1. Plant Mol Biol 13: 69–79 (1989).PubMedGoogle Scholar
  21. 21.
    Jahn W, Steinbiss J, Zetsche K: Light intensity adaptation of the phycobiliprotein content of the red alga Porphyridium. Planta 161: 536–539 (1984).CrossRefGoogle Scholar
  22. 22.
    Jeffrey SW, Humphrey GF: New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167: 191 (1975).Google Scholar
  23. 23.
    Kalla SR, Lind LK, Lidholm J, Gustafsson P: Transcriptional organization of the phycocyanin subunit gene clusters of the cyanobacterium Anacystis nidulans UTEX 625. J Bact 170: 2961–2970 (1985).Google Scholar
  24. 24.
    Kohchi T, Shirai H, Fukuzawa H, Sano T, Komano T, Umesono K, Inokuchi H, Ozeki H, Ohyama K: Structure and organization of Marchantia polymorpha chloroplast genome IV. Inverted repeat and small single copy regions. J Mol Biol 203: 353–372 (1988).CrossRefPubMedGoogle Scholar
  25. 25.
    Lemaux PG, Grossman AR: Major light-harvesting polypeptides encoded in polycistronic transcripts in a eukaryotic algal. EMBO J 4: 1911–1919 (1985).PubMedGoogle Scholar
  26. 26.
    Levy I, Gantt E: Light acclimation in Porphyridium purpureum (Rhodophyta): growth, photosynthesis and phycobilisomes. J Phycol 24: 452–458 (1988).Google Scholar
  27. 27.
    Levy I, Gantt E: Development of photosynthetic activity in Porphyridium purpureum (Rhodophyta) following nitrogen starvation. J Phycol 26: 62–68 (1990).CrossRefGoogle Scholar
  28. 28.
    Lundell DJ, Williams RC, Glazer AN: Molecular architecture of a light-harvesting antenna. In vitro assembly of the rod substructures of Synechococcus 6301 phycobilisomes. J Biol Chem 256: 3580–3592 (1981).PubMedGoogle Scholar
  29. 29.
    MacColl R, Gaurd-Frair D: Phycobiliproteins. CRC-Press, Boca Raton, FL (1987).Google Scholar
  30. 30.
    Magruder WH: Specialized appendages from the red alga Aglaothamnion neglectum (Ceramiales, Ceramiaceae) specifically bind with trichogynes. J Phycol 20: 436–440 (1984).Google Scholar
  31. 31.
    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).PubMedGoogle Scholar
  32. 32.
    Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, NY (1982).Google Scholar
  33. 33.
    Nutsch W, Agel G: Fluence rate and wavelength dependence of photobleaching in the cyanobacterium Anabaena variabilis. Arch. Microbiol 144: 268–271 (1986).Google Scholar
  34. 34.
    Offner GD, Brown-Masson AS, Ehrhardt MM, Troxler RF: Primary structure of phycocyanin from the unicellular rhodophyte Cyanidium caldarium. I. complete amino acid sequence of the α subunit. J Biol Chem 256: 12167–12175 (1981).PubMedGoogle Scholar
  35. 35.
    Offner GD, Troxler RF: Primary structure of allophycocyanin from the unicellular rhodophyte Cyanidium caldarium: The complete amino acid sequences of the α and β subunits. J Biol Chem 258: 9931–9940 (1983).PubMedGoogle Scholar
  36. 36.
    Rieth M, Douglas S: Localization of B-phycoerythrin to the thylakoid lumen of Cryptomonas Φ does not involve a signal peptide. Plant Mol Biol 15: 585–592 (1990).CrossRefPubMedGoogle Scholar
  37. 37.
    Roell MK: Molecular genetics in a macrophytic red alga; characterization of the operon encoding phycoerythrin, the major light-harvesting pigment of Polysiphonia boldii. Ph.D. thesis, University of Calif, Santa Barbara (1991).Google Scholar
  38. 38.
    Roell MK, Morse D: Fractionation of nuclear, chloroplast and mitochondria DNA from Polysiphonia boldii (Rhodophyta) using a rapid and simple method for the simultaneous isolation of RNA and DNA. J Phycol 27: 299–305 (1991).Google Scholar
  39. 39.
    Rosen KM, Lamperti ED, Villa-Komaroff L: Optimizing the Northern blot procedure. Biotechniques 8: 398–403 (1990).PubMedGoogle Scholar
  40. 40.
    Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).PubMedGoogle Scholar
  41. 41.
    Shine J, Dalgarno L: The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342–1346 (1974).PubMedGoogle Scholar
  42. 42.
    Shivji MS: Organization of the chlorplast genome in the red alga Porphyra yezoensis. Curr Genet 19: 49–54 (1991).Google Scholar
  43. 43.
    Sidler W, Kumpf B, Suter F, Klotz AV, Glazer AN, Zuber H: The complete amino acid sequence of the α and β subunits of B-phycoerythrin form the Rhodophytan alga Porphyridium cruentum. Biol Chem Hoppe-Seyler 370: 115–124 (1989).PubMedGoogle Scholar
  44. 44.
    Troxler RF, Ehrhardt MM, Brown-Mason AS, Offner GD: Primary structure of phycocyanin from the unicellular rhodophyte Cyanidium caldarium. II. Complete amino acid sequence of the β subunit. J Biol Chem 256: 12176–12184 (1981).PubMedGoogle Scholar
  45. 45.
    Valentin K, Zetsche K: Rubisco genes indicate a close phylogenetic relation between the plastids of chromophyta and rhodophyta. Plant Mol Biol 15: 575–584 (1990).PubMedGoogle Scholar
  46. 46.
    Waaland SD, Cleland R: Development in the red alga, Griffthsia pacifica: Control by internal and external factors. Planta 105: 196–204 (1972).Google Scholar
  47. 47.
    Waaland JR, Waaland SD, Bates G: Chloroplast structure and pigment composition in the red alga Griffthsia pacifica: regulation by light intensity. J Phycol 10: 193–199 (1974).Google Scholar
  48. 48.
    Wada K, Wada Y, Doi H, Ishibashi F, Gojobori T, Ikemura T: Codon usage tabulated from the GenBank genomic sequence data. Nucl Acids Res 19: 1981–1985 (1991).PubMedGoogle Scholar
  49. 49.
    Yamanaka G, Glazer AN: Dynamic aspects of phycobilisome structure, phycobilisome turnover during nitrogen starvation in Synechococcus sp. Arch Microbiol 124: 39–47 (1980).CrossRefGoogle Scholar
  50. 50.
    Yu M-H, Glazer AN, Williams RC: Cyanobacterial phycobilisomes. Phycocyanin assembly in the rod substructures of Anabaena variabilis phycobilisomes. J Biol Chem 256: 13130–13139 (1981).PubMedGoogle Scholar
  51. 51.
    Zuber H, Brunisholz R, Sidler W: Structure and function of light-harvesting pigment complexes. In: Amesz J (ed) Photosynthesis, pp. 233–271. Elsevier Biomedical, Amsterdam (1987).Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Kirk E. Apt
    • 1
  • Arthur R. Grossman
    • 1
  1. 1.Department of Plant BiologyCarnegie Institution of WashingtonStanfordUSA

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