Abstract
The psbB gene from the cyanobacterium Anabaena 7120 was cloned and its nucleotide sequence determined. This gene codes for the photosystem II chlorophyll-binding protein CP-47. We identified an open reading frame of 1527 bases that can code for a polypeptide with a predicted molecular weight of 56254. Expression of the psbB gene in Anabaena 7120 results in two transcripts that begin 302 or 238 bp upstream of the open reading frame and both end 288 bp downstream following a 21 bp inverted repeat. We also show that the levels of these psbB gene transcripts as well as those of the glnA, rbcLS, and psbA genes, in RNA prepared from whole filaments, remain constant during heterocyst differentiation.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adams DG, Carr NG: Developmental biology of heterocyst and akinete formation in cyanobacteria. Crit Rev Microbiol 9: 45–100 (1981).
Alam J, Whitaker RA, Krogmann DW, Curtis SE: Isolation and sequence of the gene for Ferredoxin I from the cyanobacterium Anabaena sp. strain PCC 7120. J Bact 168: 1265–1271 (1986).
Almon H, Böhme H: Components and activity of the photosynthetic electron transport system of intact heterocysts isolated from the blue-green alga Nostoc muscorum. Biochim Biophys Acta 592: 113–120 (1980).
Belknap WR, Haselkorn R: Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaend. EMBO J 6: 871–884 (1987).
Benton WD, Davis RW: Screening γgt recombinant clones by hybridization to single plaques in situ. Science 196: 180–181 (1977).
Bergman B, Lindblad P, Pettersson A, Renström E, Tiberg E: Immuno-gold localization of glutamine synthetase in a nitrogen fixing cyanobacterium (Anabaena cylindrica). Planta 166: 329–334 (1985).
Bergman B, Lindblad P, Rai AN: Nitrogenase in freeliving and symbiotic cyanobacteria: immunoelectron microscopic localization. FEMS Microbiol Lett 35: 75–78 (1986).
Bergman B, Rai AN, Söderbäck E: Nostoc of the Anthoceros and Gunnera symbioses: Immunoelectron microscopic localization of key proteins. Proceedings Sixth International Symposium on Photosynthetic Prokaryotes: 50 (1988).
Böhme H, Haselkorn R: Molecular cloning and nucleotide sequence analysis of the gene coding for heterocyst ferredoxin from the cyanobacterium Anabaena sp. strain PCC 7120. Mol Gen Genet 214: 278–285 (1988).
Bolivar F, Backman K: Plasmids of Escherichia coli as cloning vectors. In: Wu R (ed) Methods in Enzymology, vol 68, pp. 245–267. Academic Press, New York (1979).
Braun-Howland EB, Nierzwicki-Bauer SA: Localization of the 32 kd protein in an Azolla endosymbiont. Proceedings Sixth International Symposium on Photosynthetic Prokaryotes: 122 (1988).
Casadaban M, Cohen SN: Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179–207 (1980).
Chan TM, Markley JL: Nuclear magnetic resonance studies of two-iron-sulfur ferredoxins. 1. Properties of the histidine residues. Biochemistry 22: 5982–5987 (1983).
Codd GA, Stewart WDP: Ribulose-1,5-diphosphate carboxylase in heterocysts and vegetative cells of Anabaena cylindrica. FEMS Microbiol Lett 2: 247–249 (1977).
Curtis SE: Genes encoding the beta and epsilon subunits of the proton-translocating ATPase from Anabaena sp. strain PCC 7120. J Bact 169: 80–86 (1987).
Curtis SE, Haselkorn R: Isolation and sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 80: 1835–1839 (1983).
Curtis SE, Haselkorn R: Isolation, sequence and expression of two members of the 32 kd thylakoid membrane protein gene family from the cyanobacterium Anabaena 7120. Plant Mol Biol 3: 249–258 (1984).
Deisenhofer J, Epp O, Miki K, Huber R, Michel H: Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624 (1985).
Deisenhofer J, Epp O, Miki K, Huber R, Michel H: X-ray structure analysis of a membrane protein complex. J Mol Biol 180: 385–398 (1984).
Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387–395 (1984).
Fleming H, Haselkorn R: Differentiation in Nostoc muscorum: nitrogenase is synthesized in heterocysts. Proc Natl Acad Sci USA 70: 2727–2731 (1973).
Fleming H, Haselkorn R: The program of protein synthesis during heterocyst differentiation in nitrogen fixing blue-green algae. Cell 3: 159–170 (1974).
Golden JM, Carrasco CD, Mulligan ME, Schneider GJ, Haselkorn R: Deletion of a 55 kb DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120. J Bact 170: 5034–5041 (1988).
Golden JM, Robinson SJ, Haselkorn R: Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature 314: 419–423 (1985).
Golden SS, Brusslan J, Haselkorn R: Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5: 2789–2798 (1986).
Golden SS, Brusslan J, Haselkorn R: Genetic engineering of the cyanobacterial chromosome. In: Wu R, Grossman L (eds) Methods in Enzymology, vol 153, pp. 215–231. Academic Press, San Diego (1987).
Haselkorn R: Heterocysts. Ann Rev Plant Physiol 29: 319–344 (1978).
Haselkorn R, Rice D, Curtis SE, Robinson SJ: Organization and transcription of genes important in Anabaena heterocyst differentiation. Ann Microbiol 134B: 181–193 (1983).
Kratz WA, Myers J: Nutrition and growth of several blue-green algae. Am J Bot 42: 282–287 (1955).
Kyte J, Doolittle RF: A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132 (1982).
Lammers PJ, Haselkorn R: Sequence of the nifD gene coding for the α subunit of dinitrogenase from the cyanobacterium Anabaena. Proc Natl Acad Sci USA 80: 4723–4727 (1983).
Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).
Marck C: DNA Strider': a ‘C’ program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res 16: 1829–1836 (1988).
Maxam AM, Gilbert W: Sequencing end-labeled DNA with base-specific chemical cleavages. In: Grossman L, Moldave K (eds) Methods in Enzymology, vol 65, pp. 499–559. Academic Press, New York (1980).
Mazur BJ, Chui CF: Sequence of the gene coding for the β-subunit of dinitrogenase from the blue-green alga Anabaena. Proc Natl Acad Sci USA 79: 6782–6786 (1982).
Mazur BJ, Rice D, Haselkorn R: Identification of bluegreen algal nitrogen fixation genes using heterologous DNA hybridization probes. Proc Natl Acad Sci USA 77: 186–190 (1980).
Mevarech M, Rice D, Haselkorn R: Nucleotide sequence of a cyanobacterial nifH gene coding for nitrogenase reductase. Proc Natl Acad Sci USA 77: 6476–6480 (1980).
Morris J, Herrmann RG: Nucleotide sequence of the gene for the P680 chlorophyll a apoprotein of the photosystem II reaction center from spinach. Nucleic Acids Res 12: 2837–2850 (1984).
Mulligan ME, Buikema WJ, Haselkorn R: Bacterial-type ferredoxin genes in the nitrogen-fixation regions of the cyanobacterium Anabaena sp. strain PCC 7120 and Rhizobium meliloti. J Bact 170: 4406–4410 (1988).
Nakatani HY, Ke B, Dolan E, Arntzen CJ: Identity of the photosystem II reaction center polypeptide. Biochim Biophys Acta 765: 347–352 (1984).
Nanba O, Satoh K: Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112 (1987).
Newbury SF, Smith NH, Higgins CF: Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell 51: 1131–1143 (1987).
Nierzwicki-Bauer SA, Curtis SE, Haselkorn R: Cotranscription of genes encoding the small and large subunits of ribulose-1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 81: 5961–5965 (1984).
Norrander J, Kempe T, Messing J: Construction of improved M13 vectors using oligonucleotide-directed mutagenesis. Gene 26: 101–106 (1983).
Orr J, Haselkorn R: Regulation of glutamine synthetase activity and synthesis in free-living and symbiotic Anabaena spp. J Bact 152: 626–635 (1982).
Rice D, Mazur BJ, Haselkorn R: Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J Biol Chem 257: 13157–13163 (1982).
Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).
Schneider GJ, Lang JD, Haselkorn R: Anabaena promoters defined by in vitro transcription. Manuscript in preparation.
Schrautemeier B, Böhme H: A distinct ferredoxin for nitrogen fixation isolated from heterocysts of the cyanobacterium Anabaena variabilis. FEBS Lett 184: 304–308 (1985).
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).
Smith AJH: DNA sequence analysis by primed synthesis. In: Grossman L, Moldave K (eds) Methods in Enzymology, vol 65, pp. 560–580. Academic Press, New York (1980).
Stern DB, Gruissem W: Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51: 1145–1157 (1987).
Taber S, Richardson CC: DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci USA 84: 4767–4771 (1987).
Thomas J: Absence of pigments of photosystem II of photosynthesis in heterocysts of a blue-green alga. Nature 258: 715–716 (1970).
Thomas PS: Hybridization of denatured RNA transferred or dotted to nitrocellulose paper. In: Wu R, Grossman L, Moldave K (eds) Methods in Enzymology, vol 100, pp. 255–266. Academic Press, New York (1983).
Tronrud DE, Schmid MF, Matthews BW: Structure and X-ray amino acid sequence of a bacteriochlorophyll a protein from Prosthecochloris aestuarii refined at 1.9 Å resolution. J Mol Biol 188: 443–454 (1986).
Tumer NE, Robinson SJ, Haselkorn R: Different promoters for the Anabaena glutamine synthetase gene during growth using molecular or fixed nitrogen. Nature 306: 337–341 (1983).
Vermaas WFJ, Ikeuchi M, Inoue Y: Protein composition of the photosystem II core complex in genetically engineered mutants of the cyanobacterium Synechocystis sp. PCC 6803. Photosynthetic Res 17: 97–113 (1988).
Vermaas WFJ, Williams JGK, Arntzen CJ: Sequencing and modification of psbB, the gene encoding the CP-47 protein of Photosystem II, in the cyanobacterium Synechocystis 6803. Plant Mol Biol 8: 317–326 (1987).
Winkenbach F, Wolk CP: Activities of enzymes of the oxidative and the reductive pentose phosphate pathways in heterocysts of a blue-green alga. Plant Physiol 52: 480–483 (1973).
Wood NB, Haselkorn R: Control of phycobiliprotein proteolysis and heterocyst differentiation in Anabaena. J Bact 141: 1375–1385 (1980).
Yamagishi A, Katoh S: A photoactive photosystem-II reaction center complex lacking a chlorophyll-binding 40 kilodalton subunit from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 765: 118–124 (1984).
Yamagishi A, Katoh S: Further characterization of the two Photosystem II reaction center complex preparations from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 807: 74–80 (1985).
Yamanaka G, Glazer AN: Phycobiliproteins in Anabaena 7119 heterocysts. In: Papageorgiou GC, Packer L (eds) Photosynthetic Prokaryotes, pp. 69–90. Elsevier, Amsterdam (1983).
Yanisch-Perron C, Vieira J, Messing J: Improved M13 phage cloning vectors and host strains: nucleotide sequence of the M13 mp18 and pUC19 vectors. Gene 33: 103–119 (1985).
Zuker M, Stiegler P: Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res 9: 133–148 (1980).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lang, J.D., Haselkorn, R. Isolation, sequence and transcription of the gene encoding the photosystem II chlorophyll-binding protein, CP-47, in the cyanobacterium Anabaena 7120. Plant Mol Biol 13, 441–456 (1989). https://doi.org/10.1007/BF00015556
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00015556