Abstract
Under conditions of iron deprivation cyanobacteria produce flavodoxin to replace ferredoxin as the terminal electron acceptor of photosynthesis. In unicellular cyanobacteria, the gene for flavodoxin is the second open reading frame in a dicistronic operon whose transcription is tightly regulated by iron. The first gene, isiA, produces a protein that is very similar to CP43, a chlorophyll-binding, antenna protein of the photosystem II reaction center. In the filamentous, heterocystous cyanobacterium Anabaena sp. PCC 7120, isiA and the gene for flavodoxin are located in separate operons with independent promoters. In this paper, we report on the sequence of isiA and show that it is found in a monocistronic operon that is transriptionally regulated to be expressed under iron stress but does not produce detectable transcripts under conditions of iron repletion. We also report on the sequence, organization and expression of the gene that codes for CP43, psbC. In Anabaena sp. PCC 7120, psbC has a genetic organization similar to that of other cyanobacteria and higher plants; the 5′ end of psbC overlaps the 3′ end of psbDI. Transcriptional analysis of the psbDC operon showed that it is constitutively expressed in both iron-repleted and iron-stressed conditions; however, a new monocistronic transcript was detected that contains psbC and is preferentially expressed under iron stress conditions.
Similar content being viewed by others
References
Allen M: Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4: 1–4 (1968).
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).
Alt J, Morris J, Westhoff P, Herrmann R: Nucleotide sequence of the clustered genes for the 44kd chlorophyll a apoprotein and the ‘32kd’-like protein of the Photosystem II reaction center in the spinach plastid chromosome. Curr Genet 8: 597–606 (1984).
Bookjans G, Stummann B, Rasmussen O, Henningsen K: Structure of a 3.2 kb region of pea chloroplast DNA containing the gene for the 44 kd Photosystem II polypeptide. Plant Mol Biol 6: 359–366 (1986).
Braun V, Hantke K: Genetics of bacterial iron transport. In: Winkelmann G (ed) CRC Handbook of Microbial Iron Chelates, pp. 107–138. CRC Press, Boca Raton, FL (1991).
Bricker TM: The structure and function of CPa-1 and CPa-2 in Photosystem II. Photosynth Res 24: 1–13 (1990).
Carpenter SD, Charite J, Eggers B, Vermaas WFJ: The psbC start codon in Synechocystis sp. PCC 6803. FEBS Lett 260: 135–137 (1990).
Chrisholm D, Williams JGK: Nucleotide sequence of psbC, the gene encoding the CP-43 chlorophyll a-binding protein of Photosystem II, in the cyanobacterium Synechocystis 6803. Plant Mol Biol 10: 293–301 (1988).
Dale RMK, McClure BA, Houchins JP: A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing. Application to sequencing the corn mitochondrial 18S rRNA. Plasmid 13: 31–40 (1985).
Entsch B, Smillie RM: Oxidation-reduction properties of phytoflavin, a flavoprotein from blue-green algae. Arch Biochem Biophys 151: 378–386 (1972).
Erickson M, Rahire M, Malnoe P, Girard-Bascou J, Pierre Y, Bennoun P, Rochaix J-D: Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects Photosystem II stability and D1 expression. EMBO J 5: 1745–1754 (1986).
Fillat MF, Sandmann B, Gomez-Moreno C: Flavodoxin from the nitrogen-fixing cyanobacterium Anabaena PCC 7119. Arch Microbiol 150: 160–164 (1988).
Gingrich JC, Gasparich GE, Sauer K, Bryant DA: Nucleotide sequence and expression of the two genes encoding D2 protein and the single gene encoding the CP43 protein of photosystem II in the cyanobacterium Synechococcus sp. PCC 7002. Photosynth Res 24: 137–150 (1990).
Golden SS, Brusslan J, Haselkorn R: Genetic engineering of the cyanobacterial chromosome. Meth Enzymol 153: 215–231 (1987).
Golden SS, Stearns GW: Nucleotide sequence and transcript analysis of three Photosystem II genes from the cyanobacterium Synechococcus sp. PCC 7942. Gene 67: 85–96 (1988).
Guikema JA, Sherman LA: Organization and function of chlorophyll in membranes of cyanobacteria during iron starvation. Plant Physiol 73: 250–256 (1983).
Hanahan D: Techniques for transformation of E. coli. In: Glover DM (ed) DNA Cloning, vol 1: A Practical Approach, pp. 109–135. IRL Press, Oxford (1984).
Holschuh K, Bottomley W, Whitfield PR: Structure of the spinach chloroplast genes for the D2 and 44 kDa reaction center proteins of Photosystem II and for tRNA-ser (UGA). Nucl Acids Res 12: 8819–8834 (1984).
Hutber GN, Hutson KG, Rogers LJ: Effect of iron deficiency on levels of two ferredoxins and flavodoxin in a cyanobacterium. FEMS Microbiol Lett 1: 193–196 (1977).
Kjems J, Garrett RA: Novel splicing mechanism for the ribosomal RNA intron in the archaebacterium Desulfurococcus mobilis. Cell 54: 693–703 (1988).
Laudenbach DE, Reith ME, Straus NA: Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2. J Bact 170: 258–264 (1988).
Laudenbach DE, Straus NA: Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bact 170: 5018–5026 (1988).
Leonhardt KG, Straus NA: An iron stress operon involved in photosynthetic electron transport in the marine cyanobacterium Synechococcus sp. PCC 7002. J Gen Microbiol 138: 1613–1621 (1992).
Ohyama K, Fukazawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H: Complete nucleotide sequence of liverwort Marchantia polymorpha chloroplast DNA. Plant Mol Biol Rep 4(3): 149–175 (1986).
Pakrasi HB, Riethman HC, Sherman LA: Organization of pigment proteins in the photosystem II complex of the cyanobacterium Anacystis nidulans R2. Proc Natl Acad Sci USA 83: 6903–6907 (1985).
Pardo MB, Gomez-Moreno C, Peleato ML: Effect of iron deficiency on ferredoxin levels in Anabaena variabilis PCC 6309. Arch Microbiol 153: 528–530 (1990).
Pirrotta V: Cloning Drosophila genes. In:Roberts DB (ed) Drosophila: A Practical Approach, pp. 83–110. IRL Press, Oxford (1986).
Riethman HC, Sherman LA: Immunological characterization of iron-regulated membrane proteins in the cyanobacterium Anacystis nidulans R2. Plant Physiol 88: 497–505 (1988).
Riethman HC, Sherman LA: Purification and characterization of an iron stress-induced chlorophyll-protein from the cyanobacterium Anacystis nidulans R2. Biochim Biophys Acta 935: 141–151 (1988).
Rosenberg M, Court D: Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet 13: 319–353 (1979).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
Sandmann G: Consequences of iron deficiency on photosynthetic electron transport in blue green algae. Photosynth Res 6: 261–271 (1985).
Sandmann G, Malkin R: Iron-sulfur centers and activities of the photosynthetic electron transport chain in irondeficient cultures of the blue-green alga Aphanocapsa. Plant Physiol 73: 724–728 (1983).
Sandmann G, Peleato ML, Fillat MF, Lazaro MC, Gomez-Moreno C: Consequences of iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains. Photosynth Res 26: 119–125 (1990).
Schantz R: Mapping of the chloroplast genes coding for the chlorophyll A-binding proteins in Euglena gracilis. Plant Sci Lett 40: 43–49 (1985).
Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayshida N, Matsubayasha T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita H, Deno T, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kata A, Tohdoh N, Shimada H, Sugiura M: The complete nucleotide sequence of the tobacco chloroplast genome. Plant Mol Biol Rep 4(3): 111–147 (1986).
Vermaas WFJ, Ikeuchi M: Photosystem II. In: Bogorad L, Vasil IK (eds) The Photosynthetic Apparatus: Molecular Biology and Operation, pp. 25–111. Academic Press, San Diego (1991).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Leonhardt, K., Straus, N.A. Photosystem II genes isiA, psbDI and psbC in Anabaena sp. PCC 7120: cloning, sequencing and the transcriptional regulation in iron-stressed and iron-repleted cells. Plant Mol Biol 24, 63–73 (1994). https://doi.org/10.1007/BF00040574
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00040574