Summary
A 9 kDa polypeptide which is loosely attached to the inner surface of the thylakoid membrane and is important for the oxygen-evolving activity of Photosystem II in the thermophilic cyanobacterium Phormidium laminosum has been purified, a partial amino acid sequence obtained and its gene cloned and sequenced. The derived amino acid sequence indicates that the 9 kDa polypeptide is initially synthesised with an N-terminal leader sequence of 44 amino acids to direct it across the thylakoid membrane. The leader sequence consists of a positively charged N-terminal region, a long hydrophobic region and a typical cleavage site. These features have analogous counterparts in the “thylakoid-transfer domain” of lumenal polypeptides from chloroplasts of higher plants. These findings support the view of the proposed function of this domain in the two-stage processing model for import of lumenal, nuclear-encoded polypeptides. In addition, there is striking primary sequence homology between the leader sequences of the 9 kDa polypeptide and those of alkaline phosphatase (from the periplasmic space of Escherichia coli) and, particularly in the region of the cleavage site, the 16 kDa polypeptide of the oxygen-evolving apparatus in the thylakoid lumen of spinach chloroplasts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baker A, Schatz G (1987) Sequences from a prokaryotic genome or the mouse dihydrofolate reductase gene can restore the import of a truncated precursor protein into yeast mitochondria. Proc Natl Acad Sci USA 84:3117–3121
Castenholz RW (1970) Laboratory culture of thermophilic cyanophytes. Schweiz Z Hydrol 32:538–551
Curtis SE, Haselkorn R (1983) 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
Davis LG, Dibner MD, Battey JF (1986) Basic methods in molecular biology. Elsevier Science Publishing, New York, NY
Garnier J, Osguthorpe DJ, Robson B (1978) Analysis of the accuracy and implications of simple methods for predicting secondary structure of globular proteins. J Mol Biol 120:97–120
Hird SM, Dyer TA, Gray JC (1986) The gene for the 10 kDa phosphoprotein of photosystem II is located in chloroplast DNA. FEBS Lett 209:181–186
Homann PH (1987) The relations between the chloride, calcium, and polypeptide requirements of photosynthetic water oxidation. J Bioenerg Biomembr 19:105–123
Jansen T, Rother C, Steppuhn H, Reinke H, Beyreuther K, Jansson C, Andersson B, Hermann RG (1987) Nucleotide sequence of cDNA clones encoding the complete “23 kDa” and “16 kDa” precursor proteins associated with the photosynthetic oxygenevolving complex from spinach. FEBS Lett 216:234–240
Kikuchi Y, Yoda K, Yamasaki M, Tamura G (1981) The nucleotide sequence of the promoter and the amino-terminal region of alkaline phosphatase structural gene (Pho A) of Escherichia coli. Nucleic Acids Res 9:5671–5678
Kirwin PM, Elderfield PD, Robinson C (1987) Transport of proteins into chloroplasts: partial purification of a thylakoidal processing peptidase involved in plastocyanin biogenesis. J Biol Chem 262:16386–16390
Kuwabara T, Reddy KJ, Sherman LA (1987) Nucleotide sequence of the gene from the cyanobacterium Anacystis nidulans R2 encoding the Mn-stabilizing protein involved in photosystem II water oxidation. Proc Natl Acad Sci USA 84:8230–8234
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Laursen RA (1971) Solid-phase Edman degradation. An automatic peptide sequencer. Eur J Biochem 20:89–102
Lautner A, Klein R, Ljungberg U, Reilander H, Bartling D, Andersson B, Reinke H, Beyreuther K, Herrmann RG (1988) Nucleotide sequence of cDNA clones encoding the complete precursor for the “10-kDa” polypeptide of Photosystem II from spinach. J Biol Chem 263:10077–10081
Lipman DH, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NY
Marmur J (1961) A procedure for isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218
Murata N, Miyao M (1985) Extrinsic membrane proteins in the photosynthetic oxygen-evolving complex. Trends Biochem Sci 10:122–124
Philbrick JB, Zilinskas BA (1988) Cloning, nucleotide sequence and mutational analysis of the gene encoding the photosystem II manganese-stabilizing polypeptide of Synechococcus 6803. Mol Gen Genet 212:418–425
Rother C, Jansen T, Tyagi A, Tittgen J, Hermann RG (1986) Plastocyanin is encoded by an uninterrupted nuclear gene in spinach. Curr Genet 11:171–176
Smeekens S, de Groot M, van Binsbergen J, Weisbeek P (1985) Sequence of the precursor of the chloroplast thylakoid lumen protein plastocyanin. Nature 317:456–458
Staden R (1982) An interactive graphics program for computing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10:2951–2961
Staden R (1984) Computer methods to locate signals in nucleic acid sequences. Nucleic Acids Res 12:505–519
Staden R (1985) In: Setlow JK, Hollaender A (eds) Genetic engineering: Principles and methods. 7:67–114
Stewart AC, Bendall DS (1981) Properties of oxygen-evolving photosystem II particles from Phormidium laminosum, a thermophilic blue-green alga. Biochem J 194:877–887
Stewart AC, Ljungberg U, Åkerlund H-E, Andersson B (1985a) Studies on the polypeptide composition of the cyanobacterial oxygen-evolving complex. Biochim Biophys Acta 808:353–362
Stewart AC, Siczkowski M, Ljungberg U (1985b) Glycerol stabilizes oxygen evolution and maintains binding of a 9 kDa polypeptide in photosystem II particles from the cyanobacterium Phormidium laminosum. FEBS Lett 193:175–179
Tomioka N, Sugiura M (1983) The complete nucleotide sequence of a 16S ribosomal RNA gene from a blue-green alga, Anacystis nidulans. Mol Gen Genet 191:46–50
Tyagi A, Hermans J, Steppuhn J, Jansson Ch, Vater F, Hermann RG (1987) Nucleotide sequence of cDNA clones encoding the complete “33 kDa” precursor protein associated with the photosynthetic oxygen-evolving complex from spinach. Mol Gen Genet 207:288–293
von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683–4690
Wachter E, Machleidt W, Hofner H, Otto J (1973) Aminopropyl glass and its p-phenylene diisothiocyanate derivative, a new support in solid-phase Edman degradation of peptides and proteins. FEBS Lett 35:97–102
Zimmerman CL, Appella E, Pisano JJ (1977) Rapid analysis of amino acid phenylthiohydantoins by high-performance liquid chromatography. Anal Biochem 77:569–573
Author information
Authors and Affiliations
Additional information
Communicated by D.M. Lonsdale
Rights and permissions
About this article
Cite this article
Wallace, T.P., Stewart, A.C., Pappin, D. et al. Gene sequence for the 9 kDa component of Photosystem II from the cyanobacterium Phormidium laminosum indicates similarities between cyanobacterial and other leader sequences. Mol Gen Genet 216, 334–339 (1989). https://doi.org/10.1007/BF00334373
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00334373