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Reconstitution of the spinach oxygen-evolving complex with recombinant Arabidopsis manganese-stabilizing protein

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Abstract

The psbO gene of cyanobacteria, green algae and higher plants encodes the precursor of the 33 kDa manganese-stabilizing protein (MSP), a water-soluble subunit of photosystem II (PSII). Using a pET-T7 cloning/expression system, we have expressed in Escherichia coli a full-length cDNA clone of psbO from Arabidopsis thaliana. Upon induction, high levels of the precursor protein accumulated in cells grown with vigorous aeration. In cells grown under weak aeration, the mature protein accumulated upon induction. In cells grown with moderate aeration, the ratio of precursor to mature MSP decreased as the optical density at induction increased. Both forms of the protein accumulated as inclusion bodies from which the mature protein could be released under mildly denaturing conditions that did not release the precursor. Renatured Arabidopsis MSP was 87% as effective as isolated spinach MSP in restoring O2 evolution activity to MSP-depleted PSII membranes from spinach; however, the heterologous protein binds to spinach PSIIs with about half the affinity of the native protein. We also report a correction to the previously published DNA sequence of Arabidopsis psbO (Ko et al., Plant Mol Biol 14 (1990) 217–227).

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References

  1. Aro E-M, Virgin I, Andersson B: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134 (1993).

    Google Scholar 

  2. Berthold DA, Babcock GT, Yocum CF: A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties. FEBS Lett 134: 231–234 (1981).

    Google Scholar 

  3. Bowden GA, Georgiou G: Folding and aggregation of β-lactamase in the periplasmic space of Escherichia coli. J Biol Chem 265: 16760–16766 (1990).

    Google Scholar 

  4. Bricker TM: Oxygen evolution in the absence of the 33-kilodalton manganese-stabilizing protein. Biochemistry 31: 4623–4628 (1992).

    Google Scholar 

  5. Burnap R, Shen J-R, Jursinic PA, Inoue Y, Sherman LA: Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese-stabilizing protein of photosystem II. Biochemistry 31: 7404–7410 (1992).

    Google Scholar 

  6. Claassen LA, Ahn B, Koo H-S, Grossman L: Construction of deletion mutants of the Escherichia coli UvrA protein and their purification from inclusion bodies. J Biol Chem 266: 11380–11387 (1991).

    Google Scholar 

  7. Debus RJ: The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352 (1992).

    Google Scholar 

  8. Ghanotakis DF, Babcock GT: Hydroxylamine as an inhibitor between Z and P680 in photosystem II. FEBS Lett 153: 231–234 (1983).

    Google Scholar 

  9. Ghanotakis DF, Babcock GT, Yocum CF: Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted photosystem II preparations. FEBS Lett 167: 127–130 (1984).

    Google Scholar 

  10. Ghanotakis DF, Babcock GT, Yocum CF: Structural and catalytic properties of the oxygen-evolving complex: correlation of polypeptide and manganese release with the behavior of Z in chloroplasts and a highly resolved preparation of the PSII complex. Biochim Biophys Acta 765: 388–398 (1984).

    Google Scholar 

  11. Ghanotakis DF, Yocum CF: Photosystem II and the oxygen-evolving complex. Annu Rev Plant Physiol Plant Mol Biol 41: 255–276 (1990).

    Google Scholar 

  12. Halpin C, Elderfield PD, James HE, Zimmermann R, Dunbar B, Robinson C: The reaction specificities of the thylakoidal processing peptidase and Escherichia coli leader peptidase are identical. EMBO J 8: 3917–3921 (1989).

    Google Scholar 

  13. Harlow E, Lane D: Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1988).

    Google Scholar 

  14. Imaoka A, Yanagi M, Akabori K, Toyoshima Y: Reconstitution of photosynthetic charge accumulation and oxygen evolution in CaCl2-treated PSII particles. FEBS Lett 176: 341–345 (1984).

    Google Scholar 

  15. Kaback HR: Active transport in Escherichia coli: passage to permease. Annu Rev Biophys Chem 15: 279–319 (1986).

    Google Scholar 

  16. Ko K, Cashmore AR: Targeting of proteins to the thylakoid lumen by the bipartite transit peptide of the 33 kd oxygen-evolving protein. EMBO J 9: 3187–3194 (1989).

    Google Scholar 

  17. Ko K, Granell A, Bennett J, Cashmore AR: Isolation and characterization of cDNAs from Lycopersicon esculentum and Arabidopsis thaliana encoding the 33 kDa protein of the photosystem II-associated oxygen-evolving complex. Plant Mol Biol 14: 217–227 (1990).

    Google Scholar 

  18. Kuwabara T, Miyao M, Murata T, Murata N: The function of 33-kDa protein in the photosynthetic oxygenevolution system studied by reconstitution experiments. Biochim Biophys Acta 806: 283–289 (1985).

    Google Scholar 

  19. Lowry OH, Rosebrough NJ, Farr AL, Randall RL: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275 (1951).

    Google Scholar 

  20. Marston FAO: The purification of eukaryotic polypeptides expressed in Escherichia coli. In: Glover DM (ed) DNA Cloning: A Practical Approach, Vol. 1, pp 59–87. IRL Press, Oxford (1984).

    Google Scholar 

  21. Mayes SR, Cook KM, Self SJ, Zhang Z, Barber J: Deletion of the gene encoding the photosystem II 33 kDa protein from Synechocystis PCC 6803 does not inactivate water-splitting but increases vulnerability to photoinhibition. Biochim Biophys Acta 1060: 1–12 (1991).

    Google Scholar 

  22. Meadows JW, Robinson C: The full precursor of the 33 kDa oxygenevolving complex protein of wheat is exported by Escherichia coli and processed to the mature size. Plant Mol Biol 17: 1241–1243 (1991).

    Google Scholar 

  23. Miyao M, Murata N: Partial reconstitution of the photosynthetic oxygen evolution system by rebinding of the 33-kDa polypeptide. FEBS Lett 164: 375–378 (1983).

    Google Scholar 

  24. Miyao M, Murata N: Role of the 33-kDa polypeptide in preserving Mn in the photosynthetic oxygen-evolution system and its replacement by chloride ions. FEBS Lett 170: 350–354 (1984).

    Google Scholar 

  25. Miyao M, Murata N: The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the photosystem II complex of spinach. Biochim Biophys Acta 977: 315–321 (1989).

    Google Scholar 

  26. Miyao M, Murata N, Lavorel J, Maison-Peteri B, Boussac A, Etienne A-L: Effect of the 33-kDa protein on the S-state transitions in photosynthetic oxygen evolution. Biochim Biophys Acta 890: 151–159 (1987).

    Google Scholar 

  27. Noren GH, Boerner RJ, Barry BA: EPR characterization of an oxygen-evolving photosystem II preparation from transformable cyanobacterium Synechocystis 6803. Biochemistry 30: 3943–3950 (1991).

    Google Scholar 

  28. Oh-oka H, Tanaka S, Wada K, Kuwabara T, Murata N: Complete amino acid sequence of 33 kDa protein isolated from spinach photosystem II particles. FEBS Lett 197: 63–66 (1986).

    Google Scholar 

  29. Ono T-A, Inoue Y: Reconstitution of photosynthetic oxygen evolving activity by rebinding of 33 kDa protein to CaCl2− extracted PS II particles. FEBS Lett 166: 381–384 (1984).

    Google Scholar 

  30. Ono T-A, Inoue Y: Effects of removal and reconstitution of the extrinsic 33, 24 and 16 kDa proteins on flash oxygen yield in photosystem II particles. Biochim Biophys Acta 850: 380–389 (1986).

    Google Scholar 

  31. Philbrick JB, Diner BA, Zilinskas BA: Construction and characterization of cyanobacterial mutants lacking the manganesestabilizing polypeptide of photosystem II. J Biol Chem 266: 13370–13376 (1991).

    Google Scholar 

  32. Piccioni R, Bellemare G, Chua N-H: Methods of polyacrylamide gel electrophoresis in the analysis and preparation of plant polypeptides. In: Edelman M, Hallick RB, Chua N-H (eds) Methods in Chloroplast Molecular Biology, pp. 985–1014. Elsevier Biomedical Press, Amsterdam (1982).

    Google Scholar 

  33. Sanger R, Nicklen S, Coulsen AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74, 5463–5467 (1977).

    Google Scholar 

  34. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW: Use of T7 RNA polymerase to direct expression of cloned genes. Meth Enzymol 185: 60–89 (1990).

    Google Scholar 

  35. Tanaka S, Wada K: The status of cysteine residues in the extrinsic 33 kDa protein of spinach photosystem II complexes. Photosyn Res 17: 255–266 (1988).

    Google Scholar 

  36. Tang X-S, Satoh K: Reconstitution of photosynthetic water-splitting activity by the addition of 33 kDa polypeptide to urea-treated PS II reaction center complex. FEBS Lett 201: 221–224 (1986).

    Google Scholar 

  37. Waggoner CM, Pecoraro V, Yocum CF: Monovalent cations (Na+, K+, Cs+) inhibit calcium activation of photosynthetic oxygen evolution. FEBS Lett 244: 237–240 (1989).

    Google Scholar 

  38. Xu Q, Bricker TM: Structural organization of proteins on the oxidizing side of photosystem II: two molecules of the 33-kDa manganese-stabilizing proteins per reaction center. J Biol Chem 267: 25816–25821 (1992).

    Google Scholar 

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Betts, S.D., Hachigian, T.M., Pichersky, E. et al. Reconstitution of the spinach oxygen-evolving complex with recombinant Arabidopsis manganese-stabilizing protein. Plant Mol Biol 26, 117–130 (1994). https://doi.org/10.1007/BF00039525

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  • DOI: https://doi.org/10.1007/BF00039525

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