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Evidence for an association of the early light-inducible protein (ELIP) of pea with photosystem II

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Abstract

The precursor to the nuclear-coded 17 kDa early light-inducible protein (ELIP) of pea has been transported into isolated intact chloroplasts. The location of the mature protein in the thylakoid membranes was investigated after using cleavable crosslinkers such as DSP and SAND in conjunction with immuno-fractionation methods and by application of mild detergent fractionation. We show that ELIP is integrated into the membranes via the unstacked stroma thylakoids. After isolation of protein complexes by solubilization of membranes with Triton X-100 and sucrose density-gradient centrifugation the crosslinked ELIP comigrates with the PS II core complex. Using SAND we identified ELIP as a 41–51 kDa crosslinked product while with DSP four products of 80 kDa, 70 kDa, 50–42 kDa and 23–21 kDa were found. The immunoprecipitation data suggested that the D1-protein of the PS II complex is one of the ELIP partners in crosslinked products.

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Abbreviations

chl:

chlorophyll

D1 :

herbicide-binding protein

DSP:

dithiobis-(succinimidylpropionate)

ELIP:

early light-inducible protein

LHC I and LHC II:

light-harvesting chlorophyll a/b complex associated with photosystem I or II

PAGE:

polyacrylamide gel electrophoresis

poly(A)-rich RNA:

polyadenyd mRNA

PS I and PS II:

photosystems I and II

SAND:

sulfosuccinimidyl 2-(m-azido-o-nitro-benzamido)-ethyl-1,3′-dithiopropionate

Triton X-100:

octylphenoxypolyethoxyethanol

References

  1. Akoyunoglou A, Akoyunoglou G: Mechanism of thylakoid reorganization during chloroplast development in higher plants. Israel J Bot 33: 149–162 (1984).

    Google Scholar 

  2. Akoyunoglou G, Argyroudi-Akoyunoglou JH: Organization of the photosynthetic units, and onset of electron transport and excitation energy distribution in greening leaves. Photosynth Res 10: 171–180 (1986).

    Google Scholar 

  3. Akoyunoglou G, Argyroudi-Akoyunoglou JH: Posttranslational regulation of chloroplast differentiation. In: Akoyunoglou G, Senger H (eds) Regulation of Chloroplast Differentiation, pp. 571–582. Alan R. Liss, New York (1986).

    Google Scholar 

  4. Apel K, Kloppstech K: The plastid membranes of barley (Hordeum vulgare). Light-induced appearance of mRNA coding for the apoprotein of the light-harvesting chlorophyll a/b protein. Eur J Biochem 85: 581–588 (1978).

    PubMed  Google Scholar 

  5. Bogorad L: Chloroplasts. J Cell Biol 91: 256–270 (1981).

    Article  Google Scholar 

  6. Bonner WM, Laskey RA: A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem 46: 83–88 (1974).

    PubMed  Google Scholar 

  7. Cullen SE, Schwartz BD: An improved method for isolation of H-2 and IA alloantigens with immunoprecipitation induced by protein A bearing Staphylococci. J Immunol 117: 136–142 (1976).

    PubMed  Google Scholar 

  8. Cuming AC, Bennett J: Biosynthesis of the lightharvesting chlorophyll a/b protein. Control of messenger RNA activity by light. Eur J Biochem 118: 71–80 (1981).

    PubMed  Google Scholar 

  9. DeBlas AL, Czerwinski HM: Detection of antigens on nitrocellulose paper immunoblots with monoclonal antibodies. Anal Biochem 133: 214–219 (1983).

    PubMed  Google Scholar 

  10. Douce R, Joyard J: Structure and function of the plastid envelope. Adv Bot Res 7: 1–116 (1979).

    Google Scholar 

  11. Enami I, Satoh K, Katoh S: Crosslinking between the 33 kDa extrinsic protein and the 47 kDa chlorophyll carrying protein of the PS II reaction center core complex. FEBS Lett 226: 161–165 (1987).

    Article  Google Scholar 

  12. Fluhr R, Kuhlemeier C, Nagy F, Chua NH: Organ-specific and light induced expression of plant genes. Science 232: 1106–1112 (1986).

    Google Scholar 

  13. Fromm H, Devic M, Fluhr R, Edelman M: Control of psbA gene expression in mature Spirodela chloroplasts: Light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J 4: 291–295 (1985).

    Google Scholar 

  14. Gallagher TF, Ellis RJ: Light-stimulated transciption of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J 1: 1493–1498 (1982).

    Google Scholar 

  15. Grimm B, Kloppstech K: The early light inducible proteins of barley. Characterization of two families of 2-h-specific nuclear-coded chloroplast proteins. Eur J Biochem 167: 493–499 (1987).

    PubMed  Google Scholar 

  16. Grimm B, Kruse E, Kloppstech K: Transiently expressed early light-inducible thylakoid proteins share transmembrane domains with light-harvesting chlorophyll binding proteins. Plant Mol Biol 13: 583–593 (1989).

    Google Scholar 

  17. Grossman AR, Bartlett SG, Schmidt GW, Mullet JE, Chua NH: Optimal conditions for post-translational uptake of proteins by isolated chloroplasts. J Biol Chem 257: 1558–1563 (1982).

    Google Scholar 

  18. Holger JH, Kaplan S: Topology and neighbour analysis of the photosynthetic reaction centre from Rhodopseudomonas sphaeroides. J Biol Chem 260: 6932–6937 (1985).

    PubMed  Google Scholar 

  19. Ji TH: The application of chemical crosslinking for studies on cell membranes and the identification of surface reporters. Biochim Biophys Acta 559: 39–69 (1979).

    PubMed  Google Scholar 

  20. Kloppstech K: Diurnal and circadian rhythmicity in the expression of light-induced plant nuclear messenger RNAs. Planta 165: 502–506 (1985).

    Google Scholar 

  21. Kloppstech K, Meyer G, Bartsch K, Hundrieser J, Link G: Control of gene expression during the early phase of chloroplast development. In: Wiesner W, Robinson DG, Starr RC (eds) Compartments in algal cells and their interaction, pp. 36–46. Springer-Verlag, Berlin/Heidelberg/New York (1984).

    Google Scholar 

  22. Kloppstech K, Pfisterer J, Meyer G, Müller M: Control of expression of chloroplast membrane proteins in higher plants. In: Cell Function and Differentiation Part B: 101–110, Alan R. Liss, New York (1982).

    Google Scholar 

  23. Knack G, Otto B, Ottersbach P, Alexander R, Liu Z, Kloppstech K: Structure and possible function of chloroplast heat-shock proteins and effect of cyclic heat-shock on plastid morphogenesis and circadian rhythmicity. In: Baltscheffsky M (ed) Current Research in Photosynthesis, vol 6: 579–586. Martinus Nijhoff Publishers, The Netherlands (1990).

    Google Scholar 

  24. Kohorn BD, Harel E, Chitnis PR, Thornber JP, Tobin EM: Functional and mutational analysis of the light-harvesting chlorophyl a/b protein of thylakoid membranes. J Cell Biol 102: 972–981 (1986).

    Article  PubMed  Google Scholar 

  25. Lewis RV, Roberts MF, Dennis EA, Allison WS: Photoactivated heterobifunctional cross-linking reagents which demonstrate the aggregation state of phospholipase A2. Biochemistry 16: 5650–5654 (1977).

    PubMed  Google Scholar 

  26. Mattoo AK, Edelman M: Intermembrane translocation and posttranslational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proc Natl Acad Sci USA 84: 1497–1501 (1987).

    PubMed  Google Scholar 

  27. Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M: Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32 kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380–1384 (1984).

    Google Scholar 

  28. Mattoo AK, Pick U, Hoffman-Falk H, Edelman M: The rapidly metabolized 32000-dalton polypeptide of the chloroplast is the ‘proteinaceous shield’ regulating photosystem II electron transport and mediating diuron herbicide sensitivity. Proc Natl Acad Sci USA 78: 1572–1576 (1981).

    PubMed  Google Scholar 

  29. Meyer G: Untersuchungen zur differentiellen Genexpression in höheren Pflanzen: Das Auftreten kerngenomkodierter Chloroplastenproteine während der frühen Phase der Ergrünung und nach Hitzeschock. PhD thesis, Hannover, FRG (1986).

  30. Meyer G, Kloppstech K: A rapidly light-induced chloroplast protein with a high turnover coded for by pea nuclear DNA. Eur J Biochem 138: 201–207 (1984).

    PubMed  Google Scholar 

  31. Millner PA, Gogel G, Barber J: Investigation of the spatial relationships between photosystem 2 polypeptides by reversible crosslinking and diagonal electrophoresis. Photosynth Res 13: 185–198 (1987).

    Google Scholar 

  32. Neville DM: Molecular weight determination of protein-dodecyl-sulfate complexes by electrophoresis in discontinuous buffer system. J Biol Chem 246: 6328–6334 (1971).

    Google Scholar 

  33. Oakley BR, Kirsch DR, Morris RN: A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal Biochem 105: 361–363 (1980).

    PubMed  Google Scholar 

  34. Otto B, Grimm B, Ottersbach P, Kloppstech K: Circadian control of the accumulation of mRNAs for light- and heat-inducible chloroplast proteins in pea (Pisum sativum L.). Plant Physiol 88: 21–25 (1988).

    Google Scholar 

  35. Pemberton RE, Liberti PA, Baglioni C: Isolation of messenger RNA from polysomes by chromatography on oligo-(dT)-cellulose. Anal Biochem 66: 18–28 (1975).

    PubMed  Google Scholar 

  36. Pfisterer J, Lachmann P, Kloppstech K: Transport of proteins into chloroplasts. Binding of nuclear-coded chloroplast proteins to the chloroplast envelope. Eur J Biochem 126: 143–148 (1982).

    PubMed  Google Scholar 

  37. Poincelot RP: Isolation of chloroplast envelope membranes. Meth Enzymol 69: 121–128 (1980).

    Google Scholar 

  38. Ricciardi RP, Miller JS, Roberts BE: Purification and mapping of specific mRNAs by hybridization selection and cell-free translation. Proc Natl Acad Sci USA 76: 4927–4931 (1979).

    PubMed  Google Scholar 

  39. Roberts BE, Paterson BM: Efficient translation of tobacco mosaic virus RNA and globin 9S RNA in a cell-free system from commercial wheat-germ. Proc Natl Acad Sci USA 70: 2330–2334 (1973).

    PubMed  Google Scholar 

  40. Sane PV, Goodchild DJ, Park RB: Characterization of chloroplast PSI and II separated by a nondetergent method. Biochim Biophys Acta 216: 162–178 (1970).

    PubMed  Google Scholar 

  41. Schwartz MA, Das OP, Hynes RO: A new radioactive cross-linking reagent for studying the interactions of proteins. J Biol Chem 257: 2343–2349 (1982).

    PubMed  Google Scholar 

  42. Scopsi L, Larsson LI: Lucreased sensitivity in peroxidase immunocytochemistry; A comparative study of a number of peroxidase visualization methods employing a model system. Histochemistry 84: 221–230 (1986).

    PubMed  Google Scholar 

  43. Steinback KE, Mullet JE, Arntzen CJ: Fractionation of thylakoid membrane protein complexes by sucrose density-gradient centrifugation. In: Methods in Chloroplast Molecular Biology, 864–871. Elsevier Biomedical Press (1982).

  44. Tavladoraki P, Kloppstech K, Argyroudi-Akoyunoglou J: Circadian rhythm in the expression of the mRNA coding for the apoprotein of the light-harvesting complex of photosystem II. Plant Physiol 90: 665–672 (1989).

    Google Scholar 

  45. Tobin EM, Silverthorne J: Light regulation of gene expression in higher plants. Ann Rev Plant Physiol 36: 569–593 (1985).

    Google Scholar 

  46. Towbin H, Staehelin T, Gordon J: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4354 (1979).

    PubMed  Google Scholar 

  47. Uchiumi T, Terao K, Ogata K: Identification of neighboring protein pairs in rat liver 60S ribosomal subunits cross-linked with dimethyl suberimidate or dimethyl 3,3-dithiobispropionimidate. J Biochem 88: 1033–1044 (1980).

    PubMed  Google Scholar 

  48. Viro M, Kloppstech K: Differential expression of the genes for ribulose-1,5-bisphosphate carboxylase and light-harvesting chlorophyll a/b protein in the developing barley leaf. Planta 150: 41–45 (1980).

    Google Scholar 

  49. Viro M, Kloppstech K: Expression of genes for plastid membrane proteins in barley under intermittent light conditions. Planta 154: 18–23 (1982).

    Google Scholar 

  50. Wang K, Richards FM: An approach to nearest neighbor analysis of membrane proteins. J Biol Chem 249: 8005–8018 (1974).

    PubMed  Google Scholar 

  51. Weber K, Osborn J: The reliability of molecular weight determinations by dodecylsulfate-polyacrylamide gel electrophoresis. J Biol Chem 244: 4406–4412 (1969).

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Institut für Botanik, Universität Hannover, Herrenhäuser Str. 2, 3000, Hannover 21, Germany

    Iwona Adamska & Klaus Kloppstech

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  1. Iwona Adamska
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  2. Klaus Kloppstech
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Adamska, I., Kloppstech, K. Evidence for an association of the early light-inducible protein (ELIP) of pea with photosystem II. Plant Mol Biol 16, 209–223 (1991). https://doi.org/10.1007/BF00020553

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  • DOI: https://doi.org/10.1007/BF00020553

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