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Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts

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Abstract

The nuclear gene mutant of barley, vir-115, shows a developmentally induced loss of D1 synthesis that results in inactivation of Photosystem II. Translation in plastids isolated from 1 h illuminated vir-115 seedlings is similar to wild type. In wild-type barley, illumination of plants for 16 to 72 h results in increased radiolabel incorporation into the D1 translation intermediates of 15–24 kDa. In contrast, these D1 translation intermediates were not observed in vir-115 plastids isolated from plants illuminated for 16–72 h. In addition, after 72 h of illumination, radiolabel incorporation into D1 was undetectable in vir-115 plastids. The level and distribution ofpsbA mRNA in membrane-associated polysomes was similar in wild-type and vir-115 mutant plastids isolated from plants illuminated for 16–72 h. Toeprint analysis showed similar levels of translation initiation complexes onpsbA mRNA in vir-115 and wild-type plastids. These results indicate that translation initiation and elongation of D1 is not significantly altered in the mutant plastids. Ribosome pausing onpsbA mRNA was observed in wild-type and vir-115 mutant plastids. Therefore, the absence of D1 translation intermediates in mutant plastids is not due to a lack of ribosome pausing onpsbA mRNA. Based on these results, it is proposed that vir-115 lacks or contains a modified nuclear-encoded gene product which normally stabilizes the D1 translation intermediates. In wild-type plastids, ribosome pausing and stabilization of D1 translation intermediates is proposed to facilitate assembly of cofactors such as chlorophyll will D1 allowing continued D1 synthesis and accumulation in mature chloroplasts.

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References

  1. Adamska I, Kloppstech K: Evidence for an association of the early light-inducible protein ELIP of pea with photosystem II. Plant Mol Biol 16: 209–224 (1991).

    Google Scholar 

  2. Adamska I, Kloppstech K, Ohad I. UV light stress induces the synthesis of the early light-inducible protein and prevents its degradation. J Biol Chem 267: 24732–24737 (1992).

    Google Scholar 

  3. Adamska I, Ohad I, Kloppstech K: Synthesis of the early light-inducible protein is controlled by blue light and related to light stress. Proc Natl Acad Sci USA 89: 2610–2613 (1992).

    Google Scholar 

  4. Allen JP, Feher G, Yeates TO, Komiya H, Rees DC: Structure of the reaction center fromRhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84: 6162–6166 (1987).

    Google Scholar 

  5. Barber J, Andersson B: Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66 (1992).

    Google Scholar 

  6. Baumgartner BJ, Rapp JC, Mullet JE: Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development. Plant Physiol 101: 781–791 (1993).

    Google Scholar 

  7. Bechmann RP, Mizzen LA, Welch WJ: Interaction of HSP 70 with newly synthesized proteins: implications for protein folding and assembly. Science 248: 850–854 (1990).

    Google Scholar 

  8. Deisenhofer J, Michel H: The photosynthetic reaction centre from the purple bacteriumRhodopseudomonas viridis. EMBO J 8: 2149–2170 (1989).

    Google Scholar 

  9. Deisenhofer J, Epp O, Miki K, Huber R, Michel H: Structure of the protein subunits in the photosynthetic reaction centre ofRhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624 (1985).

    Google Scholar 

  10. Eichacker I, Soll J, Lauterbach P, Rüdiger W, Klein RR, Mullet JE:In vitro synthesis of chlorophylla in the dark triggers accumulation of chlorophylla apoproteins in barley etioplasts. J Biol Chem 265: 13566–13571 (1990).

    Google Scholar 

  11. Feher G, Allen JP, Okamura MY, Rees C. Structure and function of bacterial photosynthetic reaction centres. Nature 339: 111–116 (1989).

    Google Scholar 

  12. Gamble PE, Mullet JE: Translation and stability of proteins encoded by the plastidpsbA andpsbB genes are regulated by a nuclear gene during light-induced chloroplast development in barley. J Biol Chem 264: 7236–7243 (1989).

    Google Scholar 

  13. Greenberg BM, Gaba V, Mattoo AK, Edelman M: Identification of a primaryin vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem EMBO J 6: 2865–2869 (1987).

    Google Scholar 

  14. Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK, Edelman M: Separate photosensitizers mediate degradation of the 32-kDa photosystem II reaction center protein in the visible and UV spectral regions. Proc Nalt Acad Sci USA 86: 6617–6620 (1989).

    Google Scholar 

  15. 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 

  16. Hartz D, McPheeters DS, Traut R, Gold L: Extension Inhibition Analysis of translation initiation complexes. Meth Enzymol 164: 419–425 (1988).

    Google Scholar 

  17. Kim J, Klein PG, Mullet JE: Ribosomes pause at specific sites during synthesis of membrane-bound chloroplast reaction center protein D1. J Biol Chem 266: 14931–14938 (1991).

    Google Scholar 

  18. Klein RR, Mullet JE: Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J Biol Chem 261: 14931–14938 (1991).

    Google Scholar 

  19. Klein RR, Mullet JE: Control of gene expression during higher plant chloroplast biogenesis. J Biol Chem 262: 4341–4348 (1987).

    Google Scholar 

  20. Klein RR, Gamble PE, Mullet JE: Light-dependent accumulation of radiolabeled plastid-encoded chlorophylla-apoproteins requires chlorophylla. Plant Physiol 88: 1246–1256 (1988).

    Google Scholar 

  21. Klein BR, Mason HS, Mullet JE: Light-regulated translation of chloroplast proteins. I. Transcripts ofpsaA-psaB, psbA andrbcL are associated with polysomes in dark-grown and illuminated barley seedlings. J Cell Biol 106: 289–301 (1988).

    Google Scholar 

  22. Marder JB, Goloubinoff P, Edelman M: Molecular architecture of the rapidly metabolized 32-kilodalton protein of photosystem II. J Biol Chem 259: 3900–3984 (1984).

    Google Scholar 

  23. Mattoo AK, Marder JB, Edelman M: Dynamics of the photosystem II reaction center. Cell 56: 241–246 (1989).

    Google Scholar 

  24. Melis A, Nemson JA, Harrison MA. Damage to functional components and partial degradation of photosystem II reaction center proteins upon chloroplast exposure to ultraviolet-B radiation. Biochim Biophys Acta 1100: 312–320 (1992).

    Google Scholar 

  25. Mullet JE, Klein RR, Grossman AR: Optimization of protein synthesis in isolated higher plant chloroplasts. Eur J Biochem 155: 331–338 (1986).

    Google Scholar 

  26. Mullet JE, Klein PG, Klein RR: Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc Natl Acad Sci USA 87: 4038–4042 (1990).

    Google Scholar 

  27. Ohad I, Kyle DJ, Hirschberg J: Light-dependent degradation of the QB-protein in isolated pea thylakoids. EMBO J 4: 1655–1659 (1985).

    Google Scholar 

  28. Poetter E, Kloppstech K. Effects of light stress on the expression of early ligh-inducible proteins in barley. Eur J Biochem 214: 779–786 (1993).

    Google Scholar 

  29. Rothman JE: Polypeptide chain binding proteins: catalysis of protein folding and related processes in cells. Cell 59: 591–601 (1989).

    Google Scholar 

  30. Salter AH, Virgin I, Hagman A, Andersson B: On the molecular mechanism of light-induced D1 protein degradation in photosystem II core particles. Biochemistry 31: 3990–3998 (1992).

    Google Scholar 

  31. Sayer RT, Andersson B, Bogorad L: The topology of a membrane protein: the orientation of the 32 kd Qbbinding chloroplast thylakoid membrane protein. Cell 47: 601–608 (1986).

    Google Scholar 

  32. Schmidt GW, Sieburth LE, Jensen KH, Greer KL, Plumley FG, Herrin DL: In: Biggins J (ed) Progress in Photosynthesis Research, vol. 4, pp. 637–644. Martinus Nijhoff Publishers, Dordrecht, Netherlands (1987).

    Google Scholar 

  33. Sexton TB, Christopher DA, Mullet JE: Light-induced switch in barleypsbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression. EMBO J 9: 4485–4494 (1990).

    Google Scholar 

  34. Shipton CA, Barber J: Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem: evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc Natl Acad Sci USA 88: 6691–6695 (1991).

    Google Scholar 

  35. Trebst A: The topology of the plastoquinone and herbicide binding peptides of photosystem II in the thylakoid membrane. Z Naturforsch 41C: 240–245 (1986).

    Google Scholar 

  36. Virgin I, Ghanotakis DF, Andersson B: Light-induced D1 protein degradation in isolated photosystem II core complexes. FEBS Lett 269: 45–48 (1990).

    Google Scholar 

  37. Yalorvsky S, Paulsen H, Michaeli D, Chinitis PR, Nechushtai R: Involvement of a chloroplast HSP70 heat shock protein in the integration of a protein (light-harvesting complex protein precursor) into the thylakoid membrane. Proc Natl Acad Sci USA 89: 5616–5619 (1992).

    Google Scholar 

  38. Wettern M, Galling G: Degradation of the 32-kilodalton thylakoid-membrane polypeptide ofChlamydomonas reinhardi Y-1. Planta 166: 474–482 (1985).

    Google Scholar 

  39. Yeates TO, Komiya H, Rees DC, Allen JP, Feher G: Structure of the reaction center fromRhodobacter sphaeroides R-26: membrane-protein interactions. Proc Natl Acad Sci USA 84: 6438–6442 (1987).

    Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry and Biophysics, Texas A&M University, 77843-2128, College Station, TX, USA

    Jungmook Kim & John E. Mullet

  2. Department of Horticulture and Landscape Architecture, University of Kentucky, 40546-0091, Lexington, KY, USA

    Patricia Gamble Klein

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  1. Jungmook Kim
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  2. Patricia Gamble Klein
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  3. John E. Mullet
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Kim, J., Klein, P.G. & Mullet, J.E. Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts. Plant Mol Biol 25, 459–467 (1994). https://doi.org/10.1007/BF00043874

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  • DOI: https://doi.org/10.1007/BF00043874

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