Skip to main content
SpringerLink
Log in

Transiently expressed early light-inducible thylakoid proteins share transmembrane domains with light-harvesting chlorophyll binding proteins

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The early light-inducible proteins (ELIPs) of barley chloroplasts are encoded in two multigene families yielding end products of different molecular mass. Sequencing of complete cDNA clones showed that the low and high molecular mass proteins differ by the presence or absence of a 65 amino acid peptide in the amino-terminal part of the mature proteins. Two domains of the ELIPs reveal striking similarity in amino acid sequence with two transmembrane domains of all known light-harvesting chlorophyll a/b-binding proteins from photosystem I and II and may be of importance in anchoring the polypeptides in the membrane.

The cDNA sequences of two low molecular mass ELIPs differ by an insert of 5 codons in the putative transit peptide. By in vitro transcription and translation of the cloned DNA and subsequent transport of the products into chloroplasts it could be established that the two precursors are processed into products of identical apparent molecular mass. In vitro translated ELIPs were incorporated into thylakoid membranes both as precursors and mature polypeptides. It is suggested that ELIPs are pigment-free substitutes for light-harvesting polypeptides in the assembly of photosynthetic units during early development of thylakoids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. 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 

  2. Barkadottir RB, Jensen BF, Kreiberg JD, Nielsen PS, Gausing K: Expression of selected nuclear genes during leaf development in barley. Developm Genet 8: 495–511 (1987).

    Google Scholar 

  3. Birnboim HC, Doly J: A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl Acids Res 7: 1513–1523 (1979).

    PubMed  Google Scholar 

  4. 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 

  5. Chitnis PR, Harel E, Kohorn BD, Tobin EM, Thornber JP: Assembly of the precursor and processed light-harvesting chlorophyll a/b protein of Lemna into the light-harvesting complex II of barley etiochloroplasts. J Cell Biol 102: 982–988 (1986).

    Article  PubMed  Google Scholar 

  6. Chitnis PR, Morishige DT, Nechushtai R, Thorner JP: Assembly of the barley light-harvesting chlorophyll a/b proteins in barley etiochloroplasts involves processing of the precursor on thylakoids. Plant Mol Biol 11: 95–107 (1988).

    Google Scholar 

  7. Cline K: Import of proteins into chloroplasts: membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem 261: 14804–14810 (1986).

    PubMed  Google Scholar 

  8. Droppa M, Ghirardi ML, Horvath G, Melis A: Chlorphyll b deficiency in soybean mutants. II. Thylakoid membrane development and differentiation. Biochim Biophys Acta 932: 138–145 (1988).

    Google Scholar 

  9. 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 

  10. 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).

    PubMed  Google Scholar 

  11. Heinje Gv, Steppuhn J, Herrmann RG: Domaine structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535–545 (1989).

    PubMed  Google Scholar 

  12. Heintze H, Herzfeld F, Kiper M: Light-induced appearance of polysomal poly(A)-rich messenger RNA during greening of barley plants. Eur J Biochem 111: 137–144 (1980).

    PubMed  Google Scholar 

  13. Hinz UG, Welinder KG: The light-harvesting complex of photosystem II in barley. Structure and chlorophyll organization. Carlsberg Res Commun 52: 39–54 (1987).

    Google Scholar 

  14. Hoffman NE, Pichersky E, Malik VS, Castresana C, Ko K, Darr SC, Cashmore AR: The nucleotide sequence of a tomato cDNA clone encoding a photosystem I protein with homology to photosystem II chlorophyll a/b-binding polypeptides. Proc Natl Acad Sci USA 84: 8844–8843 (1987).

    PubMed  Google Scholar 

  15. Katz L, Kingbury ET, Helinski DR: Stimulation of cyclic adenosine monophoshate of plasmid deoxyribonucleic acid replication and catabolite repression of the plasmid deoxyribonucleic acid-protein relaxation complex. J Bact 114: 577–591 (1973).

    PubMed  Google Scholar 

  16. Karlin-Neumann GA, Tobin EM: Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J 5: 9–13 (1986).

    PubMed  Google Scholar 

  17. Karlin-Neumann GA, Kohorn BD, Thornber JP, Tobin EM: A chlorophyll a/b-protein encoded by a gene containing an Intron with characteristics of a transp posable element. J Mol Appl Genet 3: 45–61 (1985).

    PubMed  Google Scholar 

  18. 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 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  21. Kolanus W, Scharnhorst C, Kühne U, Herzfeld F: The structure and light-dependent transient expression of a nuclear-encoded chloroplast protein gene from pea (Pisum sativum L.). Mol Gen Genet 209: 234–239 (1987).

    Article  Google Scholar 

  22. Kyte J, Doolittle RF: A simple method of displaying the hydropathic character of a protein. J Mol Biol 157: 105–132 (1982).

    PubMed  Google Scholar 

  23. Lamppa GK, Morelli G, Chua NH: Structure and developmental regulation of a wheat gene encoding the major chlorophyll a/b-binding polypeptide. Mol Cell Biol 5: 1370–1378 (1985).

    Google Scholar 

  24. Leutwiler LS, Meyerowitz EM, Tobin EM: Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucl Acids Res 14: 4051–4064 (1986).

    PubMed  Google Scholar 

  25. Maniatis T, Frisch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  26. 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 

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

    PubMed  Google Scholar 

  28. 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 

  29. Pichersky E, Hoffman NE, Bernatzky R, Piechulla B, Tanksley SD, Cashmore AR: Molecular characterization and genetic mapping of DNA sequences encoding the type I chlorophyll a/b-binding polypeptide of photosystem I in Lycopersicon esculentum (tomato). Plant Mol Biol 9: 205–216 (1987).

    Google Scholar 

  30. 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 

  31. Rogers S, Wells R, Rechsteiner M: Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science 234: 364–368 (1986).

    PubMed  Google Scholar 

  32. 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 

  33. Sanger F, Nicklen S, Coulson AR: Sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  34. Scharnhorst C, Heintze H, Meyer G, Kolanus W, Bartsch K, Heinrichs S, Gudschun T, Möller M, Herzfeld F: Molecular cloning of a pea mRNA encoding an early light induced, nuclear coded chloroplast protein. Plant Mol Biol 4: 241–245 (1985).

    Google Scholar 

  35. Stayton MM, Brosio P, Dunsmuir P: Characterization of a full-length petunia cDNA encoding a polypeptide of the light-harvesting complex associated with photosystem I. Plant Mol Biol 10: 127–137 (1987).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  38. Yanish-Perron C, Vieira J, Messing J: Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103–109 (1985).

    Article  PubMed  Google Scholar 

  39. Zuber H: Structure of light-harvesting antenna complexes of photosynthetic bacteria, cyanobacteria and red algae. TIBS 11: 414–419 (1986).

    Google Scholar 

Download references

Author information

Author notes

  1. Bernhard Grimm

    Present address: Department of Physiology, Carlsberg Laboratory, Gamle Carlsberg Vej 10, 2500, Copenhagen-Valby, Denmark

Authors and Affiliations

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

    Bernhard Grimm, Elisabeth Kruse & Klaus Kloppstech

Authors
  1. Bernhard Grimm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisabeth Kruse
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Klaus Kloppstech
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

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). https://doi.org/10.1007/BF00027318

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00027318

Key words

Search

Navigation