Skip to main content
SpringerLink
Log in

Expression of two nuclear genes encoding chloroplast proteins during early development of cucumber seedlings

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Cloned complementary DNA probes have been used to measure steady-state transcript levels for the small subunit of ribulose bisphosphate carboxylase-oxygenase (SSU) and the chlorophyll a/b-binding protein (LHCP) in cotyledons during early development of cucumber seedlings. Initial accumulation of trancripts to SSU occurs 2d after germination and is independent of light and developmentally programmed. Although transcripts accumulate in dark-grown tissues, their levels increase rapidly in light-grown cotyledons from day 4, coinciding with emergence above the soil, so that by day 6 levels are 2.4 times higher in light-grown compared with dark-grown cotyledons. In contrast, accumulation of transcripts to LHCP occurs only in light-grown cotyledons. Southern blot analysis of genomic DNA indicates that in cucumber there are one and two genes encoding SSU and LHCP, respectively, considerably fewer than in those other plant species that have been examined. Both LHCP genes are expressed in light-grown cotyledons.

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

Abbreviations

cDNA:

complementary DNA

kb:

kilobasepairs

LHCP:

light-harvesting chlorophyll a/b-binding protein

poly(A)+RNA:

polyadenylated RNA

SSU:

small subunit of ribulose bisphosphate carboxylase-oxygenase

References

  • Apel, K., Kloppstech, K. (1978) 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

    Google Scholar 

  • Bankier, A.T., Barrell, B.G. (1983) Shotgun DNA sequencing. In: Techniques in the life sciences, vol. B5: Nucleic acid biochemistry. Elsevier/North Holland Scientific, Ireland

    Google Scholar 

  • Becker, W.M., Leaver, C.J., Weir, E.M., Reizman, H. (1978) Regulation of glyoxysomal enzymes during germination of cucumber. I. Developmental changes in cotyledonary protein, RNA and enzyme activities during germination. Plant Physiol. 62, 542–549

    Google Scholar 

  • Bedbrook, J.R., Smith, S.M., Ellis, R.J. (1980) Molecular cloning and sequencing of cDNA encoding the precursor to the small subunit of chloroplast ribulose-1,5-bisphosphate carboxylase. Nature 287, 692–697

    Google Scholar 

  • Birnboim, H.C., Doly, J. (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7, 1513–1523

    Google Scholar 

  • Broglie, R., Bellemare, G., Bartlett, S., Chua, N.-H., Cashmore, A. (1981) Cloned DNA sequences complementary to mRNAs encoding precursor to the small subunit of ribulose-1,5-bisphosphate carboxylase and a chlorophyll a/b binding protein. Proc. Natl. Acad. Sci. USA 78, 7304–7308

    Google Scholar 

  • Broglie, R., Coruzzi, G., Lamppa, G., Keith, B., Chua, N.-H. (1983) Structural analysis of nuclear genes coding for the precursor to the small subunit of wheat ribulose-1,5-bisphosphate carboxylase. Bio/Technology 1, 55–61

    Google Scholar 

  • Butler, W.L. (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu. Rev. Plant Physiol. 29, 345–378

    Google Scholar 

  • Cashmore, A.R. (1984) Structure and expression of a pea nuclear gene encoding a chlorophyll a/b-binding protein. Proc. Natl. Acad. Sci. USA 81, 2960–2964

    Google Scholar 

  • Cashmore, A.R., Szabo, L., Timko, M., Kausch, A., Van den Broeck, G., Schreirer, P., Bohnert, H., Herrera-Estrella, L., Van Montagu, M., Schell, J. (1985) Import of proteins into chloroplasts. Bio/Technology 3, 803–808

    Google Scholar 

  • Chirgwin, J.M., Przybyla, A.E., MacDonald, R.J., Rutter, W.J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonucleic acid. Biochemistry 18, 5294–5299

    Google Scholar 

  • Coruzzi, G., Broglie, R., Cashmore, A., Chua, N.-H. (1983) Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose 1,5-bisphosphate carboxylase and the major chlorophyll a/b-binding thylakoid polypeptide. J. Biol. Chem. 258, 1399–1402

    Google Scholar 

  • Covey, S.N., Hull, R. (1981) Transcription of cauliflower mosaic virus DNA. Detection of trancripts, properties, and location of the gene encoding the virus inclusion body protein. Virology 111, 463–474

    Google Scholar 

  • Cuming, A.C., Bennett, J. (1981) Biosynthesis of the light-harvesting chlorophyll a/b protein. Control of messenger RNA activity by light. Eur. J. Biochem. 118, 71–80

    Google Scholar 

  • Dean, C., Leech, R.M. (1982) Genome expression during normal leaf development. 2. Direct correlation between ribulose bisphosphate content and nuclear ploidy in a polyploid series of wheat. Plant Physiol. 70, 1605–1608

    Google Scholar 

  • Dean, C., Van den Elzen, P., Tamaki, S., Dunsmuir, P., Bedbrook, J. (1985) Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multi-gene family. Proc. Natl. Acad. Sci. USA 82, 4964–4968

    Google Scholar 

  • Dunsmuir, P. (1985) The petunia chlorophyll a/b binding protein genes: a comparison of Cab genes from different gene families. Nucleic Acids Res. 13, 2503–2518

    Google Scholar 

  • Dunsmuir, P., Smith, S.M., Bedbrook, J. (1983) The major chlorophyll a/b binding protein of petunia is composed of several polypeptides encoded by a number of distinct nuclear genes. J. Mol. Appl. Genet. 2, 285–300

    Google Scholar 

  • Ellis, R.J. (1981) Chloroplast proteins: synthesis, transport and assembly. Annu. Rev. Plant Physiol. 32, 111–137

    Google Scholar 

  • Ellis, R.J., Gallagher, T.F., Jenkins, G.I., Lennox, C.R. (1984) Photoregulation of the biosynthesis of ribulose bisphosphate carboxylase. J. Embryol. Exp. Morph. 83, Suppl., 163–178

    Google Scholar 

  • Feinberg, A.P., Vogelstein, B. (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13

    Google Scholar 

  • Fitzgerald, M., Shenk, T. (1981) The sequence 5′-AAUAAA-3′ forms part of the recognition site for polyadenylation of late SV40 mRNAs. Cell 24, 251–260

    Google Scholar 

  • Gallagher, T.F., Ellis, R.J. (1982) Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J. 1, 1493–1498

    Google Scholar 

  • Glazer, A.N. (1983). Comparative biochemistry of photosynthetic light-harvesting systems. Annu. Rev. Biochem. 52, 125–157

    Google Scholar 

  • Gollmer, I., Apel, K. (1983) The phytochrome-controlled accumulation of mRNA sequences encoding the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare L.) Eur. J. Biochem. 133, 309–313

    Google Scholar 

  • Gubler, U., Hoffman, B.J. (1983) A simple and very efficient method for generating cDNA libraries. Gene 25, 263–269

    Google Scholar 

  • Holland, I.B., Pritchard, R.H. (1985) Basic cloning techniques, p. 14–50, Blackwell Scientific Publications. Oxford

    Google Scholar 

  • Jenkins, G.I., Hartley, M.R., Bennett, J. (1983) Photoregulation of chloroplast development: transcriptional, translational and post-translational controls. Phil. Trans. R. Soc. London Ser. B 303, 419–431

    Google Scholar 

  • Jenkins, G.I., Gallagher, T.F., Hartley, M.R., Bennett, J., Ellis, R.J. (1984) Photoregulation of gene expression during chloroplast biogenesis. In: Advances in photosynthesis research vol. IV, pp. 863–872, Sybesma, C., ed. Junk, The Hague

    Google Scholar 

  • Jenkins, G.I., Smith, H. (1985) Red: far red ratio does not modulate the abundance of transcripts for two major chloroplast polypeptides in light-grown Pisum sativum terminal shoots. Photochem. Photobiol. 42, 679–684

    Google Scholar 

  • Kohorn, B.D., Harel, E., Chitnis, P.R., Thornber, J.P., Tobin, E.M. (1986) Functional and mutational analysis of the light-harvesting chlorophyll a/b protein of thylakoid membranes. J. Cell Biol. 102, 972–981

    Google Scholar 

  • Lamppa, G.K., Morelli, G., Chua, N.-H. (1985) Structure and developmental regulation of a wheat gene encoding the major chorophyll a/b binding polypeptide. Mol. Cell. Biol. 5, 1370–1378

    Google Scholar 

  • Maniatis, T., Fritsch, E.F., Sambrook, J. (1982) Molecular cloning. A laboratory manual, Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Miziorko, H.M., Lorimer, G.H. (1983) Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu. Rev. Biochem. 52, 507–535

    Google Scholar 

  • Morelli, G., Nagy, F., Fraley, R.T., Rogers, S.G., Chua, N.-H. (1985) A short conserved sequence is involved in the light-inducibility of a gene encoding ribulose 1,5-bisphosphate carboxylase small subunit of pea. Nature 315, 200–204

    Google Scholar 

  • Nelson, T., Harpster, M.H., Mayfield, S.P., Taylor, W.C. (1984) Light-regulated gene expression during maize leaf development. J. Cell. Biol. 98, 558–564

    Google Scholar 

  • Sanger, F., Nicklen, S., Coulsen, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5476

    Google Scholar 

  • Smith, S.M., Ellis, R.J. (1981) Light-stimulated accumulation of transcripts of nuclear and chloroplast genes for ribulose bisphosphate carboxylase. J. Mol. Appl. Genet. 1, 127–137

    Google Scholar 

  • Stark, M.J.R., Mileham, A.J., Romanos, M.A., Boyd, A. (1984) Nucleotide sequence and transcription analysis of a linear DNA plasmid associated with the killer character of the yeast Kluyveromyces lactis. Nucleic Acids Res. 12, 6011–6030

    Google Scholar 

  • Stiekema, W.J., Wimpee, C.F., Silverthorne, J., Tobin, E. (1983) Phytochrome control of the expression of two nuclear genes encoding chloroplast proteins in Lemna gibba L. G-3. Plant Physiol. 72, 717–724

    Google Scholar 

  • Thompson, W.F., Everett, M., Polans, N.O., Jorgensen, R.A., Palmer, J.D. (1983) Phytochrome control of RNA levels in developing pea and mung-bean leaves. Planta 158, 487–500

    Google Scholar 

  • Timko, M.P., Kausch, A.P., Castresana, C., Fassler, J., Herrera-Estrella, L., Van den Broeck, G., Van Montagu, M., Schell, J., Cashmore, A.R. (1985) Light-regulation of plant gene expression by an upstream enhancer-like element. Nature 318, 579–582

    Google Scholar 

  • Tobin, E.M. (1981) Phytochrome-mediated regulation of messenger RNAs for the small subunit of ribulose 1,5-bisphosphate carboxylase and the light-harvesting chlorophyll a/b protein in Lemna gibba. Plant Molec. Biol. 1, 35–51

    Google Scholar 

  • Tobin, E.M., Silverthorne, J. (1985) Light regulation of gene expression in higher plants. Annu. Rev. Plant Physiol. 36, 569–593

    Google Scholar 

  • Walden, R. (1979) Synthesis of chloroplast proteins during germination and early development of cucumber (Cucumis sativus). Ph. D. thesis, University of Edinburgh

  • Walden, R., Leaver, C.J. (1981) Synthesis of chloroplast proteins during germination and early development of cucumber. Plant Physiol. 67, 1090–1096

    Google Scholar 

Download references

Author information

Author notes

  1. A. J. Greenland

    Present address: ICI Plant Biotechnology Group, Seed Support Laboratories, Jealotts Hill Research Station, RG12 6EY, Bracknell, Berks, UK

Authors and Affiliations

  1. Leicester Biocentre, University of Leicester, University Road, LE1 7RH, Leicester, UK

    A. J. Greenland, M. V. Thomas & R. M. Walden

Authors
  1. A. J. Greenland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. V. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. M. Walden
    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

Greenland, A.J., Thomas, M.V. & Walden, R.M. Expression of two nuclear genes encoding chloroplast proteins during early development of cucumber seedlings. Planta 170, 99–110 (1987). https://doi.org/10.1007/BF00392386

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00392386

Key words

Search

Navigation