Skip to main content
SpringerLink
Log in

Phytochrome regulation of mRNA levels of ribulose-1,5-bisphosphate carboxylase in etiolated rye seedlings (Secale cereale)

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The effect of red light and far-red light on the appearance of mRNA for the small and large subunit of ribulose-1,5-bisphosphate carboxylase in rye seedlings has been analysed. Irradiation of etiolated seedlings with a pulse of red light increased the mRNA level of the small subunit by a factor of 7–10 and that of the large subunit by a factor of 3. A pulse of far-red light resulted in a much lower, but measurable increase. The effect of red light is reverted by an immediate far-red pulse, demonstrating the classical phytochrome response.In vitro transcription experiments with nuclei isolated from red light-treated seedlings showed that the transcription rate of the small subunit mRNA was increased only by a factor of 1.5–2.5, indicating posttranscriptional as wells as transcriptional regulations of the small subunit of ribulose-1,5-bisphosphate carboxylase.

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. Batschauer A, Mösinger E, Kreuz K, Dörr I, Apel K: The implication of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b protein. Eur J Biochem 154: 625–634 (1986).

    Google Scholar 

  2. Bedbrook J, Kolodner R: The structure of chloroplast DNA. Ann Rev Plant Physiol 30: 593–620 (1979).

    Google Scholar 

  3. Bennett J, Jenkins GI, Hartley MR: Differential regulation of the accumulation of the light-harvesting chlorophyll a/b complex and ribulose bisphosphate carboxylase/oxygenase in greening pea leaves. In: Thornber JP, Staehelin LA, Hallick RB (eds) Biosynthesis of the Photosynthetic Apparatus. Molecular Biology, Development and Regulation. Alan R. Liss Inc., New York (1984) pp 211–223.

    Google Scholar 

  4. Berry JO, Nikolau BJ, Carr JP, Klessig DF: Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol 5: 2238–2246 (1985).

    Google Scholar 

  5. Berry-Lowe SA, Meagher RB: Transcriptional regulation of a gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean tissue is linked to the phytochrome response. Mol Cell Biol 5: 1910–1917 (1985).

    Google Scholar 

  6. Berry-Lowe SL, McKnight TD, Shah DM, Meagher RB: The nucleotide sequence, expression and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J Mol Appl Genet 1: 483–498 (1982).

    Google Scholar 

  7. Birnbaum HC, Doly J: A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7: 1513–1523 (1981).

    Google Scholar 

  8. Broglie R, Corruzi G, Lamppa G, Keith B, Chua N-H: 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 (1983).

    Google Scholar 

  9. Chappell J, Hahlbrock K: Transcription of plant defence genes in response to UV light or fungal elicitor. Nature 311: 76–78 (1984).

    Google Scholar 

  10. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ: Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299 (1981).

    Google Scholar 

  11. Chua N-H, Schmidt GW: Post-translational transport into intact chloroplasts of a precursor to the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 75: 6110–6114 (1978).

    Google Scholar 

  12. Coen DM, Bedbrook JR, Bogorad L, Rich A: Maize chloroplast DNA fragment encoding the large subunit of ribulose bisphosphate carboxylase. Proc Natl Acad Sci USA 74: 5487–5491 (1977).

    Google Scholar 

  13. Colbert JT, Hershey HP, Quail PH: Phytochrome regulation of mRNA abundance. Plant Mol Biol 5: 91–101 (1985).

    Google Scholar 

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

    Google Scholar 

  15. Darnell JE: Variety in the level of gene control in eukaryotic cells. Nature 297: 365–371 (1982).

    Google Scholar 

  16. Dean C, Leech RM: The co-ordinated synthesis of the large and small subunits of ribulose bisphosphate carboxylase during early cellular development within a seven day wheat leaf. FEBS Lett 140: 113–116 (1982).

    Google Scholar 

  17. Donnis-Keller H, Maxam AM, Gilbert W: Mapping adenines, guanines and pyrimidines in RNA. Nucleic Acids Res 4: 2527–2538 (1977).

    Google Scholar 

  18. Dunsmair P, Smith S, Bedbrook J: A number of different nuclear genes for the small subunit of RuBPcase are transcribed in petunia. Nucleic Acids Res 11: 4177–4183 (1983).

    Google Scholar 

  19. Dynan WS, Tjian R: Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature 316: 774–777 (1985).

    Google Scholar 

  20. Ellis RJ: The most abundant protein in the world. TIBS 11: 241–244 (1979).

    Google Scholar 

  21. Ellis RJ: Chloroplast proteins: synthesis, transport and assembly. Ann Rev Plant Physiol 32: 111–137 (1981).

    Google Scholar 

  22. Ernst D, Oesterhelt D: Purified phytochrome influencesin vitro transcription in rye nuclei. EMBO J 3: 3075–3078 (1984).

    Google Scholar 

  23. Evans MI, Gatehouse JA, Croy RRD, Boulter D: Regulation of the transcription of storage-protein mRNA in nuclei isolated from developing pea (Pisum sativum L.) cotyledons. Planta 160: 559–568 (1984).

    Google Scholar 

  24. Fourcroy P, Klein-Eude D, Lambert C: Phytochrome control of gene expression in radish seedlings. Plant Sci Lett 37: 235–244 (1985).

    Google Scholar 

  25. Furuya M: Molecular properties of phytochrome. Phil Trans R Soc Lond B 303: 361–375 (1983).

    Google Scholar 

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

    Google Scholar 

  27. Gallagher TF, Jenkins GI, Ellis RJ: Rapid modulation of transcription of nuclear genes encoding chloroplast proteins by light. FEBS Lett 186: 241–245 (1985).

    Google Scholar 

  28. Gollmer I, Apel K: 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 (1983).

    Google Scholar 

  29. Gubler U, Hoffman BJ: A simple and very efficient method for generating cDNA libraries. Gene 25: 263–269 (1983).

    Google Scholar 

  30. Highfield DE, Ellis RJ: Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271: 420–424 (1978).

    Google Scholar 

  31. Inamine G, Nash B, Weissbach H, Brot N: Light regulation of the synthesis of the large subunit of ribulose-1,5-bisphosphate carboxylase in peas: Evidence for translational control. Proc Natl Acad Sci USA 82: 5690–5694 (1985).

    Google Scholar 

  32. Jenkins GI, Hartley MR, Bennett J: Photoregulation of chloroplast development: transcriptional, translational and post-translational controls? Phil Trans R Soc Lond B 303: 419–431 (1983).

    Google Scholar 

  33. Kaufman LS, Thompson WF, Briggs WR: Different red light requirements for phytochrome-induced accumulation of cab RNA and rbcS RNA. Science 226: 1447–1449 (1984).

    Google Scholar 

  34. Kerscher L: Subunit size, absorption spectra and dark kinetics of rye phytochrome purified in the far-red absorbing form. Plant Sci Lett 32: 133–138 (1983).

    Google Scholar 

  35. Kleinkopf GE, Huffaker RC, Matheson A: Light-induced de novo synthesis of ribulose-1,5-diphosphate carboxylase in greening leaves of barley. Plant Physiol 46: 416–418 (1970).

    Google Scholar 

  36. Lagarias JC: Progress in the molecular analysis of phytochrome. Photochem Photobiol 42: 811–820 (1985).

    Google Scholar 

  37. Link G: Phytochrome control of plastid mRNA in mustard (Sinapis alba L.). Planta 154: 81–86 (1982).

    Google Scholar 

  38. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  39. Mandoli DF, Briggs WR: Phytochrome control of two low-irradiance responses in etiolated oat seedlings. Plant Physiol 67: 733–739 (1981).

    Google Scholar 

  40. Marzluff WF, Huang RCC: Transcription of RNA in isolated nuclei. In: Hames BD, Higgins SJ (eds) Transcription and Translation. IRL Press, Oxford/Washington (1984) pp 89–129.

    Google Scholar 

  41. Melton DA, Krieg PA, Rebagliati MR, Maniatis T, Zinn K, Green MR: Efficientin vitro synthesis of biologically active RNA and RNA hybridization probes from plasmid containing a Bacteriophage SP6 promoter. Nucleic Acids Res 12: 7035–7056 (1984).

    Google Scholar 

  42. Michelson AM, Orkin SH: Characterization of the homopolymer tailing reaction catalyzed by terminal deoxynucleotide transferase. J Biol Chem 257: 14773–14782 (1981).

    Google Scholar 

  43. Miller ME, Jurgenson JE, Reardon EM, Price CA: Plastid translationin organello andin vitro during light-induced development inEuglena. J Biol Chem 258: 14478–14484 (1983).

    Google Scholar 

  44. Mishkind ML, Schmidt GW: Posttranscriptional regulation of ribulose-1,5-bisphosphate carboxylase small subunit inChlamydomonas reinhardtii. Plant Physiol 72: 847–854 (1983).

    Google Scholar 

  45. Miziorka HM, Lorimer GH: Ribulose-1,5-bisphosphate carboxylase-oxygenase. Ann Rev Biochem 52: 507–535 (1983).

    Google Scholar 

  46. Mösinger E, Schäfer E:In vivo phytochrome control ofin vitro transcription rates in isolated nuclei from oat seedlings. Planta 161: 444–450 (1984).

    Google Scholar 

  47. Mösinger E, Batschauer A, Schäfer E, Apel K: Phytochrome control ofin vitro transcription of specific genes in isolated nuclei from barley (Hordeum vulgare). Eur J Biochem 147: 137–142 (1985).

    Google Scholar 

  48. Nelson T, Harpster MH, Mayfield SP, Taylor WC: Light-regulated gene expression during maize leaf development. J Cell Biol 98: 558–564 (1984).

    Google Scholar 

  49. Nichols SE, Laties GG: Ethylene-regulated gene transcription in carrot roots. Plant Mol Biol 3: 393–401 (1984).

    Google Scholar 

  50. Nivison HT, Stocking CR: Ribulose bisphosphate carboxylase synthesis in barley leaves. Plant Physiol 73: 906–911 (1983).

    Google Scholar 

  51. Oelmüller R, Mohr H: Mode of action between blue/UV light and light adsorbed by phytochrome in light-mediated anthocyanin formation in the milo (Sorghum vulgare Pers.) seedling. Proc Natl Acad Sci USA 82: 6124–6128 (1985).

    Google Scholar 

  52. Palatnik CM, Storti RV, Jacobsen A: Fractionation and functional analysis of newly synthesized and decaying messenger RNA from vegetative cells ofDictyostelium discoideum. J Mol Biol 128: 371–398 (1981).

    Google Scholar 

  53. Peacock SL, McIver CM, Monohan JJ: Transformation ofE. coli using homopolymer-linked plasmid chimers. Biochim Biophys Acta 655: 243–250 (1981).

    Google Scholar 

  54. Possingham JV: Plastid replication and development in the life cycle of higher plants. Ann Rev Plant Physiol 31: 113–129 (1980).

    Google Scholar 

  55. Quail PH, Colbert JT, Hershey HP, Vierstra RD: Phytochrome: molecular properties and biogenesis. Phil Trans R Soc Lond B 303: 387–402 (1983).

    Google Scholar 

  56. Quail PH, Colbert JT, Peters NK, Christensen AH, Sharrock RA, Lissemore LJ: Phytochrome and the regulation of the expression of its genes. Phil Trans R Soc Lond B 314: 469–480 (1986).

    Google Scholar 

  57. Richter G, Wessel K: Red light inhibits blue light-induced chloroplast development in cultured plant cells at the mRNA level. Plant Mol Biol 5: 175–182 (1985).

    Google Scholar 

  58. Rodermel SR, Bogorad L: Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development. J Cell Biol 100: 463–470 (1985).

    Google Scholar 

  59. Rüdiger W: Chemistry of phytochrome photoconversions. Phil Trans R Soc Lond B 303: 377–386 (1983).

    Google Scholar 

  60. Sasaki Y, Ishiye M, Sakahima T, Kamikubo T: Light-induced increase of mRNA activity coding for the small subunit of ribulose-1,5-bisphosphate carboxylase. J Biol Chem 256: 2315–2320 (1981).

    Google Scholar 

  61. Sasaki Y, Sakahima T, Kamikubo T, Shinozaki K: Phytochrome-mediated regulation of two mRNAs, encoded by nuclei and chloroplasts of ribulose-1,5-bisphosphate carboxylase/oxygenase. Eur J Biochem 133: 617–620 (1983).

    Google Scholar 

  62. Sasaki Y, Tomoda Y, Kamikubo T: Light regulates the gene expression of ribulosebisphosphate carboxylase at the levels of transcription and gene dosage in greening pea leaves. FEBS Lett 173: 31–35 (1984).

    Google Scholar 

  63. Sasaki Y, Tomoda Y, Tomi H, Kamikubo T, Shinozaki K: Synthesis of ribulose bisphosphate carboxylase in greening pea leaves. Eur J Biochem 152: 179–186 (1985).

    Google Scholar 

  64. Sasaki Y, Nakamura Y, Matsuno R: Phytochrome-mediated accumulation of chloroplast DNA in pea leaves. FEBS Lett 196: 171–174 (1986).

    Google Scholar 

  65. Schenborn ET, Mierendorf RC: A novel transcription property of SP6 and T7 TNA polymerases. Nucleic Acids Res 13: 6223–6236 (1985).

    Google Scholar 

  66. Shinozaki K, Sasaki Y, Sakihama T, Kamikubo T: Coordinate light-induction of two mRNAs, encoded in nuclei and chloroplasts, of ribulose 1,5-bisphosphate carboxylase/oxygenase. FEBS Lett 144: 73–76 (1982).

    Google Scholar 

  67. Simpson J, VanMontagu M, Herrera-Estrella L: Photosynthesis-associated gene families: differences in response to tissue-specific and environmental factors. Science 233: 34–38 (1986).

    Google Scholar 

  68. Silverthorne J, Tobin EM: Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc Natl Acad Sci USA 81: 1112–1116 (1984).

    Google Scholar 

  69. Smith SM, Ellis RJ: Light-stimulated accumulation of transcripts of nuclear and chloroplast genes for ribulose-bisphosphate carboxylase. J Mol Appl Gen 1: 127–137 (1981).

    Google Scholar 

  70. Stiekema WJ, Wimpee CF, Silverthorne J, Tobin EM: Phytochrome control of the expression of two nuclear genes encoding chloroplast proteins inLemna gibba L. G-3. Plant Physiol 72: 717–724 (1983).

    Google Scholar 

  71. Thomas PC: Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci USA 77: 5201–5205 (1980).

    Google Scholar 

  72. Thompson WF, Everett M, Polans NO, Jorgensen RA: Phytochrome control of RNA levels in developing pea and mung-bean leaves. Planta 158: 487–500 (1983).

    Google Scholar 

  73. Tobin EM: Phytochrome-mediated regulation of messenger RNAs for the small subunit of ribulose 1,5-bisphosphate carboxylase and the light-harvesting chlorophyll a/b-protein inLemna gibba. Plant Mol Biol 1: 35–51 (1981).

    Google Scholar 

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

    Google Scholar 

  75. Tobin EM, Wimpee CF, Silverthorne J, Stiekema WJ, Neumann GA, Thornber JP: Phytochrome regulation of the expression of two nuclear-coded chloroplast proteins. In: Thornber JP, Staehelin LA, Hallick RB (eds) Biosynthesis of the Photosynthetic Apparatus. Molecular Biology, Development and Regulation. Alan R. Liss Inc., New York (1984) pp 325–334.

    Google Scholar 

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

    Google Scholar 

  77. Zhu YS, Kung SD, Bogorad L: Phytochrome control of levels of mRNA complementary to plastid and nuclear genes of maize. Plant Physiol 79: 371–376 (1985).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Max-Planck-Institut für Biochemie, 8033, Martinsried, FRG

    D. Ernst, F. Pfeiffer, K. Schefbeck, C. Weyrauch & D. Oesterhelt

Authors
  1. D. Ernst
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Pfeiffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Schefbeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Weyrauch
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. Oesterhelt
    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

Ernst, D., Pfeiffer, F., Schefbeck, K. et al. Phytochrome regulation of mRNA levels of ribulose-1,5-bisphosphate carboxylase in etiolated rye seedlings (Secale cereale). Plant Mol Biol 10, 21–33 (1987). https://doi.org/10.1007/BF00014183

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00014183

Key words

Search

Navigation