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Developmental, circadian and light regulation of wheat ferredoxin gene expression

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Abstract

A genomic clone encoding the precursor of wheat leaf ferredoxin has been isolated and characterised. The uninterrupted PetF gene encodes a polypeptide of 143 amino acid residues, consisting of an N-terminal presequence of 46 amino acid residues and a mature polypeptide of 97 amino acid residues. Southern blot analysis suggests that six copies of the PetF gene are present in the wheat haploid genome. Northern blot analysis has shown that the genes are both developmentally and light regulated in wheat seedlings and provides evidence that a circadian rhythm regulates the steady-state levels of ferredoxin transcripts. The intact wheat gene and several chimeric constructs, containing portions of the 5′-upstream region fused to the β-glucuronidase reporter gene, have been introduced into tobacco plants, but levels of β-glucuronidase activity above background were not detected, suggesting that the 5′-upstream region is unable to function as a promoter in tobacco plants.

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References

  1. Arnon DI: The discovery of ferredoxin: the photosynthetic path. Trends Biochem Sci 13: 30–37 (1988).

    Google Scholar 

  2. Berk AJ, Sharp PA: Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease digested hybrids. Cell 12: 721–732 (1977).

    Google Scholar 

  3. Bevan MW: Binary Agrobacterium vectors for plant transformation. Nucl Acids Res 12: 179–185 (1984).

    Google Scholar 

  4. Caspar T, Quail PH: Promoter and leader regions involved in the expression of the Arabidopsis ferredoxin A gene. Plant J 3: 161–174 (1993).

    Google Scholar 

  5. Cseke C, Buchanan BB: Regulation of the formation and utilization of photosynthate in leaves. Biochim Biophys Acta 853: 43–63 (1986).

    Google Scholar 

  6. Decottignes P, Schmitter J-M, Migniac-Maslow M, Le Marechal P, Jacquot J-P, Gadal P: Primary structure of the light-dependent regulatory site of corn NADP-malate dehydrogenase. J Biol Chem 263: 11780–11785 (1988).

    Google Scholar 

  7. Dickey LF, Gallo-Meagher M, Thompson WF: Light regulatory sequences are located within the 5′ portion of the Fed-1 message sequence. EMBO J 11: 2311–2317 (1992).

    Google Scholar 

  8. Dobres MS, Elliott RC, Watson JC, Thompson WF: A phytochrome regulated pea transcript encodes ferredoxin I. Plant Mol Biol 8: 53–59 (1987).

    Google Scholar 

  9. Elliott RC, Dickey LF, White MJ, Thompson WF: Cis-acting elements for light regulation of pea ferredoxin-1 gene expression are located within transcribed sequences. Plant Cell 1: 691–698 (1989).

    Google Scholar 

  10. Elliott RC, Pedersen TJ, Fritensky B, White MJ, Dickey LF, Thompson WF: Characterisation of a single-copy gene encoding ferredoxin-1 from pea. Plant Cell 1: 681–690 (1989).

    Google Scholar 

  11. Ellis JG, Llewellyn DJ, Dennis ES, Peacock WJ: Maize ADH-1 promoter sequences control anaerobic regulation: addition of upstream promoter elements from constitutive genes is necessary for expression in tobacco. EMBO J 6: 11–16 (1987).

    Google Scholar 

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

    Google Scholar 

  13. Gallo-Meagher M, Sowinski DA, Thompson WF: The pea ferredoxin I gene exhibits different light responses in pea and tobacco. Plant Cell 4: 383–388 (1992).

    Google Scholar 

  14. Gallo-Meagher M, Sowinski DA, Elliott RC, Thompson WF: Both internal and external regulatory elements control expression of the pea Fed-1 gene in transgenic tobacco seedlings. Plant Cell 4: 389–395 (1992).

    Google Scholar 

  15. Gavel Y, vonHeijne G: A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett 261: 455–458 (1990).

    Google Scholar 

  16. Gilmartin PM, Sarokin L, Memelink J, Chua N-H: Molecular light switches for plant genes. Plant Cell 2: 369–378 (1990).

    Google Scholar 

  17. Henikoff S: Unidirectional digestion with exonuclease III in DNA sequence analysis. Meth Enzymol 155: 156–165 (1987).

    Google Scholar 

  18. Horsch RB, Fry JE, Hoffman N, Eichholtz D, Rogers SG, Fraley RT: A simple and general method of transferring genes into plants. Science 227: 1229–1231 (1985).

    Google Scholar 

  19. Hosler JP, Yocum CF: Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport. Plant Physiol 83: 965–969 (1987).

    Google Scholar 

  20. Huisman JG, Bernards A, Liebregts P, Gebbink MGT, Stegwee D: Qualitative and quantitative immunofluorescence studies of chloroplast ferredoxin. Planta 137: 279–286 (1977).

    Google Scholar 

  21. Huisman JG, Gebbink MGT, Moddermann P, Stegwee D: The coding site of chloroplast ferredoxin. Planta 137: 97–105 (1977).

    Google Scholar 

  22. Huisman JG, Moorman AFM, Verkley FN: In vitro synthesis of chloroplast ferredoxin as a high molecular weight precursor in a cell-free protein synthesizing system from wheat germs. Biochem Biophys Res Commun 82: 1121–1131 (1978).

    Google Scholar 

  23. Jefferson RA: Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5: 387–405 (1987).

    Google Scholar 

  24. Jefferson RA, Kavanagh TA, Bevan MW: GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).

    Google Scholar 

  25. Kaufman LS, Roberts LL, Briggs WR, Thompson WF: Phytochrome control of specific mRNA levels in developing pea buds: kinetics of accumulation, reciprocity and escape kinetics of the low fluence response. Plant Physiol 81: 1033–1038 (1986).

    Google Scholar 

  26. Kaufman LS, Briggs WR, Thompson WF: Phytochrome control of specific mRNA levels in developing pea buds. Plant Physiol 78: 388–393 (1985).

    Google Scholar 

  27. Keith B, Chua N-H: Monocot and dicot pre-mRNAs are processed with different efficiencies in transgenic tobacco. EMBO J 5: 2419–2425 (1986).

    Google Scholar 

  28. Kwanyuen P, Wildman SG: Nuclear DNA codes for Nicotiana ferredoxin. Biochim Biophys Acta 405: 167–174 (1975).

    Google Scholar 

  29. Lamppa G, Morelli G, Chua N-H: 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 

  30. Leech RM: Stability and plasticity during chloroplast development. In: Jennings DH, Trewavas AJ (eds) Plasticity in Plants, pp. 121–155. Company of Biologists, Cambridge (1986).

    Google Scholar 

  31. 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).

    Google Scholar 

  32. Lissmore JL, Quail PH: Rapid transcriptional regulation of the genes for phytochrome and cab in Avena sativa. Mol Cell Biol 8: 4840–4850 (1988).

    Google Scholar 

  33. Lloyd JC, Raines CA, John UP, Dyer T: The chloroplast FBPase gene of wheat: structure and expression of the promoter in photosynthetic and meristematic cells of transgenic tobacco plants. Mol Gen Genet 225: 209–216 (1991).

    Google Scholar 

  34. Marcus F: Moberly L, Latshaw SP: Comparative amino acid sequence of FBPases: identification of a region unique to the light regulated chloroplast enzyme. Proc Natl Acad Sci USA 85: 5379–5383 (1988).

    Google Scholar 

  35. Millar AJ, Kay SA: Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell 3: 541–550 (1991).

    Google Scholar 

  36. Murphy G, Kavanagh TA: Speeding-up the sequencing of double-stranded DNA. Nucl Acids Res 16: 5198 (1988).

    Google Scholar 

  37. Nagy F, Kay SA, Chua N-H: A circadian clock regulates transcription of the wheat cab-1 gene. Genes Devel 2: 376–382 (1988).

    Google Scholar 

  38. Raines CA, Lloyd JC, Longstaff M, Bradley D, Dyer T: Chloroplast fructose-1,6-bisphosphatase: the product of a mosaic gene. Nucl Acids Res 16: 7931–7942 (1988).

    Google Scholar 

  39. Robert LS, Thompson RD, Flavell RB: Tissue-specific expression of a high molecular weight glutenin gene in transgenic tobacco. Plant Cell 1: 569–578 (1989).

    Google Scholar 

  40. Sakihama N, Shin M: Evidence from HPLC for the existence of two ferredoxins in higher plants. Arch Biochem Biophys 256: 430–434 (1987).

    Google Scholar 

  41. Sakihama N, Shin M, Toda H: Separation and identification of two native forms of spinach ferredoxin by hydrophobic chromatography. J Biochem 100: 43–47 (1986).

    Google Scholar 

  42. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  43. Sager AD, Horwitz BA, Elliott RC, Thompson WF, Briggs WR: Light effects on several chloroplast components in norflurazon-treated pea seedlings. Plant Physiol 88: 340–347 (1988).

    Google Scholar 

  44. Sanger F, Coulson AR, Barrell BG, Smith AJH, Roe BA: Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol 143: 161–178 (1980).

    Google Scholar 

  45. Shen W-J, Forde BG: Efficient transformation of Agrobacterium spp. by high voltage electroporation. Nucl Acids Res 17: 8385 (1989).

    Google Scholar 

  46. Smeekens S, Bauerle C, Hageman J, Keegstra K, Weisbeek P: The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46: 365–375 (1986).

    Google Scholar 

  47. Smeekens S, Geerts D, Bauerle C, Weisbeek P: Essential function in chloroplast recognition of the ferredoxin transit peptide processing region. Mol Gen Genet 216: 178–182 (1989).

    Google Scholar 

  48. Smeekens S, vanBinsbergen J, Weisbeek P: The plant ferredoxin precursor: nucleotide sequence of a full length cDNA clone. Nucl Acids Res 13: 3179–3194 (1985).

    Google Scholar 

  49. Smeekens S, vanSteeg H, Bauerle C, Bettenbroek H, Keegstra K, Weisbeek P: Import into chloroplasts of a yeast mitochondrial protein directed by ferredoxin and plastocyanin transit peptides. Plant Mol Biol 9: 377–388 (1987).

    Google Scholar 

  50. Somers DE, Casper T, Quail PH: Isolation and characterization of a ferredoxin gene from Arabidopsis thaliana. Plant Physiol 93: 572–577 (1990).

    Google Scholar 

  51. Takruri I, Boulter D: The amino acid sequence of ferredoxin from Triticum aestivum (wheat). Biochem J 179: 373–378 (1979).

    Google Scholar 

  52. van derMark F, van denBriel W, Huisman HG: Phytoferritin is synthesised in vitro as a high molecular weight precursor. Biochem J 214: 943–950 (1983).

    Google Scholar 

  53. vonHeijne G, Steppuhn J, Herrmann RG: Domain structure of mitochondrial and chloroplast targetting peptides. Eur J Biochem 180: 535–545 (1989).

    Google Scholar 

  54. Vorst O, vanDam F, Oosterhoff-Teertstra R, Smeekens S, Weisbeek P: Tissue-specific expression directed by an Arabidopsis thaliana preferredoxin promoter in transgenic tobacco plants. Plant Mol Biol 14: 491–499 (1990).

    Google Scholar 

  55. Vorst O, vanDam F, Weisbeek P, Smeekens S: Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-translational processes. Plant J 3: 793–803 (1993).

    Google Scholar 

  56. Weaver RF, Weismann C: Mapping of RNA by a modification of the Berk-Sharp procedure: the 5′ termini of the 15S β-globin mRNA precursor and mature 10S β-globin mRNA have identical map coordinates. Nucl Acids Res 7: 1175–1193 (1979).

    Google Scholar 

  57. Wedel N, Bartling D, Herrmann RG: Analysis of cDNA clones encoding the entire ferredoxin precursor polypeptide from spinach. Bot Acta 101: 295–300 (1988).

    Google Scholar 

  58. Weising K, Kahl G: Towards an understanding of plant gene regulation: the action of nuclear factors. Z Naturforsch 46c: 1–11 (1991).

    Google Scholar 

  59. Yang N-S, Russell D: Maize sucrose synthase-1 promoter directs phloem cell-specific expression of GUS gene in transgenic tobacco plants. Proc Natl Acad Sci USA 87: 4144–4148 (1990).

    Google Scholar 

  60. Young RA, Davis RW: Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci USA 80: 1194–1198 (1983).

    Google Scholar 

  61. Young RA, Davis RW: Yeast RNA polymerase II genes: isolation with antibody probes. Science 222: 778–782 (1983).

    Google Scholar 

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Bringloe, D.H., Dyer, T.A. & Gray, J.C. Developmental, circadian and light regulation of wheat ferredoxin gene expression. Plant Mol Biol 27, 293–306 (1995). https://doi.org/10.1007/BF00020184

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