Light and plastid signals regulate the expression of the pea plastocyanin gene through a common region at the 5′ end of the coding region

Plant Journal

Volumn 43, Issue 4, 2005, Pages 541-552

  Brown, Naomi J ^a   Sullivan, James A ^a,b   Gray, John C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Chloroplast; Light regulation; PetE; Plastid signals; Plastocyanin; Post transcriptional

Indexed keywords

CROPS; CYTOLOGY; LIGHT; SEED; SIGNALING;

LIGHT REGULATION; PETE; PLASTID SIGNALS; PLASTOCYANIN; POST-TRANSCRIPTIONAL;

GENES;

CHLOROPHYLLS; CYTOLOGY; FARM CROPS; GENES; PLASTIDS; SEEDLINGS; TOBACCO;

ARABIDOPSIS; NICOTIANA TABACUM; PISUM SATIVUM;

PLASTOCYANIN;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CODON; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PEA; PHYSIOLOGY; PLASTID; SIGNAL TRANSDUCTION; TOBACCO; TRANSGENIC PLANT;

ARABIDOPSIS; CODON; GENE EXPRESSION REGULATION, PLANT; LIGHT; PEAS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PLASTOCYANIN; SIGNAL TRANSDUCTION; TOBACCO;

EID: 27144557648     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2005.02474.x     Document Type: Article

References (59)

1. Bechtold, N., Ellis, J. and Pelletier, G. (1993) In planta Agrobacterium-mediated gene-transfer by infiltration of adult Arabidopsis thaliana plants. Compt. Rend. Acad. Sci. Ser. III - Sci De La Vie-Life Sci. 316, 1194-1199.
2. Bevan, M. (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711-8721.
3. Bichler, J. and Herrmann, R.G. (1990) Analysis of the promoters of the single-copy genes for plastocyanin and subunit δ of the chloroplast ATP synthase from spinach. Eur. J. Biochem. 190, 415-426.
4. Bolle, C., Herrmann, R. and Oelmüller, R. (1996) Intron sequences are involved in the plastid-and light-dependent expression of the spinach PsaD gene. Plant J. 10, 919-924.
5. Chua, Y.L., Brown, A.P.C. and Gray, J.C. (2001) Targeted histone acetylation and altered nuclease accessibility over short regions of the pea plastocyanin gene. Plant Cell, 13, 599-612.
6. Chua, Y.L., Watson, L.A. and Gray, J.C. (2003) The transcriptional enhancer of the pea plastocyanin gene associates with the nuclear matrix and regulates gene expression through histone acetylation. Plant Cell, 15, 1468-1479.
7. Dickey, L.F., Gallo-Meagher, M. and Thompson, W.F. (1992) Light-regulatory sequences are located within the 5′ portion of the Fed-1 message sequence. EMBO J. 11, 2311-2317.
8. Dickey, L.F., Nguyen, T.-T., Allen, G.C. and Thompson, W.F. (1994) Light modulation of ferredoxin mRNA abundance requires an open reading frame. Plant Cell, 6, 1171-1176.
9. Dickey, L.F., Petracek, M.E., Nguyen, T.T., Hansen, E.R. and Thompson, W.F. (1998) Light regulation of Fed-1 mRNA requires an element in the 5′ untranslated region and correlates with differential polyribosome association. Plant Cell, 10, 475-484.
10. Elliott, R.C., Dickey, L.F., White, M.J. and Thompson, W.F. (1989) Cis-acting elements for light regulation of pea ferredoxin gene expression are located within transcribed sequences. Plant Cell, 1, 691-698.
11. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
12. Flieger, K., Wicke, A., Herrmann, R.G. and Oelmüller, R. (1994) Promoter and leader sequences of the spinach PsaD and PsaF genes direct an opposite light response in tobacco cotyledons: PsaD sequences downstream of the ATG codon are required for a positive light response. Plant J. 6, 359-368.
13. Frisch, D.A., Harris-Haller, L.W., Yokubaitis, N.T., Thomas, T.L., Hardin, S.H. and Hall, T.C. (1995) Complete sequence of the binary vector Bin19. Plant Mol. Biol. 27, 405-409.
14. Gallo-Meagher, M., Sowinski, D.A., Elliott, R.C. and Thompson, W.F. (1992) Both internal and external regulatory elements control expression of the pea Fed-1 gene in transgenic tobacco. Plant Cell, 4, 389-395.
15. Gorman, D.S. and Levine, R.P. (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 54, 1665-1669.
16. Gray, J.C., Sornarajah, R., Zabron, A.A., Duckett, C.M. and Khan, M.S. (1995) Chloroplast control of nuclear gene expression. In Photosynthesis: From Light to Biosphere, Vol. III (Mathis, P., ed.). Dordrecht: Kluwer Academic Publishers, pp. 543-550.
17. Gray, J.C., Sullivan, J.A., Wang, J.-H., Jerome, C.A. and MacLean, D. (2003) Coordination of plastid and nuclear gene expression. Phil. Trans. R. Soc. Lond. B, 358, 135-145.
18. Haehnel, W., Jansen, T., Gause, K., Klosgen, R.B., Stahl, B., Michl, D., Huvermann, B., Karas, M. and Herrmann, R.G. (1994) Electron transfer from plastocyanin to photosystem I. EMBO J. 13, 1028-1038.
19. Hahn, D. and Kück, V. (1999) Identification of DNA sequences controlling light- and chloroplast-dependent expression of the Lhcb1 gene from Chlamydomonas reinhardtii. Curr. Genet. 34, 459-466.
20. Hansen, E.R., Petracek, M.E., Dickey, L.F. and Thompson, W.F. (2001) The 5′ end of the pea ferredoxin-1 mRNA mediates rapid and reversible light-directed changes in translation in tobacco. Plant Physiol. 125, 770-778.
21. Helliwell, C.A. and Gray, J.C. (1995) The sequence surrounding the translation initiation codon of the pea plastocyanin gene increases translational efficiency of a reporter gene. Plant Mol. Biol. 29, 621-626.
22. Helliwell, C.A., Wesbter, C.I. and Gray, J.C. (1997) Light-regulated expression of the pea plastocyanin gene is mediated by elements within the transcribed region of the gene. Plant J. 12, 499-506.
23. Horsch, R.B., Fry, J.E., Hoffman, N.L., Eichholtz, D., Rogers, S.G. and Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science, 227, 1229-1231.
24. Jacobson, A. and Peltz, S.W. (1996) Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65, 693-739.
25. Katoh, S. (1960) A new copper protein from Chlorella ellipsoidea. Nature, 186, 533-534.
26. Katoh, S. and Takamiya, A. (1961) A new leaf copper protein 'plastocyanin', a natural Hill oxidant. Nature, 189, 665-666.
27. Kavanagh, T.A., Jefferson, R.A. and Bevan, M.W. (1988) Targeting a foreign protein to chloroplasts using fusions to the transit peptide of a chlorophyll a/b protein. Mol. Gen. Genet. 215, 38-45.
28. Kozak, M. (1978) How do eukaryotic ribosomes select initiation regions in messenger RNA? Cell, 15, 1109-1123.
29. Kozak, M. (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene, 209, 1-34.
30. Kusnetsov, V., Bolle, C., Lübberstedt, T., Sopory, S., Herrmann, R.G. and Oelmüller, R. (1996) Evidence that the plastid signal and light operate via the same cis-acting elements in the promoters of nuclear genes for plastid proteins. Mol. Gen. Genet. 252, 631-639.
31. Last, D.I. and Gray, J.C. (1989) Plastocyanin is encoded by a single-copy gene in the pea haploid genome. Plant Mol. Biol. 12, 655-666.
32. Last, D.I. and Gray, J.C. (1990) Synthesis and accumulation of pea plastocyanin in transgenic tobacco plants. Plant Mol. Biol. 14 229-238.
33. Ling, J., Wells, D.R., Tanguay, R.L., Dickey, L.F., Thompson, W.F. and Gallie, D.R. (2000) Heat shock protein HSP101 binds to the Fed-1 internal light regulatory element and mediates its high translational activity. Plant Cell, 12, 1213-1227.
34. Lübberstedt, T., Bolle, C.E.H., Sopory, S., Flieger, K., Herrmann, R.G. and Oelmüller, R. (1994a) Promoters from genes for plastid proteins possess regions with different sensitivities towards red and blue light. Plant Physiol. 104, 997-1006.
35. Lübberstedt, T., Oelmüller, R., Wanner, G. and Herrmann, R.G. (1994b) Interacting cis elements in the plastocyanin promoter from spinach ensure regulated high-level expression. Mol. Gen. Genet. 242, 602-613.
36. Lütcke, H.A., Chow, K.C., Mickel, F.C., Moss, K.A., Kern, H.F. and Scheele, G.A. (1987) Selection of AUG initiation codons differ in plants and animals. EMBO J. 6, 43-48.
37. Martínez-Hernández, A., López-Ochoa, L., Argüello-Astorga, G. and Herrera-Estrella, L. (2002) Functional properties and regulatory complexity of a minimal RBCS light-responsive unit activated by phytochrome, cryptochrome, and plastid signals. Plant Physiol. 128, 1223-1233.
38. McDowell, J.M., An, Y.-q., Shurong, H., McKinney, E.C. and Meagher, R.B. (1996) The Arabidopsis ACT7 actin gene is expressed in rapidly developing tissues and responds to several external stimuli. Plant Physiol. 111, 699-711.
39. Mochizuki, N., Brusslan, J.A., Larkin, R., Nagatani, A. and Chory, J. (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl Acad. Sci. USA, 98, 2053-2058.
40. i plasmids: analysis of T-DNA functions. Gene, 14, 33-50.
41. Oswald, O., Martin, T., Dominy, P.J. and Graham, I.A. (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc. Natl Acad. Sci. USA, 98, 2047-2052.
42. Parker, R. and Jacobson, A. (1990) Translation and a 42-nucleotide segment within the coding region of the mRNA encoded by the MATα1 gene are involved in promoting rapid mRNA decay in yeast. Proc. Natl Acad. Sci. USA, 87, 2780-2784.
43. Petracek, M.E., Dickey, L.F. and Thompson, W.F. (1997) Light-regulated changes in abundance and polyribosome association of ferredoxin are dependent on photosynthesis. Plant Cell, 9, 2291-2300.
44. Petracek, M.E., Dickey, L.F., Nguyen, T.T., Gatz, C., Sowinski, D.A., Allen, G.C. and Thompson, W.F. (1998) Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc. Natl Acad. Sci. USA, 95, 9009-9013.
45. Petracek, M.E., Nguyen, T.T., Thompson, W.F. and Dickey, L.F. (2000) Premature termination codons destabilize ferredoxin-1 mRNA when ferredoxin-1 is translated. Plant J. 21, 563-569.
46. Puente, P., Wei, N. and Deng, X.-W. (1996) Combinatorial interplay of promoter elements constituting the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 15, 3732-3743.
47. Pwee, K.-H. and Gray, J.C. (1993) The pea plastocyanin promoter directs cell-specific but not full light-regulated expression in transgenic tobacco plants. Plant J. 3, 437-449.
48. Schiavi, S.C., Wellington, C.L., Shyu, A.-B., Chen, C.-Y.A., Greenberg, M.E. and Belasco, J.G. (1994) Multiple elements in the c-fos protein-coding region facilitate mRNA deadenylation and decay by a mechanism coupled to translation. J. Biol. Chem. 269, 3441-3448.
49. Shen, W.J. and Forde, B.G. (1989) Efficient transformation of Agrobacterium spp. by high-voltage electroporation. Nucleic Acids Res. 17, 8385.
50. Sherameti, I., Nakamura, M., Yamamoto, Y.Y., Pfannschmidt, T., Obokata, J. and Oelmüller, R. (2002) Polyribosome loading of spinach mRNAs for photosystem I subunits is controlled by photosynthetic electron transport. Plant J. 32, 631-639.
51. Strand, A., Asam, T., Alonso, J., Ecker, J.R. and Chory, J. (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature, 421, 79-83.
52. Sullivan, J.A. and Gray, J.C. (1999) Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in the roots of the pea lip 1 mutant. Plant Cell, 11, 901-910.
53. Sullivan, J.A. and Gray, J.C. (2002) Multiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. Plant J. 32, 763-774.
54. Susek, R.E., Ausubel, F.M. and Chory, J. (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell, 74, 787-799.
55. Tang, L., Bhat, S. and Petracek, M.E. (2003) Light control of nuclear gene mRNA abundance and translation in tobacco. Plant Physiol. 133, 1979-1990.
56. Thangavelu, M., Belostotsky, D., Bevan, M.W., Flavell, R.B., Rogers, H.J. and Lonsdale, D.M. (1993) Partial characterization of the Nicotiana tabacum actin gene family: evidence for pollen-specific expression of one of the gene family members. Mol. Gen. Genet. 240, 290-295.
57. Vinti, G., Hills, A., Campbell, S., Bowyer, J.R., Mochizuki, N., Chory, J. and López-Juez, E. (2000) Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signalling. Plant J. 24, 883-894.
58. Vorst, O., van Dam, F., Weisbeek, P. and Smeekens, S. (1993a) Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-transcriptional processes. Plant J. 3, 793-803.
59. Vorst, O., Kock, P., Lever, A., Weterings, B., Weisbeek, P. and Smeekens, S. (1993b) The promoter of the Arabidopsis thaliana plastocyanin gene contains a far upstream enhancer-like element involved in chloroplast-dependent expression. Plant J. 4, 933-945.