Abstract
Nuclear-encoded genes for proteins of the photosynthetic maschinery represent a particular subset of genes. Their expression is cooperatively stimulated by discrete factors including the developmental stage of plastids and light. We have analyzed in transgenic tobacco the plastid- and light-dependent expression of a series of 5′ promoter deletions of various nuclear genes from spinach, of fusions of defined promoter segments with the 90-bp 35S RNA CaMV minimal promoter, as well as with mutations in sequences with homologies to characterizedcis-elements, to address the question of whether the plastid signal and light operate via the same or differentcis-acting elements. In none of the 160 different transgenic lines (representing 32 promoter constructs from seven genes) analyzed, could significant differences be identified in the responses to the two regulatory pathways. The data are compatible with the idea that both signals control the expression of nuclear genes for plastid proteins via the samecis-acting elements.
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References
Adamska I, Kloppstech K, Ohad I (1992) UV light stress induces the synthesis of the early light-inducible protein and prevents its degradation. J Biol Chem 34:24732–24737
Apel K (1981) The protochlorophyllide of barley (Hordeum vulgare L.): phytochrome induced decrease of mRNA coding for NADPH-protochlorophyllide-oxidoreductase. Eur J Biochem 120:89–93
Apel K, Santel HJ, Redlinger T, Falk H (1980) The protochlorophyllide holochrome of barley (Hordeum vulgare L.): isolation and characterization of NADPH-protochlorophyllide oxidoreductase. Eur J Biochem 111:251–258
Barnes SA, Quaggio RB, Chua N-H (1995)1 Phytochrome signal-transduction: characterization of pathways and isolation of mutants. Philos Trans R Soc Lond B Biol Sci 350:67–74
Barnes SA, Nishizawa NK, Quaggio RB, Whitelam GC, Chua N-H (1996) Far-red light blocks greening ofArabidopsis seedlings via a phytochrome A-mediated change in plastid development. Plant Cell 8:601–615
Bartley GE, Scolnik PA (1993) cDNA cloning, expression during development, and genome mapping ofPSY2, a second tomato gene encoding phytoene synthase. J Biol Chem 268:25718–25721
Bolle C, Sopory S, Lübberstedt T, Klösgen RB, Herrmann RG, Oelmüller R (1994) The role of plastids in the expression of nuclear genes for thylakoid proteins studied with chimericβ-glucuronidase gene fusions. Plant Physiol 105:1355–1364
Bolle C, Herrmann RG, Oelmüller R (1995) Regulatory elements involved in the expression of nuclear genes for plastid proteins. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol. 3. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 703–706
Bolle C, Herrmann RG, Oelmüller R (1996a) Intron sequences are involved in the plastid- and light-dependent expression of the spinachPsaD gene. Plant J, in press
Bolle C, Kusnetsov VV, Herrmann RG, Oelmüller R (1996b) The spinachAtpC andAtpD genes contain elements for light-regulated, plastid-dependent and organ-specific expression in the vicinity of the transcription start sites. Plant J 9:21–30
Bowler C, Chua N-H (1994) Emerging themes of plant signal transduction. Plant Cell 6:1529–1541
Bowler C, Neuhaus G, Yamagata H, Chua N-H (1994a) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77:73–81
Bowler C, Yamagata H, Neuhaus G, Chua N-H (1994b) Phytochrome signal transduction pathways are regulated by reciprocal control mechanisms. Genes Dev 8:2188–2202
Bovy A, Van den Berg C, De Vrieze G, Thompson WF, Weisbeek P, Smeekens S (1995) Light-regulated expression of theArabidopsis thaliana ferredoxin gene requires sequences upstream and downstream of the transcription initiation site. Plant Mol Biol 27:27–39
Bradford MJ (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Dickey LF, Gallo-Meagher M, Thompson WF (1992) Light regulatory sequences are located within the 5′ portion of theFed-1 message sequence. EMBO J 11:2311–2317
Dickey LF, Nguyen T-T, Allen, GC, Thompson WF (1994) Light modulation of ferredoxin mRNA abundance requires an open reading frame. Plant Cell 6:1171–1176
Flieger K, Tyagi A, Sopory S, Cseplö A, Herrmann RG, Oelmüller R (1993) A 42 bp promoter fragment of the gene for subunit III of photosystem I (psaF) is crucial for its activity. Plant J 1:9–17
Flieger K, Wicke A, Herrmann RG, Oelmüller R (1994) Promoter and leader sequences of the spinachPsaD andPsaF 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
Forreiter C, Cleve B van, Schmidt A, Apel K (1990) Evidence for a general light-dependent negative control of NADPH-protochlorophyllide oxidoreductase in angiosperms. Planta 183:126–132
Gilmartin PM, Memelink J, Hiratsuka K, Kay SA, Chua N-H (1992) Characterization of a gene encoding a DNA binding protein with specificity for a light-responsive element. Plant Cell 4:839–849
Giuliano G, Bartley GE, Scolnik PA (1993) Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5:379–387
Green PJ, Yong M-H, Cuozzo M, Kano-Murakami Y, Silverstein P, Chua N-H (1988) Binding site requirements for pea nuclear protein factor GT-1 correlate with sequences required for the light-dependent transcriptional activation of therbcS-3A gene. EMBO J 7:4035–4044
Griffiths WT (1975) Characterization of the terminal stage of chlorophyll(ide) synthesis in etioplast membrane preparations. Biochem J 152:623–635
Griffiths WT (1978) Reconstitution of chlorophyll formation by isolated etioplast membranes. Biochem J 174:681–692
Harrak H, Lagrange T, Bisanz-Seyer C, Lerbs-Mache S, Mache R (1995) The expression of nuclear genes encoding plastid ribosomal proteins precedes the expression of chloroplast genes during early phases of chloroplast development. Plant Physiol 108:685–692
Helliwell CA, Gray JC (1996) Light-regulated expression of the pea plastocyanin gene is mediated by elements within the transcribed region of the gene and requires the intact 5′untranslated leader sequence. Plant J. (submitted)
Herrmann RG, Westhoff P, Link G (1992) Biogenesis of plastids in higher plants. In: Herrmann RG (ed) Plant gene research, vol. 6, cell organelles. Springer, Heidelberg, Berlin, New York, pp 275–349
Hoekema A, Horsch PR, Kaoykaas JJ, Schilperoot RA (1983) A binary plant vector strategy based on separation ofvir- and T-region of theAgrobacterium tumefaciens Ti-plasmid. Nature 303:179–180
Horsch R, Fry F, Hofmann N, Eichholtz D, Rogers S, Fraley R (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231
Hübel A, Lee JH, Wu C, Schöffl F (1995)Arabidopsis heat shock factor is constitutively active inDrosophila and human cells. Mol Gen Genet 248:136–141
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions:β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Kendrick RE, Kronenberg GHM (1994) Photomorphogenesis in plants. Kluwer Academic Press, Dordrecht
Lebedev N, Cleve B van, Armstrong G, Apel K (1995) Chlorophyll synthesis in a deetiolated (det340) mutant ofArabidopsis without NADPH-protochlorophyllide (PChide) oxidoreductase (POR) A and photoactive PChide-F655. Plant Cell 7:2081–2090
Lefkowitz RJ (1993) G protein-coupled receptor kinases. Cell 74:409–412
Lübberstedt Th, Oelmüller R, Wanner G, Herrmann RG (1994) Interactingcis elements in the plastocyanin promoter from spinach ensure regulated high-level expression. Mol Gen Genet 242:602–613
Ma H (1994) GTP-binding proteins in plants: new members of an old family. Plant Mol Biol 26:1611–1636
Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochim Sci 20:506–510
Mikaelian I, Sergeant A (1992) A general and fast method to generate multiple site directed mutations. Nucleic Acids Res 20:376
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Neer EJ (1995) Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80:249–257
Neuhaus G, Bowler C, Kern R, Chua N-H (1993) Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell 73:937–952
Oelmüller R (1989) Photooxidative destruction of chloroplasts and its effect on nuclear gene expression and extraplastidic enzyme levels. Photochem Photobiol 49:229–239
Oelmüller R, Bolle C, Tyagi AK, Niekrawietz N, Breit S, Herrmann RG (1993) Characterization of the promoter from the single-copy gene ferredoxin-NADP+-oxidoreductase from spinach. Mol Gen Genet 237:261–272
Oelmüller R, Levitan I, Bergfeld R, Rajasekhar VK, Mohr H (1986) Expression of nuclear genes as affected by treatments acting on plastids. Planta 168:482–492
Pwee K-H, Gray JC (1993) The pea plastocyanin promoter directs cell-specific but not full light-regulated expression in transgenic tobacco plants. Plant J 3:437–449
Reinbothe S, Reinbothe C, Holtorf H, Apel K (1995) Two NADPH: protochlorophyllide oxidoreductases in barley: evidence for the selective disappearance of PORA during the light-induced greening of etiolated seedlings. Plant Cell 7:1933–1940
Runge S, Sperling U, Frick G, Apel K, Armstrong GA (1996) Distinct roles for light-dependent NADPH: protochlorophyllide oxidoreductases (POR) A and B during greening in higher plants. Plant J 9:513–523
Schindler U, Cashmore AR (1990) Photoregulated gene expression may involve ubiquitous DNA binding proteins. EMBO J 9:3415–3427
Shacklock RS, Read ND, Trewavas AJ (1992) Cytosolic free calcium mediates red light-induced photomorphogenesis. Nature 358:753–755
Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants ofArabidopsis uncouple nuclearCAB andRBCS gene expression from chloroplast development. Cell 74:787–799
Taylor WC (1989) Regulatory interaction between nuclear and plastid chromosomes. Annu Rev Plant Physiol Plant Mol Biol 40:211–233
Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46:445–474
Thompson WF, White MJ (1991) Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42:423–466
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Kusnetsov, V., Bolle, C., Lübberstedt, T. et al. Evidence that the plastid signal and light operate via the samecis-acting elements in the promoters of nuclear genes for plastid proteins. Molec. Gen. Genet. 252, 631–639 (1996). https://doi.org/10.1007/BF02173968
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DOI: https://doi.org/10.1007/BF02173968