Summary
The expression of the phosphoenolpyruvate carboxylase (PEPC) gene involved in C4 photosynthesis is regulated in a highly organized manner. Nuclear factors interacting with DNA fragments from the 5′ flanking region (from positions −1012 to +88 relative to the transcription start site) of the maize gene were identified by gel shift assays. Among the three kinds of such nuclear proteins (MNF1, MNF2a and MNF2b) found in the extract from maize leaves, MNF2a and MNF2b, which were distinguishable by their chromatographic behavior, interacted with the same motif of the repeated sequence (RS2) in the region from −432 to −201. MNF1 interacted with the region from −905 to −818 in which two copies of another kind of repeated sequence (RS1) reside. All of these nuclear factors were found only in the extracts from green and etiolated leaves but not in those from stems and roots. The relative content of MNFl and MNF2b was almost equal in green and etiolated leaves, while that of MNF2a was significantly higher in etiolated leaves than green leaves. It is suggested that expression of the PEPC gene is controlled by the combined effects of these nuclear factors.
Similar content being viewed by others
References
Allen RD, Bernier F, Lessard PA, Beachy RN (1989) Nuclear factors interact with a soybean β-conglycinin enhancer. Plant Cell 1:623–631
Arcangioli B, Lescure B (1985) Identification of proteins involved in the regulation of yeast Iso-l-cytochrome C expression by oxygen. EMBO J
Baeuerle PA, Baltimore D (1988) Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-κB transcription factor. Cell 53:211–217
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Broglie R, Coruzzi G, Keith B, Chua N-H (1984) Molecular biology of C4photosynthesis in Zea mays: differential localization of proteins and mRNAs in the two leaf cell types. Plant Mol Biol 3:431–444
Datta N, Cashmore AR (1989) Binding of a pea nuclear protein to promoters of certain photoregulated genes is modulated by phosphorylation. Plant Cell 1:1069–1077
Edwards G, Walker DA (1983) C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis. Blackwell Scientific Publications, Oxford, London, pp 275–367
Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85:7089–7093
Green PJ, Kay SA, Chua N-H (1987) Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A. EMBO J 6:2543–2549
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 light-dependent transcriptional activation of the rbcS-3A gene. EMBO J 7:4035–4044
Hague DR, Sims TL (1980) Evidence for light-stimulated synthesis of phosphoenolpyruvate carboxylase in leaves of maize. Plant Physiol 66: 505–509
Harada H, Fujita T, Miyamoto M, Kimura Y, Maruyama M, Furia A, Miyata T, Taniguchi T (1989) Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell 58:729–739
Harpster MH, Taylor WC (1986) Maize phosphoenolpyruvate carboxylase: Cloning and characterization of mRNA encoding isozymic forms. J Biol Chem 261:6132–6136
Hatch MD (1978) Regulation of enzymes in C4 photosynthesis. Curr Top Cell Regul 14:1–27
Hudspeth R, Grula JW (1989) Structure and expression of the maize gene encoding the phosphoenolpyruvate carboxylase isozyme involved in C4 photosynthesis. Plant Mol Biol 12:579–589
Hudspeth R, Glackin CA, Bonner J, Grula JW (1986) Genomic and cDNA clones for maize phosphoenolpyruvate carboxylase and pyruvate, orthophosphate dikinase: Expression of different gene-family members in leaves and roots. Proc Natl Acad Sci USA 83:2884–2888
Iguchi-Ariga SMM, Schaffner W (1989) CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes Dev 3:612–619
Izui K, Ishijima S, Yamaguchi Y, Katagiri F, Murata T, Shigesada K, Sugiyama T, Katsuki H (1986) Cloning and sequence analysis of cDNA encoding active phosphoenolpyruvate carboxylase of the C4-pathway from maize. Nucleic Acids Res 14:1615–1628
Kanai R, Edwards GE (1973) Separation of mesophyll protoplasts and bundle sheath cells from maize leaves for photosynthetic studies. Plant Physiol 51:1133–1137
Katagiri F, Lam E, Chua N-H (1989) Two tobacco DNA-binding proteins with homology to the nuclear factor CREB. Nature 340:727–730
Kawamura T, Shigesada K, Yanagisawa S, Izui K (1990) Phosphoenolpyruvate carboxylase prevalent in maize roots: Isolation of a cDNA clone and its use for analyses of the gene and gene expression. J Biochem 107:165–168
Lam E, Chua N-H (1989) ASF-2: A factor that binds to cauliflower mosaic virus 35 S promoter and a conserved GATA motif in Cab promoters. Plant Cell 1:1147–1156
Lam E, Benfey PN, Gilmartin PM, Fang R-X, Chua N-H (1989) Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci USA 86:7890–7894
Maier U-G, Brown JWS, Toloczyki C, Feix G (1987) Binding of a nuclear factor to a consensus sequence in the 5′ flanking region of zein genes from maize. EMBO J 6:17–22
Maier U-G, Brown JWS, Schmitz LM, Schwall M, Dietrich G, Feix G (1988) Mapping of tissue-dependent and independent protein binding sites to the 5′ upstream region of a zein gene. Mol Gen Genet 212:241–245
Maier U-G, Grasser KD, Michael MH, Feix G (1990) Multiple protein bind to the P2 promoter region of the zein gene pMS1 of maize. Mol Gen Genet 221:164–170
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Matsuoka M, Minami E (1989) Complete structure of the gene for phosphoenolpyruvate carboxylase from maize. Eur J Biochem 181:593–598
Mikami K, Tabata T, Kawata T, Nakayama T, Iwabuchi M (1987) Nuclear protein(s) binding to the conserved DNA hexameric sequence postulated to regulate transcription of wheat histone genes. FEBS Lett 223:273–278
Mikami K, Sakamoto A, Tabata T, Iwabuchi M (1989) Wheat nuclear protein HBP-1 binds to the hexameric sequence in the promoter of various plant genes. Nucleic Acids Res 17:9707–9717
Mitchell PJ, Tjian R (1989) Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245:371–378
Montminy MR, Bilezikjian LM (1987) Binding of a nuclear protein to the cyclic-AMP response element of the somatostrain gene. Nature 328:175–178
Nelson T, Harpster MH, Mayfield SP, Taylor WC (1984) Lightregulated gene expression during maize leaf development. J Cell Biol 98:558–564
Ngernprasirtsiri J, Chollet R, Kobayashi H, Sugiyama T, Akazawa T (1989) DNA methylation and differential expression of C4 photosynthesis genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 264:8241–8248
Perrot-Rechenmann C, Vidal J, Brulfert J, Burlet A, Gadal P (1982) A comparative immunocytochemical localization study of phosphoenolpyruvate carboxylase in leaves of higher plants. Planta 155:24–30
Prat S, Willmitzer L, Sanchez-Serrano JJ (1989) Nuclear proteins binding to a cauliflower mosaic virus 35 S truncated promoter. Mol Gen Genet 217:209–214
Sheen J-Y, Bogorad L (1987) Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 262:11726–11730
Shore D, Stillman D, Brand AH, Nasmyth KA (1987) Identification of silencer binding proteins from yeast: possible roles in SIR control and DNA replication. EMBO J 6:461–467
Sims TL, Hague DR (1981) Light-stimulated increase of translatable mRNA for phosphoenolpyruvate carboxylase in leaves of maize. J Biol Chem 256:8252–8255
Staiger D, Kaulen H, Schell J (1989) A CACGTG motif of the Antirrhinum majus chalcone synthase promoter is recognized by an evolutionarily conserved nuclear protein. Proc Natl Acad Sci USA 86:6930–6934
Ting IP, Osmond CB (1973) Multiple forms of plant phosphoenolpyruvate carboxylase associated with different metabolic pathways. Plant Physiol 51:448–453
Uedan K, Sugiyama T (1976) Purification and characterization of phosphoenolpyruvate carboxylase from maize leaves. Plant Physiol 57:906–910
Watson JC, Thompson WF (1986) Purification and restriction endonuclease analysis of plant nuclear DNA. Methods Enzymol 118:57–75
Werr W, Springer B, Schurmann J, Bellmann R (1988) Multiple interactions between nuclear proteins of Zea mays and the promoter of the Shrunken gene. Mol Gen Genet 212:342–350
Yanagisawa S, Izui K (1989) Maize phosphoenolpyruvate carboxylase involved in C4 photosynthesis: Nucleotide sequence analysis of the 5′ flanking region of the gene. J Biochem 106:982–987
Yanagisawa S, Izui K, Yamaguchi Y, Shigesada K, Katsuki H (1988) Further analysis of cDNA clones for maize phosphoenolpyruvate carboxylase involved in C4 photosynthesis. FEBS Lett 229:107–110
Author information
Authors and Affiliations
Additional information
Communicated by M. Sekiguchi
Rights and permissions
About this article
Cite this article
Yanagisawa, S., Izui, K. Multiple interactions between tissue-specific nuclear proteins and the promoter of the phosphoenolpyruvate carboxylase gene for C4 photosynthesis in Zea mays . Molec. Gen. Genet. 224, 325–332 (1990). https://doi.org/10.1007/BF00262425
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00262425