Abstract
We have isolated a low temperature-induced maize gene, mlip15, via cross hydridization using ricelip19. The longest cDNA isolated comprised 1179 bp and coded for a 135 amino acid bZIP (basic region/leucine zipper) protein. The gene showed 61.4% and 68.9% identity with the rice gene at the DNA and amino acid sequence levels, respectively, and is distinct from other maize genes that code for bZIP proteins. The level of mlip15 transcript was positively regulated by low temperature in the same way as thelip19 transcript. The levels of the transcript were also strongly increased by salt stress and exogenous abscisic acid, and slightly increased by anaerobiosis, but were not affected by heat shock and drought. The mLIP15 protein and truncated derivatives, produced in rabbit reticulocyte lysates or in anEscherichia coli expression system, were able to bind to a fragment of the wheat histone H3 gene promoter. This binding was diminished by addition of a molar excess of the hexamer sequence 5′-ACGTCA-3′ found in the promoter and of the G-box-like sequence, but not by the addition of the ocs sequence or a mutated hexamer sequence. The factor bound to a promoter region of the maizeAdhl gene, expression of which is also induced by low temperature. These results lead to the conclusion that mlip15 is a strong candidate for a low temperature-induced transcription factor in maize.
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References
Abler ML, Scandalios JG (1993) Isolation and characterization of a genomic sequence encoding the maizeCat3 catalase gene. Plant Mol Biol 22: 1031–1038
Agre P, Johnson PF, McKnight SL (1989) Cognate DNA binding specificity retained after leucine zipper exchange between GCN4 and C/EBP. Science 246: 922–926
Aguan K, Sugawara K, Suzuki N, Kusano T (1991) Isolation of genes for low-temperature-induced proteins in rice by a simple subtractive method. Plant Cell Physiol 32: 1285–1289
Aguan K, Sugawara K, Suzuki N, Kusano T (1993) Low-temperature-dependent expression of a rice gene encoding a protein with a leucine-zipper motif. Mol Gen Genet 240: 1–8
Andrews N, Kotkow K, Ney P, Erdjument-Bromage H, Tempst P, Orkin S (1993) Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Proc Natl Acad Sci USA 90: 11488–11492
Armstrong GA, Weisshaar B, Hahlbrock K (1992) Homodimeric and heterodimeric leucine zipper proteins and nuclear factors from parsley recognize diverse promoter elements with ACGT cores. Plant Cell 4: 525–537
Baker S, Wilhelm K, Thomashow M (1994) The 5′-region ofArabidopsis thaliana cor15a hascis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24: 701–713
Bouchez D, Tokuhisa JG, Llewellyn DJ, Dennis ES, Ellis JG (1989) The ocs-element is a component of the promoters of several T-DNA and plant viral genes. EMBO J 8: 4197–4204
Chodosh LA (1987) Mobility shift DNA-binding assay using gel electrophoresis. In Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York, unit 12.2.1 (Supplement B)
Christie J, Hahn M, Walbot V (1991) Low-temperature accumulation of alcohol dehydrogenase-1 mRNA and protein activity in maize and rice seedlings. Plant Physiol 95: 699–706
Christie J Alfenito M Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings Planta 194: 541–549
Dennis E, Sachs M, Gerlach W, Finnegan E, Peacock W (1985) Molecular analysis of the alcohol dehydrogenase 2 (Adh2) gene of maize. Nucleic Acids Res 13: 727–743
Foley R, Grossman C, Ellis J, Llewellyn D, Dennis E, Peacock W, Singh K (1993) Isolation of a maize bZIP protein subfamily: candidates for the ocs-element transcription factor. Plant J 3: 669–679
Foster R, Izawa T, Chua N-H (1994) Plant bZIP proteins gather at ACGT elements. FASEB J 8: 192–200
Ganal M, Hemleben V (1986) Comparison of the ribosomal RNA genes in four closely related Cucurbitaceae. Plant Syst Evol 154: 63–77
Gilmour S, Thomashow M (1991) Cold acclimation and cold-regulated gene expression in ABA mutants ofArabidopsis thaliana. Plant Mol Biol 17: 1233–1240
Gilmour S, Artus N, Thomashow M (1992) cDNA sequence analysis and expression of two cold-regulated genes ofArabidopsis thaliana. Plant Mol Biol 18: 13–21
Guiltinan M, Marcotte W, Quatrano R (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 267–271
Guo W, Ward R, Thomashow M (1992) Characterization of a cold-regulated wheat gene related toArabidopsis cor47 Plant Physiol 100: 915–922
Guy C (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41: 187–223
Hai T, Curran T (1991) Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci USA 88: 3720–3724
Houde M, Danyluk J, Lalibertie J-F, Rassart E, Dhindsa RS, Sarhan F (1992) Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99: 1381–1387
Hurst H (1994) Transcription factors. 1. bZIP proteins. Protein Profiles 1: 123–168
Izawa T, Foster R, Chua N-H (1993) Plant bZIP protein DNA binding specificity. J Mol Biol 230: 1131–1144
Katagiri F, Lam E, Chua N-H (1989) Two tobacco DNA-binding proteins with homology to the nuclear factor CREB. Nature 340: 727–730
Kazuoka T, Oeda K (1994) Purification and characterization of COR85-oligomeric complex from cold-acclimated spinach. Plant Cell Physiol 35: 601–611
Kouzarides T, Ziff E (1988) The role of the leucine zipper in the fos-jun interaction. Nature 336: L646–651
Kouzarides T, Ziff E (1989) Leucine zippers offos, jun and GCN4 dictate dimerization specificity and thereby control DNA binding. Nature 340: 568–571
Kurkela S, Franck M (1990) Cloning and characterisation of a cold- and ABA-inducibleArabidopsis gene. Plant Mol Biol 15: 137–144
Kusano T, Sugawara K (1993) Specific binding of theThiobacillus ferrooxidans RbcR protein to the intergenic sequence of therbc operon andrbcR gene. J Bacteriol 175: 1019–1025
Landschulz WH, Johnson PF, McKnight SL (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240: 1759–1763
Lång V, Heino P, Palva E (1989) Low temperature acclimation and treatment with exogenous abscisic acid induce common polypeptides inArabidopsis thaliana (L.) Heynh. Theor Appl Genet 77: 729–734
Lin C, Thomashow M (1992) A cold-regulatedArabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Biophys Res Commun 183: 1103–1108
Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227: 1435–1441
Lohmer S, Maddaloni M, Motto M, Di Fonzo N, Hartings H, Salamini F, Thompson RD (1991) The maize regulatory locusOpaque-2 encodes a DNA-binding protein which activates the transcription of theb-32 gene. EMBO J 10: 617–624
Menkens AE, Cashmore AR (1994) Isolation and characterization of a fourthArabidopsis thaliana G-box-binding factor, which has similarities to Fos oncoprotein. Proc Natl Acad Sci USA 91: 2522–2526
Mikami K, Sakamoto A, Iwabuchi M (1994) The HBP-1 family of wheat basic/leucine zipper proteins interacts with overlappingcis-acting hexamer motifs of plant histone genes. J Biol Chem 269: 9974–9985
Nagy F, Kay SA, Chua N-H (1988) Analysis of gene expression in transgenic plants. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Kluwer Academic Publishers, Dordrecht, 84, pp 1–29
Nakayama T, Sakamoto A, Yang P, Minami M, Fujimoto Y, Ito T, Iwabuchi M (1992) Highly conserved hexamer, octamer and nonamer motifs are positive cis-regulatory elements of the wheat histone H3 gene. FEBS Lett 300: 167–170
Nordin K, Heino P, Palva ET (1991) Separate signal pathways regulate the expression of a low-temperature-induced gene inArabidopsis thaliana (L.) Heynh. Plant Mol Biol 16: 1061–1071
Oeda K, Salinas J, Chua N (1991) A tobacco bZip transcription activator (TAF-1) binds to a G-box-like motif conserved in plant genes. EMBO J 10: 1793–1802
Orr W, White T, Robert L, Singh J (1992) Complementary DNA sequence of a low temperature-inducedBrassica napus gene with homology to theArabidopsis thaliana kinl gene. Plant Physiol 98: 1532–1534
Pater de S, Katagiri F, Kijne J, Chua NH (1994) bZIP proteins bind to a palindromic sequence without an ACGT core located in a seed-specific element of the pea lectin promoter. Plant J 6: 133–140
Pathak D, Sigler PB (1992) Updating structure-function relationships in the bZIP family of transcription factors. Curr Opinion Struct Biol 2: 116–123
Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell, 6: 65–74
Pysh L, Aukerman M, Schmidt R (1993) OHP1: a maize basic domain/leucine zipper protein that interacts with Opaque2. Plant Cell 5: 227–236
Saiki RK, Gelfand DH, Stoffe S, Sharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467
Sano H, Youssefian S (1991) A novelras-relatedrgp1 gene encoding a GTP-binding protein has reduced expression in 5-azacytidine-induced dwarf rice. Mol Gen Genet 228: 227–232
Schindler U, Menkens A, Beckman H, Ecker J, Cashmore A (1992a) Heterodimerization between light-regulated and ubiquitously expressedArabidopsis GBF bZIP protein. EMBO J 11: 1261–1273
Schindler U, Terzaghi W, Beckmann H, Kadesch T, Cashmore A, (1992b) DNA binding site preferences and transcriptional activation properties of theArabidopsis transcription factor GBF1. EMBO J 11: 3415–3427
Schmidt R, Burr F, Aukerman M, Burr B (1990) Maize regulatory gene opaque-2 encodes a protein with a “leucine-zipper” motif that binds to zein DNA. Proc Natl Acad Sci USA 87: 46–50
Sellers JW, Struhl K (1989) Changing Fos oncoprotein to a Jun-independent DNA-binding protein with GCN4 dimerization specificity by swapping “leucine zippers” Nature 341: 74–76
Singh K, Dennis E, Ellis J, Llewellyn D, Tokuhisa J, Wahleithner J, Peacock W (1990) OCSBF-1, a maize ocs enhancer binding factor: isolation and expression during development. Plant Cell 2: 891–903
Tabata T, Fukasawa M, Iwabuchi M (1984) Nucleotide sequence and genomic organization of a wheat histone H3 gene. Mol Gen Genet 196: 397–400
Tabata T, Takase H, Takayama S, Mikami K, Nakatsuka A, Kawata T, Nakayama T, Iwabuchi M (1989) A protein that binds to a cis-acting element of wheat histone genes has a leucine zipper motif. Science 245: 965–967
Tabata T, Nakayama T, Mikami K, Iwabuchi M (1991) HBP-1a and HBP-1b: leucine zipper-type transcription factors of wheat. EMBO J 10: 1459–1467
Tabor S (1990) Expression using the T7 RNA polymerase/promoter system. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York, unit 16.2.1 (Supplement II)
Tabor S, Richardson CC (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82: 1074–1078
Thomashow M (1990) Molecular genetics of cold acclimation in higher plants. Adv Genet 28: 99–131
Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsismyb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5: 1529–1539
Weising K, Kahl G (1991) Towards an understanding of plant gene regulation: the action of nuclear factors. Z Naturforsch 46C: 1–11
Weisshaar B, Armstrong G, Block A, da Costa e Silva O, Hahlbrock K (1991) Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance in light responsiveness. EMBO J 10: 1777–1786
Wilhelm KS, Thomashow MF (1993)Arabidopsis thaliana cor15b, an apparent homolog ofcor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol Biol 23: 1073–1077
Williams ME, Foster R, Chua NH (1992) Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell 4: 485–496
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novelcis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251–264
Yunes JA, Cord Neto G, da Silva MJ, Leite A, Ottoboni LMM, Arruda P (1994) The transcriptional activator Opaque 2 recognizes two different target sequences in the 22-kD-like α-prolamin genes. Plant Cell 6: 237–249
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Kusano, T., Berberich, T., Harada, M. et al. A maize DNA-binding factor with a bZIP motif is induced by low temperature. Molec. Gen. Genet. 248, 507–517 (1995). https://doi.org/10.1007/BF02423445
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DOI: https://doi.org/10.1007/BF02423445