Abstract
Wheat basic/leucine zipper protein HBP-1a(17) binds in vitro specifically to ACGT motif-containing cis-acting elements, such as the type I element of plant histone promoters and the G-box of hormone- and light-inducible promoters. To address the in vivo function of HBP-1a(17), we isolated and structurally analyzed theHBP-1a(17) gene and examined its expression in transgenicArabidopsis plants. TheHBP-1a(17) gene is composed of 14 exons; the basic region and leucine zipper are encoded by separate small exons, as is the case for other bZIP protein genes. The G-box of theHBP-1a(17) promoter bound specifically to HBP-1a(17) and its related HBP-1a isoforms, suggesting that theHBP-1a(17) gene may be autoregulated, although the binding affinity of these proteins in vitro is very low. InArabidopsis plants, activation of theHBP-1a(17) promoter was highly restricted to photosynthetically active mesophyll, and guard cells and vascular bundles of vegetative leaves. Etiolation of transgenic plants resulted in inhibition of expression of theHBP-1a(17) promoter. Indeed, theHBP-1a(17) promoter contains several sequence elements homologous to cis-acting elements conserved in light-inducible promoters. It is, therefore, assumed that theHBP-1a(17) gene is light regulated and that HBP-1a(17) is involved in light-responsive gene transcription via the G-box.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
Akama K, Shiraishi H, Ohta S, Nakamura K, Okada K, Shimura Y (1992) Efficient transformation ofArabidopsis thaliana: comparison of the efficiencies with various organs, plant ecotypes andAgrobacterium strains. Plant Cell Reports 12:7–11
Angel P, Hattri K, Smeal T, Karin M (1988) TheJun proto-oncogene is positively autoregulated by its product, Jun/Ap-1. Cell 55:875–885
Berger I, Shaul Y (1994) The humanjunD gene is positively and selectively autoregulated. DNA Cell Biol 13:249–255
Bowler C, Neuhaus G, Yamagata H, Chua N-H (1994) Cyclic GMP and calcium mediate photochrome phototransduction. Cell 77:73–81
Chory J (1993) Out of darkness: mutants reveal pathways controlling light-regulated development in plants. Trends Genet 9:167–172
Damiani RD, Wessler SR (1993) An upstream open reading frame represses expression of Lc, a member of the R/B family of maize transcriptional activators. Proc Natl Acad Sci USA 90: 8244–8248
Deng X-W (1994) Fresh view on light signal transduction in plants. Cell 76:423–426
Ferl RJ, Nick HS (1987) In vivo detection of regulatory factor binding sites in the 5′ flanking region of maizeAdh1. J Biol Chem 262:7947–7950
Foley RC, Grossman C, Ellis JG, Llewellyn DJ, Dennis ES, Peacock WJ, Singh KB (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
Fromm H, Katagiri F, Chua N-H (1991) The tobacco transcription activator TGA1a binds to a sequence in the 5′ upstream region of a gene encoding a TGA1a-related protein. Mol Gen Genet 229:181–188
Furuya M (1993) Phytochromes: their molecular species, gene families, and functions. Annu Rev Plant Physiol Plant Mol Biol 44:617–645
Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionary conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85:7089–7093
Guiltinan MJ, Marcotte WR, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267–271
Ha S-B, An G (1988) Identification of upstream regulatory elements involved in the developmental expression of theArabidopsis thaliana cab1 gene. Proc Natl Acad Sci USA 85:8017–8021
Harter K, Kircher S, Frohnmeyer H, Krentz M, Nagy F, Schäfer E (1994) Light-regulated modification and nuclear translocation of cytosolic G-box binding factors in parsley. Plant Cell 6:545–559
Hartings H, Maddaloni M, Lazzaroni N, Di Fonzo N, Motto M, Salamini F, Thompson R (1989) TheO2 gene which regulates zein deposition in maize endosperm encodes a protein with structural homologies to transcriptional activators. EMBO J 8:2795–2801
Katagiri F, Lam E, Chua N-H (1989) Two tobacco DNA-binding proteins with homology to the nuclear factor CREB. Nature 340:727–730
Kosugi S, Ohashi Y, Nakajima K, Arai Y (1990) An improved assay for β-gluculonidase in transformed cells: methanol almost completely suppresses a putative endogenous β-glucuronidase activity. Plant Science 70:33–140
Legraverend C, Antonson P, Flodby P, Xanthopoulos KG (1993) High level activity of the mouse CCAAT/enhancer binding protein (C/EBPα) gene promoter involves autoregulation and several ubiquitous transcription factors. Nucl Acids Res 21:1735–1742
Liu X, Lam E (1994) Two binding sites for the plant transcription factor ASF-1 can respond to auxin treatments in transgenic tobacco. J Biol Chem 269:668–675
Lohmer S, Maddaloni M, Motto M, Salamini F, Thompson RD (1993) Translation of the mRNA of the maize transcriptional activator Opaque-2 is inhibited by upstream open reading frames present in the leader sequence. Plant Cell 5:65–73
Mikami K, Iwabuchi M (1993) Regulation of cell cycle-dependent gene expression. In: Verma DPS (ed) Control of plant gene expression. CRC Press, Boca Raton, pp 51–68
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, Takase H, Tabata T, Iwabuchi M (1989) Multiplicity of the DNA-binding protein HBP-1 specific to the conserved hexameric sequence ACGTCA in various plant gene promoters. FEBS Lett 256:67–70
Mikami K, Sakamoto A, Iwabuchi M (1994) The HBP-1 family of wheat basic/leucine zipper proteins interacts with overlapping cis-acting hexamer motifs of plant histone genes. J Biol Chem 269:9974–9985
Minami M, Huh GH, Yang P, Iwabuchi M (1993) Coordinate gene expression of five subclass histones and the putative transcription factors, HBP-1a and HBP-1b, of histone genes in wheat. Plant Mol Biol 23:429–434
Nasuda S, Liu Y-G, Sakamoto A, Nakayama T, Iwabuchi M, Tsunewaki K (1993) Chromosomal locations of the genes for histone and a histone gene-binding protein family HBP-1 in common wheat. Plant Mol Biol 22:603–614
Neuhaus G, Bowler C, Kern R, Chua N-H (1993) Calcium/calmodulin-dependent and-independent photochrome signal transduction pathways. Cell 73:937–952
Oeda K, Salinas J, Chua N-H (1991) A tobacco bZip transcription activator (TAF-1) binds to a G-box-like motif conserved in plant genes. EMBO J 10:1793–1802
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd edn.) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Schindler U, Menkens AE, Beckmann H, Ecker JR, Cashmore AR (1992a) Heterodimerization between light-regulated and ubiquitously expressedArbidopsis GBF bZIP proteins. EMBO J 11:1261–1273
Schindler U, Beckmann H, Cashmore AR (1992b) TGA1 and G-box binding factors: two distinct classes ofArabidopsis leucine zipper proteins complete for the G-box-like element TGACGTGG. Plant Cell 4:1309–1319
Schmidt RJ, Burr FA, Aukerman MJ, Burr B (1990) Maize regulatory geneopaque-2 encodes a protein with a “leucine zipper” motif that binds to zein DNA. Proc Natl Acad Sci USA 87:46–50
Schulze-Lefert P, Dangl J, Becker-Andre M, Hahlbrock K, Schulz W (1989) Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J 8:651–656
Singh K, Dennis ES, Fllis JG, Llewellyn DJ, Tokuhisa JG, Wahleithner JA, Peacock WJ (1990) OCSBF-1, a maize ocs enhancer binding factor: isolation and expression during development. Plant Cell 2:891–903
Staiger D, Kaulen H, Schell J (1989) A CACGTG motif of theAntirrhinum majus calcone synthase promoter is recognized by an evolutionaily conserved nuclear proteins. Proc Natl Acad Sci USA 86:6930–6934
Susek RE, Ausubel FM, Chory J (1994) Signal transduction mutants ofArabidopsis uncouple nuclearCAB andRBCS gene expression from chloroplast development. Cell 74:787–799
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
Tabata T, Takase H, Takayama S, Mikami K, Nakatsuka A, Kawata T, Nakayama T, Iwabuchi M (1989) A protein that binds to acis-acting element of wheat histone genes has a leucine zipper motif. Science 245:965–967
Takase H, Iwabuchi M (1993) Transcriptional and post-transcriptional regulation of the expression of wheat histone genes:cis-acting elements andtrans-acting factors. J Plant Res Special Issue 3:37–50
Terada R, Nakayama T, Iwabuchi M, Shimamoto K (1993) A wheat histone H3 promoter confers cell division-dependent and-independent expression of the gusA gene in transgenic rice plants. Plant J 3:241–252
Terada R, Nakayama T, Iwabuchi M, Shimamoto K (1995) A type I element composed of the hexamer (ACGTCA) and octamer (CGCGGATC) motifs plays a role(s) in meristematic expression of a wheat histone H3 gene in transgenic rice plants. Plant Mol Biol 27:17–26
Van Beveren C, van Straaten F, Curran T, Müller R, Verma IM (1983) Analysis of FBJ-MuSV provirus andc-fos (mouse) gene reveals that viral and cellularfos gene products have different carboxyl termini. Cell 32:1241–1255
Weisshaar B, Armstrong GA, 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
Zhang B, Singh K (1994) Ocs element promoter sequences are activated by auxin and salicylic acid inArabidopsis. Proc Natl Acad Sci USA 91:2507–2511
Author information
Authors and Affiliations
Additional information
Communicated by K. Isono
Rights and permissions
About this article
Cite this article
Mikami, K., Katsura, M., Ito, T. et al. Developmental and tissue-specific regulation of the gene for the wheat basic/leucine zipper protein HBP-1a(17) in transgenicArabidopsis plants. Molec. Gen. Genet. 248, 573–582 (1995). https://doi.org/10.1007/BF02423453
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02423453