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Multiple transcripts of a gene for a leucine-rich repeat receptor kinase from morning glory (Ipomoea nil) originate from different TATA boxes in a tissue-specific manner

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Abstract

TATA boxes are the most common regulatory elements found in the promoters of eukaryotic genes because they are associated with basal transcription initiation by RNA polymerase II. Often only a single TATA element is found in a given promoter, and tissue-, stage- and/or stimulus-specific expression occurs because the TATA box is associated with other cis -acting elements that enhance or repress transcription. We used software tools for gene analysis to assist in locating potential TATA box(es) in an AT-rich region of the promoter of a gene, inrpk1, which codes for a leucine-rich receptor protein kinase in morning glory (Ipomoea nil). Through the use of RT-PCR and various combinations of forward primers bracketing most of the promoter region we were able to define the 5′-ends of transcripts in this region. The region was then targeted for analysis by RNA Ligase-Mediated-5′ Rapid Amplification of cDNA Ends (RLM-5′ RACE) to identify the transcript initiation site(s). Positioning of initiation sites with respect to TATA boxes identified by gene analysis tools allowed us to identify three operational TATA elements which regulate basal transcription from this gene. Two TATA boxes were responsible for all of the inrpk1 transcripts found in leaves and cotyledons, and about 25–30% of the transcripts in roots. A third TATA box was involved only in expression in roots and accounted for the remaining 50–70% of root transcripts. RNAs expressed from this element lack two potentially functional upstream AUG codons, and may be translated more efficiently than transcripts originating from the other TATA boxes.

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References

  • Akiyama Y (1995) TFSEARCH: searching transcription factor binding sites. Available at http://www.cbrc.jp/research/db/TFSEARCH.html

  • Arrick BA, Grendell RL, Griffin LA (1994) Enhanced translational efficiency of a novel transforming growth factor 3 mRNA in human breast cancer cells. Mol Cell Biol 14:619–628

    CAS  PubMed  Google Scholar 

  • Bassett CL, Nickerson ML, Cohen RA, Rajeevan MS (2000) Alternative transcript initiation and novel post-transcriptional processing of a leucine-rich repeat receptor-like protein kinase gene that responds to short-day photoperiodic floral induction in morning glory (Ipomoea nil). Plant Mol Biol 43:43–58

    Article  CAS  PubMed  Google Scholar 

  • Bucher P (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 212:563–578

    CAS  PubMed  Google Scholar 

  • Burke TW, Kadonaga JT (1996) Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-box-deficient promoters. Genes Dev 10:711–724

    CAS  PubMed  Google Scholar 

  • Burley SK, Kamada K (2002) Transcription factor complexes. Curr Opin Struct Biol 12:225–230

    Article  CAS  PubMed  Google Scholar 

  • Chappell SA, Mauro VP (2003) The internal ribosome entry site (IRES) contained within the RNA-binding motif protein 3 (Rbm3) mRNA is composed of functionally distinct elements. J Biol Chem 278:33793–33800

    Article  CAS  PubMed  Google Scholar 

  • Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 Angstrom resolution. Science 292:1863–1876

    Article  CAS  PubMed  Google Scholar 

  • Damiani RD Jr, 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

    CAS  PubMed  Google Scholar 

  • Fra AM, Pasqualetto E, Mancini M, Sitia R (2000) Genomic organization and transcriptional analysis of the human genes coding for caveolin-1 and caveolin-2. Gene 243:75–83

    Article  CAS  PubMed  Google Scholar 

  • Gidoni D, Brosio P, Bond-Nutter D, Bedbrook J, Dunsmuir P (1989) Novel cis -acting elements in Petunia cab gene promoters. Mol Gen Genet 215:337–344

    CAS  PubMed  Google Scholar 

  • Haley J, Bogorad L (1990) Alternative promoters are used for genes within maize chloroplast polycistronic transcription units. Plant Cell 2:323–333

    Article  CAS  PubMed  Google Scholar 

  • Han B, Zhang JT (2002) Regulation of gene expression by internal ribosome entry sites or cryptic promoters: the eIF4G story. Mol Cell Biol 22:7372–7384

    Article  CAS  PubMed  Google Scholar 

  • Hochheimer A, Tjian R (2003) Diversified transcription initiation complexes expand promoter selectivity and tissue-specific gene expression. Genes Dev 17:1309–1320

    Article  CAS  PubMed  Google Scholar 

  • Joshi CP (1987) An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucleic Acids Res 15:6643–6651

    CAS  PubMed  Google Scholar 

  • Joshi CP, Zhou H, Huang X, Chiang VL (1997) Context sequences of translation initiation codon in plants. Plant Mol Biol 35:993–1001

    CAS  PubMed  Google Scholar 

  • Kondrakhin YV, Kel AE, Kolchanov NA, Romashchenko AG, Milanesi L (1995) Eukaryotic promoter recognition by binding sites for transcription factors. Comp Appl Biosci 11:477–488

    CAS  PubMed  Google Scholar 

  • Kozak M (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125–8148

    CAS  PubMed  Google Scholar 

  • Kozak M (1991) An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 115:887–903

    CAS  PubMed  Google Scholar 

  • Kozak M (2001) Constraints on reinitiation of translation in mammals. Nucleic Acids Res 29:5226–5232

    Article  CAS  PubMed  Google Scholar 

  • Kozak M (2002) Pushing the limits of the scanning mechanism for intiation of translation. Gene 299:1–34

    Article  CAS  Google Scholar 

  • Lagrange T, Kapanidis AN, Tang H, Reinberg D, Ebright RH (1998) New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. Genes Dev 12:34–44

    CAS  PubMed  Google Scholar 

  • Lee SW, Heinz R, Robb J, Nazar RN (1994) Differential utilization of alternate initiation sites in a plant defense gene responding to environmental stimuli. Eur J Biochem 226:109–114

    CAS  PubMed  Google Scholar 

  • Lewin B (2000) Genes VII. Oxford University Press. New York, NY

  • Luo M, Orsi R, Patrucco E, Pancaldi S, Cella R (1997) Multiple transcription start sites of the carrot dihydrofolate reductase-thymidylate synthase gene, and sub-cellular localization of the bifunctional protein. Plant Mol Biol 33:709–722

    Article  CAS  PubMed  Google Scholar 

  • Lupold DS, Caoile AGFS, Stern DB (1999) The maize mitochondrial cox2 gene has five promoters in two genomic regions, including a complex promoter consisting of seven overlapping units. J Biol Chem 274:3897–3903

    Article  CAS  PubMed  Google Scholar 

  • Mauro VP, Nguyen T, Katinakis P, Verma DPS (1985) Primary structure of the soybean nodulin-23 gene and potential regulatory elements in the 5′-flanking regions of nodulin and leghemoglobin genes. Nucleic Acids Res 13:239–249

    CAS  PubMed  Google Scholar 

  • Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell Physiol 36:1405–1420

    CAS  PubMed  Google Scholar 

  • Michelet B, Lukaszewicz M, Dupriez V, Boutry M (1994) A plant plasma membrane proton-ATPase gene is regulated by development and environment and shows signs of a translational regulation. Plant Cell 6:1375–1389

    CAS  PubMed  Google Scholar 

  • Milanesi L, Muselli M, Arrigo P (1996) Hamming Clustering method for signal prediction in 5′ and 3′ regions of eukaryotic genes. Comp Appl Biosci 12:399–404

    CAS  PubMed  Google Scholar 

  • Mireau H, Lancelin D, Small ID (1996) The same Arabidopsis gene encodes both cytosolic and mitochondrial alanyl-tRNA synthetases. Plant Cell 8:1027–1039

    Article  CAS  PubMed  Google Scholar 

  • Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635–8642

    Article  CAS  PubMed  Google Scholar 

  • Navarro-Avino JP, Hentzen AE, Bennett AB (1999) Alternative transcription initiation sites generate two LCA1 Ca2+-ATPase mRNA transcripts in tomato roots. Plant Mol Biol 40:133–140

    Article  CAS  PubMed  Google Scholar 

  • Patikoglou GA, Kim JL, Sun L, Yang SH, Kodadek T, Burley SK (1999) TATA element recognition by the TATA box-binding protein has been conserved throughout evolution. Genes Dev 13:3217–3230.

    Article  CAS  PubMed  Google Scholar 

  • Pan S, Czarnecka-Verner E, Gurley WB (2000) Role of TATA binding protein-transcription factor IIB interaction in supporting basal and activated transcription in plant cells. Plant Cell 12:125–135

    Google Scholar 

  • Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comp Appl Biosci 7:203–206

    CAS  PubMed  Google Scholar 

  • Procissi A, Piazza P, Tonelli C (2002) A maize r1 gene is regulated post-transcriptionally by differential splicing of its leader. Plant Molec Biol 49:239–248

    Article  CAS  Google Scholar 

  • Quandt K, Frech K, Karas H, Wingender E, Werner T (1995) MatInd and MatInspector—new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23:4878–4884

    CAS  PubMed  Google Scholar 

  • Reese MG, Harris NL, Eeckman FH (1995) Large scale sequencing specific neural networks for promoter and splice site recognition. In: Hunter L, Klein T (eds) Proceedings of the 1996 Pacific Symposium on Biocomputing, World Scientific Press, New Jersey, pp 776

  • Schug J, Overton GC (1997) TESS: Transcription Element Search Software on the WWW. Technical Report CBIL-TR-1997-1001-v0.0. Computational Biology and Informatics Laboratory, School of Medicine, University of Pennsylvania

  • Shenk T (1981) Transcriptional control regions: nucleotide sequence requirements for initiation by RNA polymerase II and III. Curr Topics Microbiol Immunol 93:25–46

    CAS  Google Scholar 

  • Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3:225–245

    Article  CAS  PubMed  Google Scholar 

  • Short KC, Torrey JG (1972) Cytokinins in seedling roots of pea. Plant Physiol 49:155–160

    CAS  Google Scholar 

  • Smale ST, Baltimore D (1989) The “initiator” as a transcription control element. Cell 57:103–113

    CAS  PubMed  Google Scholar 

  • Tamaoki M, Tsugawa H, Minami E, Kayano T, Yamamoto N, Kano-Murakami Y, Matsuoka M (1995) Alternative RNA products from a rice homeobox gene. Plant J 7:927–938

    CAS  PubMed  Google Scholar 

  • Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345:743–746

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Wessler SR (1998) Inefficient reinitiation is responsible for upstream open reading frame-mediated translational repression of the maize R gene. Plant Cell 10:1733–1745

    Google Scholar 

  • Wang Y, Jensen RC, Stumph WE (1996) Role of TATA box sequence and orientation in determining RNA polymerase II/III transcription specificity. Nucleic Acids Res 24:3100–3106

    Article  CAS  PubMed  Google Scholar 

  • Wassarman DA, Sauer F (2001). TAFII250: a transcription toolbox. J Cell Sci 114:2895–2902

    CAS  PubMed  Google Scholar 

  • Zhang Y, Niu Z, Cohen AJ, Nah H-D, Adams SL (1997) The chick type III collagen gene contains two promoters that are preferentially expressed in different cell types and are separated by over 20 kb of DNA containing 23 exons. Nucleic Acids Res 25:2470–2477

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge that all work presented in this paper was carried out in compliance with current regulations guiding recombinant DNA experimentation. The authors would like to thank Dr. Tim Artlip for assistance with designing the gene-specific primer used in the RLM-5′RACE experiment. We would also like to acknowledge the expert technical assistance of Jami Young. As always, we acknowledge our debt to El Elyon

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Correspondence to C. L. Bassett.

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Communicated by D. Y. Thomas

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Bassett, C.L., Nickerson, M.L., Farrell, R.E. et al. Multiple transcripts of a gene for a leucine-rich repeat receptor kinase from morning glory (Ipomoea nil) originate from different TATA boxes in a tissue-specific manner. Mol Genet Genomics 271, 752–760 (2004). https://doi.org/10.1007/s00438-004-1031-7

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