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High diversity of plastidial promoters in Arabidopsis thaliana

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Abstract

Arabidopsis thaliana is well established as a model plant in modern plant biology. However, remarkably few details are known about plastidial promoters in Arabidopsis. Here, we report on the identification and analyses of sequences at transcription start sites of selected genes. The genes encoded by the plastome of higher plants are transcribed by a plastid-encoded (PEP) and a nuclear-encoded RNA plastid polymerase (NEP). To discriminate between NEP and PEP promoters we compared the 5′-ends of transcripts from chlorophyll-deficient Arabidopsis plants, which were grown on prokaryotic translation inhibitor spectinomycin to inhibit biosynthesis of PEP, with those of untreated plants. Using 5′-RACE combined with enzymatic treatment of RNAs to recognize primary and secondary 5′-ends, we unambiguously identified transcription initiation sites of the Arabidopsis accD, atpB, atpI, rpoB, rps4, rps15, and ycf1 genes. Comparison of plastidial promoters from tobacco and Arabidopsis revealed a high diversity, which may also apply to other plants. Furthermore, the diversity in individual promoter usage in different plants suggests that there are species-specific solutions for attaining control over gene expression in plastids.

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References

  • Baeza L, Bertrand A, Mache R, Lerbs-Mache S (1991) Characterization of a protein binding sequence in the promoter region of the 16S rRNA gene of the spinach chloroplast genome. Nucleic Acids Res 19:3577–3581

    Article  PubMed  CAS  Google Scholar 

  • Baumgartner BJ, Rapp JC, Mullet JE (1993) Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development: evidence for selective stabilization of psbA mRNA. Plant Physiol 101:781–791

    PubMed  CAS  Google Scholar 

  • Bensing BA, Meyer BJ, Dunny GM (1996) Sensitive detection of bacterial transcription initiation sites and differentiation from RNA processing sites in the pheromone-induced plasmid transfer system of Enterococcus faecalis. Proc Natl Acad Sci USA 93:7794–7799

    Article  PubMed  CAS  Google Scholar 

  • Berg S, Krause K, Krupinska K (2004) The rbcL genes of two Cuscuta species, C. gronovii and C. subinclusa, are transcribed by the nuclear-encoded plastid RNA polymerase (NEP). Planta 219:541–546

    Article  PubMed  CAS  Google Scholar 

  • Binder S, Brennicke A (2003) Gene expression in plant mitochondria: transcriptional and post-transcriptional control. Philos Trans R Soc Lond B Biol Sci 358:181–189

    Article  PubMed  CAS  Google Scholar 

  • Bisanz-Seyer C, Li Y-F, Seyer P, Mache R (1989) The components of the plastid ribosome are not accumulated synchronously during the early development of spinach plants. Plant Mol Biol 12:201–211

    Article  CAS  Google Scholar 

  • Cahoon AB, Harris FM, Stern DB (2004) Analysis of developing maize plastids reveals two mRNA stability classes correlating with RNA polymerase type. EMBO Rep 5:801–806

    Article  PubMed  CAS  Google Scholar 

  • Chang C-C, Sheen J, Bligny M, Niwa Y, Lerbs-Mache S, Stern DB (1999) Functional analysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell 11:911–926

    Article  PubMed  CAS  Google Scholar 

  • Christopher DA, Mullet JE (1994) Separate photosensory pathways co-regulate blue light/ultraviolet-A-activated psbD-psbC transcription and light-induced D2 and CP43 degradation in barley (Hordeum vulgare) chloroplasts. Plant Physiol 104:1119–1129

    Article  PubMed  CAS  Google Scholar 

  • Demarsy E, Courtois F, Azevedo J, Buhot L, Lerbs-Mache S (2006) Building up of the plastid transcriptional machinery during germination and early plant development. Plant Physiol 142:993–1003

    Article  PubMed  CAS  Google Scholar 

  • Emanuel C, Weihe A, Graner A, Hess WR, Börner T (2004) Chloroplast development affects expression of phage-type RNA polymerases in barley leaves. Plant J 38:460–472

    Article  PubMed  CAS  Google Scholar 

  • Fey V, Wagner R, Brautigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmuller R, Pfannschmidt T (2005) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280:5318–5328

    Article  PubMed  CAS  Google Scholar 

  • Forsberg J, Rosenquist M, Fraysse L, Allen JF (2001) Redox signalling in chloroplasts and mitochondria: genomic and biochemical evidence for two-component regulatory systems in bioenergetic organelles. Biochem Soc Trans 29:403–407

    Article  PubMed  CAS  Google Scholar 

  • Gray MW (1993) Origin and evolution of organelle genomes. Curr Opin Genet Dev 3:884–890

    Article  PubMed  CAS  Google Scholar 

  • Gruissem W, Tonkyn JC (1993) Control mechanisms of plastid gene expression. Crit Rev Plant Sci 12:19–55

    CAS  Google Scholar 

  • Gruissem W, Greenberg BM, Zurawski G, Hallick RB (1986) Chloroplast gene expression and promoter identification in chloroplast extracts. Methods Enzymol 118:253–270

    PubMed  CAS  Google Scholar 

  • Hajdukiewicz PTJ, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16:4041–4048

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hanaoka M, Kanamaru K, Takahashi H, Tanaka K (2003) Molecular genetic analysis of chloroplast gene promoters dependent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase, in Arabidopsis thaliana. Nucleic Acids Res 31:7090–7098

    Article  PubMed  CAS  Google Scholar 

  • Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep 6:545–550

    Article  PubMed  CAS  Google Scholar 

  • Hess WR, Börner T (1999) Organellar RNA polymerases of higher plants. Int Rev Cytol 190:1–59

    Article  PubMed  CAS  Google Scholar 

  • Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T (1993) Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J 12:563–571

    PubMed  CAS  Google Scholar 

  • Hoffer PH, Christopher DA (1997) Structure and blue-light-responsive transcription of a chloroplast psbD promoter from Arabidopsis thaliana. Plant Physiol 115:213–222

    Article  PubMed  CAS  Google Scholar 

  • Inada H, Seki M, Morikawa H, Nishimura M, Iba K (1997) Existence of three regulatory regions each containing a highly conserved motif in the promoter of plastid-encoded RNA polymerase gene (rpoB). Plant J 11:883–890

    Article  PubMed  CAS  Google Scholar 

  • Iratni R, Diederich L, Harrak H, Bligny M, Lerbs-Mache S (1997) Organ-specific transcription of the rrn operon in spinach plastids. J Biol Chem 272:13676–13682

    Article  PubMed  CAS  Google Scholar 

  • Kapoor S, Sugiura M (1999) Identification of two essential sequence elements in the nonconsensus Type II PatpB-290 plastid promoter by using plastid transcription extracts from cultured tobacco BY-2 cells. Plant Cell 11:1799–1810

    Article  PubMed  CAS  Google Scholar 

  • Kapoor S, Suzuki JY, Sugiura M (1997) Identification and functional significance of a new class of non-consensus-type plastid promoters. Plant J 11:327–337

    Article  PubMed  CAS  Google Scholar 

  • Khan MS (2005) Unraveling the complexities of plastid transcription in plants. Trends Biotech 23:535–538

    Article  CAS  Google Scholar 

  • Krause K, Berg S, Krupinska K (2003) Plastid transcription in the holoparasitic plant genus Cuscuta: parallel loss of the rrn16 PEP-promoter and of the rpoA and rpoB genes coding for the plastid-encoded RNA polymerase. Planta 216:815–823

    PubMed  CAS  Google Scholar 

  • Krause K, Maier RM, Kofer W, Krupinska K, Herrmann RG (2000) Disruption of plastid-encoded RNA polymerase genes in tobacco: expression of only a distinct set of genes is not based on selective transcription of the plastid chromosome. Mol Gen Genet 263:1022–1030

    Article  PubMed  CAS  Google Scholar 

  • Kühn K, Weihe A, Börner T (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res 33:337–346

    Article  PubMed  CAS  Google Scholar 

  • Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RM (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 31:171–188

    Article  PubMed  CAS  Google Scholar 

  • Lerbs-Mache S (1993) The 110-kDa polypeptide of spinach plastid DNA-dependent RNA polymerase: single-subunit enzyme or catalytic core of multimeric enzyme complexes? Proc Natl Acad Sci USA 90:5509–5513

    Article  PubMed  CAS  Google Scholar 

  • Liere K, Börner T (2007) Transcription of plastid genes. In: Grasser KD (ed) Regulation of transcription in plants. Blackwell, Oxford, pp 184–224

    Google Scholar 

  • Liere K, Kaden D, Maliga P, Börner T (2004) Overexpression of phage-type RNA polymerase RpoTp in tobacco demonstrates its role in chloroplast transcription by recognizing a distinct promoter type. Nucleic Acids Res 32:1159–1165

    Article  PubMed  CAS  Google Scholar 

  • Liere K, Kestermann M, Müller U, Link G (1995) Identification and characterization of the Arabidopsis thaliana chloroplast DNA region containing the genes psbA, trnH and rps19′. Curr Genet 28:128–130

    Article  PubMed  CAS  Google Scholar 

  • Liere K, Maliga P (1999) In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage-type plastid and plant mitochondrial promoters. EMBO J 18:249–257

    Article  PubMed  CAS  Google Scholar 

  • Liere K, Maliga P (2001) Plastid RNA Polymerases. In: Andersson B, Aro E-M (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 29–49

    Google Scholar 

  • Link G (1994) Plastid differentiation: organelle promoters and transcription factors. In: Nover L (ed) Plant promoters and transcription factors—results and problems in cell differentiation. Springer, Berlin, pp 65–85

    Google Scholar 

  • López-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577

    Article  PubMed  CAS  Google Scholar 

  • Maliga P (1998) Two plastid polymerases of higher plants: an evolving story. Trends Plant Sci 3:4–6

    Article  Google Scholar 

  • Meng BY, Tanaka M, Wakasugi T, Ohme M, Shinozaki K, Sugiura M (1988) Cotranscription of the genes encoding two P700 chlorophyll a apoproteins with the gene for ribosomal protein CS14: determination of the transcriptional initiation site by in vitro capping. Curr Genet 14:395–400

    Article  PubMed  CAS  Google Scholar 

  • Miyagi T, Kapoor S, Sugita M, Sugiura M (1998) Transcript analysis of the tobacco plastid operon rps2/atpI/H/F/A reveals the existence of a non-consensus type II (NCII) promoter upstream of the atpI coding sequence. Mol Gen Genet 257:299–307

    Article  PubMed  CAS  Google Scholar 

  • Moazed D, Noller HF (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327:389–394

    Article  PubMed  CAS  Google Scholar 

  • Nagashima A, Hanaoka M, Motohashi R, Seki M, Shinozaki K, Kanamaru K, Takahashi H, Tanaka K (2004) DNA microarray analysis of plastid gene expression in an Arabidopsis mutant deficient in a plastid transcription factor sigma, SIG2. Biosci Biotechnol Biochem 68:694–704

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Liere K (2005) Redox regulation and modification of proteins controlling chloroplast gene expression. Antioxid Redox Signal 7:607–618

    Article  PubMed  CAS  Google Scholar 

  • Reznikov W, Siegle DA, Cowing DW, Gross CA (1985) The regulation of transcription initiation in bacteria. Annu Rev Genet 19:355–387

    Article  Google Scholar 

  • Serino G, Maliga P (1998) RNA polymerase subunits encoded by the plastid rpo genes are not shared with the nucleus-encoded plastid enzyme. Plant Physiol 117:1165–1170

    Article  PubMed  CAS  Google Scholar 

  • Shen Y, Danon A, Christopher DA (2001) RNA binding-proteins interact specifically with the Arabidopsis chloroplast psbA mRNA 5′ untranslated region in a redox-dependent manner. Plant Cell Physiol 42:1071–1078

    Article  PubMed  CAS  Google Scholar 

  • Shiina T, Tsunoyama Y, Nakahira Y, Khan MS (2005) Plastid RNA polymerases, promoters, and transcription regulators in higher Plants. In: Int Rev Cytol, Academic Press, New York, pp 1–68

  • Sikdar SR, Serino G, Chaudhuri S, Pal M (1998) Plastid transformation in Arabidopsis thaliana. Plant Cell Rep V 18:20–24

    Article  CAS  Google Scholar 

  • Silhavy D, Maliga P (1998) Mapping of the promoters for the nucleus-encoded plastid RNA polymerase (NEP) in the iojap maize mutant. Curr Genet 33:340–344

    Article  PubMed  CAS  Google Scholar 

  • Sriraman P, Silhavy D, Maliga P (1998a) The phage-type PclpP-53 plastid promoter comprises sequences downstream of the transcription initiation site. Nucleic Acids Res 26:4874–4879

    Article  CAS  Google Scholar 

  • Sriraman P, Silhavy D, Maliga P (1998b) Transcription from heterologous rRNA operon promoters in chloroplasts reveals requirement for specific activating factors. Plant Physiol 117:1495–1499

    Article  CAS  Google Scholar 

  • Tahar SB, Bottomley W, Whitfeld PR (1986) Characterization of the spinach chloroplast genes for the S4 ribosomal protein, tRNAThr (UGU) and tRNASer (GGA). Plant Mol Biol 7:63–70

    Article  CAS  Google Scholar 

  • Vera A, Sugiura M (1995) Chloroplast rRNA transcription from structurally different tandem promoters: an additional novel-type promoter. Curr Genet 27:280–284

    Article  PubMed  CAS  Google Scholar 

  • Weihe A (2004) The transcription of plant organelle genomes. In: Daniell H, Chase CD (eds) Molecular biology and biotechnology of plant organelles. Kluwer, Dordrecht, pp 213–237

    Google Scholar 

  • Weihe A, Börner T (1999) Transcription and the architecture of promoters in chloroplasts. Trends Plant Sci 4:169–170

    Article  PubMed  Google Scholar 

  • Wolfe KH, Morden CW, Ems SC, Palmer JD (1992a) Rapid evolution of the plastid translational apparatus in a nonphotosynthetic plant: loss or accelerated sequence evolution of tRNA and ribosomal protein genes. J Mol Evol 35:304–317

    Article  CAS  Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1992b) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652

    Article  CAS  Google Scholar 

  • Zoschke R, Liere K, Börner T (2007) From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J:in press

  • Zubko MK, Day A (1998) Stable albinism induced without mutagenesis: a model for ribosome free plastid inheritance. Plant J 15:265–271

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thankfully acknowledge the participation of Daniela Kaden and Kristina Kühn in the initial phase of our studies on initiation sites of chloroplast transcripts. This work was supported by grants from the Deutsche Forschungsgemeinschaft (SFB429).

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  1. Institut für Biologie (Genetik), Humboldt-Universität zu Berlin, Chausseestrasse 117, 10115, Berlin, Germany

    Monika Swiatecka-Hagenbruch, Karsten Liere & Thomas Börner

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  1. Monika Swiatecka-Hagenbruch
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  2. Karsten Liere
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  3. Thomas Börner
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Correspondence to Karsten Liere.

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Communicated by R. Herrmann.

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Swiatecka-Hagenbruch, M., Liere, K. & Börner, T. High diversity of plastidial promoters in Arabidopsis thaliana . Mol Genet Genomics 277, 725–734 (2007). https://doi.org/10.1007/s00438-007-0222-4

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