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Transcription in Plant Mitochondria

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Part of the book series: Advances in Plant Biology ((AIPB,volume 1))

Abstract

Transcription in plant mitochondria is sustained by phage-type RNA polymerases that are encoded by a small nuclear encoded RpoT gene family (RNA polymerase of the T-phage type). In angiosperms, it consists of a minimum of two genes, encoding enzymes that are imported into mitochondria (RpoTm) and plastids (RpoTp). An additional gene for a dually targeted enzyme is found in eudicots (RpoTmp). The promoters recognized by mitochondrial RpoT enzymes contain a CRTA-, YYTA-, or DDTA-motif, often accompanied by an upstream A/T-rich region involved in modulating transcription. Transcription of most mitochondrial genes is driven by multiple promoters. Multiple promoters may ensure transcription despite possible mitochondrial genome rearrangements. Transcription factors have not been identified in plant mitochondria. Although proteins related to transcription factors in fungal and animal mitochondria (mtTFA and mtTFB) are encoded in the nuclear genome of Arabidopsis, none of these proteins has been shown to function as a factor assisting RNA polymerases in promoter recognition.

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References

  • Amiott, E. A., Jaehning, J. A. 2006. Mitochondrial transcription is regulated via an ATP “sensing” mechanism that couples RNA abundance to respiration. Mol. Cell 22:329–338.

    Article  PubMed  CAS  Google Scholar 

  • Antoshechkin, I., Bogenhagen, D. F. 1995. Distinct roles for two purified factors in transcription of Xenopus mitochondrial DNA. Mol. Cell. Biol. 15:7032–7042.

    PubMed  CAS  Google Scholar 

  • Antoshechkin, I., Bogenhagen, D. F., Mastrangelo, I. A. 1997. The HMG-box mitochondrial transcription factor xl-mtTFA binds DNA as a tetramer to activate bidirectional transcription. EMBO J. 16:3198–3206.

    Article  PubMed  CAS  Google Scholar 

  • Asin-Cayuela, J., Gustafsson, C. M. 2007. Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem. Sci. 32:111–117.

    Article  PubMed  CAS  Google Scholar 

  • Azevedo, J., Courtois, F., Hakimi, M.-A., Demarsy, E., Lagrange, T., Alcaraz, J.-P., Jaiswal, P., Maréchal-Drouard, L., Lerbs-Mache, L. 2008. Intraplastidial trafficking of a phage-type RNA polymerase is mediated by a thylakoid RING-H2 protein. Proc. Natl. Acad. Sci. USA 105:9123–9128.

    Article  PubMed  CAS  Google Scholar 

  • Azevedo, J., Courtois, F., Lerbs-Mache, S. 2006. Sub-plastidial localization of two different phage-type RNA polymerases in spinach chloroplasts. Nucleic Acids Res. 34:436–444.

    Article  PubMed  CAS  Google Scholar 

  • Baba, K., Schmidt, J., Espinosa-Ruiz, A., Villarejo, A., Shiina, T., Gardestrom, P., Sane, A. P., Bhalerao, R. P. 2004. Organellar gene transcription and early seedling development are affected in the RpoT;2 mutant of Arabidopsis. Plant J. 38:38–48.

    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. 358:181–188; discussion 188–189.

    Article  CAS  Google Scholar 

  • Binder, S., Hatzack, F., Brennicke, A. 1995. A novel pea mitochondrial in vitro transcription system recognizes homologous and heterologous mRNA and tRNA promoters. J. Biol. Chem. 270:22182–22189.

    Article  PubMed  CAS  Google Scholar 

  • Binder, S., Marchfelder, A., Brennicke, A. 1996. Regulation of gene expression in plant mitochondria. Plant Mol. Biol. 32:303–314.

    Article  PubMed  CAS  Google Scholar 

  • Caoile, A. G. F. S., Stern, D. B. 1997. A conserved core element is functionally important for maize mitochondrial promoter activity in vitro. Nucleic Acids Res. 25:4055–4060.

    Article  PubMed  CAS  Google Scholar 

  • Cermakian, N., Ikeda, T. M., Cedergren, R., Gray, M. W. 1996. Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res. 24:648–654.

    Article  PubMed  CAS  Google Scholar 

  • Cermakian, N., Ikeda, T. M., Miramontes, P., Lang, B. F., Gray, M. W., Cedergren, R. 1997. On the evolution of the single-subunit RNA polymerases. J. Mol. Evol. 45:671–681.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cheetham, G. M., Jeruzalmi, D., Steitz, T. A. 1999. Structural basis for initiation of transcription from an RNA polymerase-promoter complex. Nature 399:80–83.

    Article  PubMed  CAS  Google Scholar 

  • Christensen, A. C., Lyznik, A., Mohammed, S., Elowsky, C. G., Elo, A., Yule, R., Mackenzie, S. A. 2005. Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 17:2805–2816.

    Article  PubMed  CAS  Google Scholar 

  • Clifton, S. W., Minx, P., Fauron, C. M.-R., Gibson, M., Allen, J. O., Sun, H., Thompson, M., Barbazuk, W. B., Kanuganti, S., Tayloe, C., Meyer, L., Wilson, R. K., Newton, K. J. 2004. Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol. 136:3486–3503.

    Article  PubMed  CAS  Google Scholar 

  • Courtois, F., Merendino, L., Demarsy, E., Mache, R., Lerbs-Mache, S. 2007. Phage-type RNA polymerase RPOTmp transcribes the rrn operon from the PC promoter at early developmental stages in Arabidopsis. Plant Physiol. 145:712–721.

    Article  PubMed  CAS  Google Scholar 

  • Daga, A., Micol, V., Hess, D., Aebersold, R., Attardi, G. 1993. Molecular characterization of the transcription termination factor from human mitochondria. J. Biol. Chem. 268:8123–8130.

    PubMed  CAS  Google Scholar 

  • Dairaghi, D. J., Shadel, G. S., Clayton, D. A. 1995a. Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim. Biophys. Acta 1271:127–134.

    Article  PubMed  Google Scholar 

  • Dairaghi, D. J., Shadel, G. S. and Clayton, D. A. 1995b. Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim. Biophys. Acta 1271:127–134.

    Article  PubMed  Google Scholar 

  • Däschner, K., Couée, I., Binder, S. 2001. The mitochondrial isovaleryl-coenzyme a dehydrogenase of Arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiol. 126:601–612.

    Article  PubMed  Google Scholar 

  • Däschner, K., Thalheim, C., Guha, C., Brennicke, A., Binder, S. 1999. In plants a putative isovaleryl-CoA-dehydrogenase is located in mitochondria. Plant Mol. Biol. 39:1275–1282.

    PubMed  Google Scholar 

  • Delarue, M., Poch, O., Tordo, N., Moras, D., Argos, P. 1990. An attempt to unify the structure of polymerases. Protein Eng. 3:461–467.

    Article  PubMed  CAS  Google Scholar 

  • Diffley, J. F., Stillman, B. 1991. A close relative of the nuclear, chromosomal high-mobility group protein HMG1 in yeast mitochondria. Proc. Natl. Acad. Sci. USA 88:7864–7868.

    Article  PubMed  CAS  Google Scholar 

  • Diffley, J. F., Stillman, B. 1992. DNA binding properties of an HMG1-related protein from yeast mitochondria. J. Biol. Chem. 267:3368–3374.

    PubMed  CAS  Google Scholar 

  • Dombrowski, S., Hoffmann, M., Guha, C., Binder, S. 1999. Continuous primary sequence requirements in the 18-nucleotide promoter of dicot plant mitochondria. J. Biol. Chem. 274:10094–10099.

    Article  PubMed  CAS  Google Scholar 

  • Dombrowski, S., Hoffmann, M., Kuhn, J., Brennicke, A., Binder, S. 1998. On mitochondrial promoters in Arabidopsis thaliana and other flowering plants. In Plant Mitochondria: From Gene to Function, I. M. Möller, P. Gardeström, K. Glimelius, E. Glaser eds., pp. 165–170. Leiden, Netherlands: Backhuys Publishers.

    Google Scholar 

  • Edqvist, J., Bergman, P. 2002. Nuclear identity specifies transcriptional initiation in plant mitochondria. Plant Mol. Biol. 49:59–68.

    Article  PubMed  CAS  Google Scholar 

  • Elo, A., Lyznik, A., Gonzalez, D. O., Kachman, S. D., Mackenzie, S. A. 2003. Nuclear genes that encode mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome. Plant Cell 15:1619–1631.

    Article  PubMed  CAS  Google Scholar 

  • Emanuel, C., von Groll, U., Müller, M., Börner, T., Weihe, A. 2006. Development- and tissue-specific expression of the RpoT gene family of Arabidopsis encoding mitochondrial and plastid RNA polymerases. Planta 223:998–1009.

    Article  PubMed  CAS  Google Scholar 

  • Emanuel, C., Weihe, A., Graner, A., Hess, W. R., 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 

  • Falkenberg, M., Gaspari, M., Rantanen, A., Trifunovic, A., Larsson, N.-G., Gustafsson, C. M. 2002. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 31:289–294.

    Article  PubMed  CAS  Google Scholar 

  • Fey, J., Maréchal-Drouard, L. 1999. Compilation and analysis of plant mitochondrial promoter sequences: an illustration of a divergent evolution between monocot and dicot mitochondria. Biochem. Biophys. Res. Commun. 256:409–414.

    Article  PubMed  CAS  Google Scholar 

  • Filée, J., Forterre, P. 2005. Viral proteins functioning in organelles: a cryptic origin? Trends Microbiol. 13: 510–513.

    Article  PubMed  CAS  Google Scholar 

  • Finnegan, P. M., Brown, G. G. 1990. Transcriptional and post-transcriptional regulation of RNA levels in maize mitochondria. Plant Cell 2:71–83.

    PubMed  CAS  Google Scholar 

  • Fisher, R. P., Clayton, D. A. 1985. A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy- and light-strand promoters dissected and reconstituted in vitro. J. Biol. Chem. 260:11330–11338.

    PubMed  CAS  Google Scholar 

  • Forner, J., Hölzle, A., Jonietz, C., Thuss, S., Schwarzländer, M., Weber, B., Meyer, R. C., Binder, S. 2008. Mitochondrial mRNA polymorphisms in different Arabidopsis accessions. Plant Physiol. 148:1106–1116.

    Article  PubMed  CAS  Google Scholar 

  • Forner, J., Weber, B., Thuss, S., Wildum, S., Binder, S. 2007. Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5′ and 3′ end formation. Nucleic Acids Res. 35:3676–3692.

    Article  PubMed  CAS  Google Scholar 

  • Gagliardi, D., Leaver, C. J. 1999. Polyadenylation accelerates the degradation of the ­mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J. 18:3757–3766.

    Article  PubMed  CAS  Google Scholar 

  • Gaspari, M., Falkenberg, M., Larsson, N. G., Gustafsson, C. M. 2004. The mitochondrial RNA polymerase contributes critically to promoter specificity in mammalian cells. EMBO J. 23:4606–4614.

    Article  PubMed  CAS  Google Scholar 

  • Giegé, P., Hoffmann, M., Binder, S., Brennicke, A. 2000. RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep. 1:164-170.

    Article  PubMed  Google Scholar 

  • Giegé, P., Sweetlove, L. J., Cognat, V., Leaver, C. J. 2005. Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell 17:1497–1512.

    Article  PubMed  CAS  Google Scholar 

  • Gray, M. W., Lang, B. F. 1998. Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol. 6:1–3.

    Article  PubMed  CAS  Google Scholar 

  • Greenleaf, A. L., Kelly, J. L., Lehman, I. R. 1986. Yeast RPO41 gene product is required for transcription and maintenance of the mitochondrial genome. Proc. Natl. Acad. Sci. USA 83:3391–3394.

    Article  PubMed  CAS  Google Scholar 

  • Handa, H. 2003. The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids. Res. 31:5907–5916.

    Article  PubMed  CAS  Google Scholar 

  • Handa, H. 2008. Linear plasmids in plant mitochondria: peaceful coexistences or malicious ­invasions? Mitochondrion 8:15–25.

    Article  PubMed  CAS  Google Scholar 

  • Hanic-Joyce, P. J., Gray, M. W. 1991. Accurate transcription of a plant mitochondrial gene in vitro. Mol. Cell. Biol. 11:2035–2039.

    PubMed  CAS  Google Scholar 

  • Hatzack, F., Dombrowski, S., Brennicke, A., Binder, S. 1998. Characterization of DNA-binding proteins from pea mitochondria. Plant Physiol. 116:519–527.

    Article  PubMed  CAS  Google Scholar 

  • Hedtke, B., Börner, T., Weihe, A. 1997. Mitochondrial and chloroplast phage-type RNA ­polymerases in Arabidopsis. Science 277:809–811.

    Article  PubMed  CAS  Google Scholar 

  • Hedtke, B., Börner, T., Weihe, A. 2000. One RNA polymerase serving two genomes. EMBO Rep. 1:435–440.

    Article  PubMed  CAS  Google Scholar 

  • Hedtke, B., Legen, J., Weihe, A., Herrmann, R. G., Börner, T. 2002. Six active phage-type RNA polymerase genes in Nicotiana tabacum. Plant J. 30:625–637.

    Article  PubMed  CAS  Google Scholar 

  • Hedtke, B., Meixner, M., Gillandt, S., Richter, E., Börner, T., Weihe, A. 1999. Green fluorescent protein as a marker to investigate targeting of organellar RNA polymerases of higher plants in vivo. Plant J. 17:557–561.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann, M., Binder, S. 2002. Functional importance of nucleotide identities within the pea atp9 mitochondrial promoter sequence. J. Mol. Biol. 320:943–950.

    Article  PubMed  CAS  Google Scholar 

  • Holec, S., Lange, H., Canaday, J., Gagliardi, D. 2008. Coping with cryptic and defective transcripts in plant mitochondria. Biochim. Biophys. Acta 1779:566–573.

    Article  PubMed  CAS  Google Scholar 

  • Huang, C. Y., Grunheit, N., Ahmadinejad, N., Timmis, J. N., Martin, W. 2005. Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol. 138:1723–1733.

    Article  PubMed  CAS  Google Scholar 

  • Ikeda, T., Gray, M. 1999a. Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol. Cell. Biol. 19:8113–8122.

    PubMed  CAS  Google Scholar 

  • Ikeda, T., Gray, M. 1999b. Genes and proteins of the transcriptional apparatus in mitochondria. J. Hered. 90:374–379.

    Article  CAS  Google Scholar 

  • Ikeda, T. M., Gray, M. W. 1999c. Identification and characterization of T7/T3 bacteriophage-like RNA polymerase sequences in wheat. Plant Mol. Biol. 40:567–578.

    Article  PubMed  CAS  Google Scholar 

  • Kabeya, Y., Hashimoto, K., Sato, N. 2002. Identification and characterization of two phage-type RNA polymerase cDNAs in the moss Physcomitrella patens: implication of recent evolution of nuclear-encoded RNA polymerase of plastids in plants. Plant Cell Physiol. 43:245–255.

    Article  PubMed  CAS  Google Scholar 

  • Kabeya, Y., Sato, N. 2005. Unique translation initiation at the second AUG codon determines mitochondrial localization of the phage-type RNA polymerases in the moss Physcomitrella patens. Plant Physiol. 138:369–382.

    Article  PubMed  CAS  Google Scholar 

  • Kempken, F., Hermanns, J., Osiewacz, H. D. 1992. Evolution of linear plasmids. J. Mol. Evol. 35:502–513.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, Y., Dokiya, Y., Kumazawa, Y., Sugita, M. 2002. Non-AUG translation initiation of mRNA encoding plastid-targeted phage-type RNA polymerase in Nicotiana sylvestris. Biochem. Biophys. Res. Commun. 299:57–61.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, Y., Dokiya, Y., Sugita, M. 2001a. Dual targeting of phage-type RNA polymerase to both mitochondria and plastids is due to alternative translation initiation in single transcripts. Biochem. Biophys. Res. Commun. 289:1106–1113.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, Y., Dokiya, Y., Sugiura, M., Niwa, Y., Sugita, M. 2001b. Genomic organization and organ-specific expression of a nuclear gene encoding phage-type RNA polymerase in Nicotiana sylvestris. Gene 279:33–40.

    Article  PubMed  CAS  Google Scholar 

  • Kruse, B., Narasimhan, N., Attardi, G. 1989. Termination of transcription in human mitochondria: identification and purification of a DNA binding protein factor that promotes termination. Cell 58:391–397.

    Article  PubMed  CAS  Google Scholar 

  • Kubo, T., Nishizawa, S., Sugawara, A., Itchoda, N., Estiati, A., Mikami, T. 2000. The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys(GCA). Nucleic Acids Res. 28:2571–2576.

    Article  PubMed  CAS  Google Scholar 

  • Kühn, K., Bohne, A.-V., Liere, K., Weihe, A., Börner, T. 2007. Arabidopsis phage-type RNA polymerases: accurate in vitro transcription of organellar genes. Plant Cell 19:959–971.

    Article  PubMed  CAS  Google Scholar 

  • Kühn, K., Richter, U., Meyer, E., Delannoy, E., Falcon de Longevialle, A., O’Toole, N., Börner, T., Millar, A., Small, I., Whelan, J. 2009. Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell 21:2762–2779.

    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 

  • Lang, B. F., Burger, G., O’Kelly, C. J., Cedergren, R., Golding, G. B., Lemieux, C., Sankoff, D., Turmel, M., Gray, M. W. 1997. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493–497.

    Article  PubMed  CAS  Google Scholar 

  • Leino, M., Landgren, M., Glimelius, K. 2005. Alloplasmic effects on mitochondrial ­transcriptional activity and RNA turnover result in accumulated transcripts of Arabidopsis ORFs in ­cytoplasmic male-sterile Brassica napus. Plant J. 42:469–480.

    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 

  • Li, X. Q., Zhang, M., Brown, G. G. 1996. Cell-specific expression of mitochondrial transcripts in maize seedlings. Plant Cell 8:1961–1975.

    PubMed  CAS  Google Scholar 

  • Liere, K., Börner, T. 2007. Transcription and transcriptional regulation in plastids. In Topics in Current Genetics: Cell and Molecular Biology of Plastids, R. Bock ed., pp. 121–174. Berlin: Springer

    Google Scholar 

  • Linder, T., Park, C. B., Asin-Cayuela, J., Pellegrini, M., Larsson, N.-G., Falkenberg, M., Samuelsson, T., Gustafsson, C. M. 2005. A family of putative transcription termination factors shared amongst metazoans and plants. Curr. Genet. 48:265–269.

    Article  PubMed  CAS  Google Scholar 

  • Lisowsky, T., Michaelis, G. 1988. A nuclear gene essential for mitochondrial replication ­suppresses a defect of mitochondrial transcription in Saccharomyces cerevisiae. Mol. Gen. Genet. 214:218–223.

    Article  PubMed  CAS  Google Scholar 

  • Lupold, D. S., Caoile, A. G., Stern, D. B. 1999a. 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  PubMed  CAS  Google Scholar 

  • Lupold, D. S., Caoile, A. G. F. S., Stern, D. B. 1999b. Genomic context influences the activity of maize mitochondrial cox2 promoters. Proc. Natl. Acad. Sci. USA 96:11670–11675.

    Article  PubMed  CAS  Google Scholar 

  • Maier, U. G., Bozarth, A., Funk, H. T., Zauner, S., Rensing, S. A., Schmitz-Linneweber, C., Börner, T., Tillich, M. 2008. Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol. 6:36.

    Article  PubMed  CAS  Google Scholar 

  • Mangus, D. A., Jang, S. H., Jaehning, J. A. 1994. Release of the yeast mitochondrial RNA polymerase specificity factor from transcription complexes. J. Biol. Chem. 269:26568–26574.

    PubMed  CAS  Google Scholar 

  • Markov, D. A., Savkina, M., Anikin, M., Del Campo, M., Ecker, K., Lambowitz, A. M., De Gnore, J. P., McAllister, W. T. 2009. Identification of proteins associated with the yeast mitochondrial RNA polymerase by tandem affinity purification. Yeast 26:423–440.

    Article  PubMed  CAS  Google Scholar 

  • Martin, W. 2003. Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc. Natl. Acad. Sci. U.S.A 100:8612–8614.

    Article  PubMed  CAS  Google Scholar 

  • Martin, M., Cho, J., Cesare, A. J., Griffith, J. D., Attardi, G. 2005. Termination factor-mediated DNA loop between termination and initiation sites drives mitochondrial rRNA synthesis. Cell 123:1227–1240.

    Article  PubMed  CAS  Google Scholar 

  • Masters, B. S., Stohl, L. L., Clayton, D. A. 1987. Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7. Cell 51:89–99.

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga, M., Jaehning, J. A. 2004. Intrinsic promoter recognition by a “core” RNA polymerase. J. Biol. Chem. 279:44239–44242.

    Article  PubMed  CAS  Google Scholar 

  • McAllister, W. 1993. Structure and function of the bacteriophage T7 RNA polymerase (or, the virtues of simplicity). Cell. Mol. Biol. Res. 39:385–391.

    PubMed  CAS  Google Scholar 

  • McCulloch, V., Seidel-Rogol, B. L., Shadel, G. S. 2002. A human mitochondrial transcription factor is related to RNA adenine methyltransferases and binds S-adenosylmethionine. Mol. Cell. Biol. 22:1116–1125.

    Article  PubMed  CAS  Google Scholar 

  • Meskauskiene, R., Würsch, M., Laloi, C., Vidi, P., Coll, N., Kessler, F., Baruah, A., Kim, C., Apel, K. 2009. A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses O-induced cell death. Plant J. 60:399–410.

    Article  PubMed  CAS  Google Scholar 

  • Monéger, F., Smart, C. J., Leaver, C. J. 1994. Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J. 13:8–17.

    PubMed  Google Scholar 

  • Muise, R. C., Hauswirth, W. W. 1992. Transcription in maize mitochondria: effects of tissue and mitochondrial genotype. Curr. Genet. 22:235–242.

    Article  PubMed  CAS  Google Scholar 

  • Mulligan, R. M., Lau, G. T., Walbot, V. 1988. Numerous transcription initiation sites exist for the maize mitochondrial genes for subunit 9 of the ATP synthase and subunit 3 of cytochrome oxidase. Proc. Natl. Acad. Sci. U.S.A 85:7998–8002.

    Article  PubMed  CAS  Google Scholar 

  • Mulligan, R. M., Leon, P., Walbot, V. 1991. Transcription and posttranscriptional regulation of maize mitochondrial gene expression. Mol. Cell. Biol. 11:533–543.

    PubMed  CAS  Google Scholar 

  • Nayak, D., Guo, Q., Sousa, R. 2009. A promoter recognition mechanism common to yeast mitochondrial and phage T7 RNA polymerases. J. Biol. Chem. 284:13641–13647.

    Article  PubMed  CAS  Google Scholar 

  • Newton, K. J., Winberg, B., Yamato, K., Lupold, S., Stern, D. B. 1995. Evidence for a novel mitochondrial promoter preceding the cox2 gene of perennial teosintes. EMBO J. 14:585–593.

    PubMed  CAS  Google Scholar 

  • Notsu, Y., Masood, S., Nishikawa, T., Kubo, N., Akiduki, G., Nakazono, M., Hirai, A., Kadowaki, K. 2002. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol. Genet. Genomics 268:434–445.

    Article  PubMed  CAS  Google Scholar 

  • Ogihara, Y., Yamazaki, Y., Murai, K., Kanno, A., Terachi, T., Shiina, T., Miyashita, N., Nasuda, S., Nakamura, C., Mori, N., Takumi, S., Murata, M., Futo, S., Tsunewaki, K. 2005. Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res. 33:6235–6250.

    Article  PubMed  CAS  Google Scholar 

  • Okada, S., Brennicke, A. 2006. Transcript levels in plant mitochondria show a tight homeostasis during day and night. Mol. Genet. Genomics 276:71–78.

    Article  PubMed  CAS  Google Scholar 

  • Parisi, M. A., Clayton, D. A. 1991a. Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252:965–969.

    Article  PubMed  CAS  Google Scholar 

  • Parisi, M. A., Xu, B., Clayton, D. A. 1993. A human mitochondrial transcriptional activator can functionally replace a yeast mitochondrial HMG-box protein both in vivo and in vitro. Mol. Cell. Biol. 13:1951–1961.

    PubMed  CAS  Google Scholar 

  • Park, A. K., Kim, H., Jin, H. J. 2009. Comprehensive phylogenetic analysis of evolutionarily conserved rRNA adenine dimethyltransferase suggests diverse bacterial contributions to the nucleus-encoded plastid proteome. Mol. Phylogenet. Evol. 50:282–289.

    Article  PubMed  CAS  Google Scholar 

  • Rantanen, A., Gaspari, M., Falkenberg, M., Gustafsson, C., M., Larsson, N.-G. 2003. Characterization of the mouse genes for mitochondrial transcription factors B1 and B2. Mamm. Genome 14:1–6.

    Article  PubMed  CAS  Google Scholar 

  • Rapp, W. D., Stern, D. B. 1992. A conserved 11 nucleotide sequence contains an essential ­promoter element of the maize mitochondrial atp1 gene. EMBO J. 11:1065–1073.

    PubMed  CAS  Google Scholar 

  • Rapp, W. D., Lupold, D. S., Mack, S., Stern, D. B. 1993. Architecture of the maize mitochondrial atp1 promoter as determined by linker-scanning and point mutagenesis. Mol. Cell. Biol. 13:7232–7238.

    PubMed  CAS  Google Scholar 

  • Richter, U., Kiessling, J., Hedtke, B., Decker, E., Reski, R., Börner, T., Weihe, A. 2002. Two RpoT genes of Physcomitrella patens encode phage-type RNA polymerases with dual targeting to mitochondria and plastids. Gene 290:95–105.

    Article  PubMed  CAS  Google Scholar 

  • Richter, U., Kühn, K., Okada, S., Brennicke, A., Weihe, A., Börner, T. 2009. A mitochondrial rRNA dimethyltransferase in Arabidopsis. Plant J. Published Online DOI: 10.1111/j.1365-313X.2009.04079.x.

    Google Scholar 

  • Roberti, M., Polosa, P. L., Bruni, F., Manzari, C., Deceglie, S., Gadaleta, M. N., Cantatore, P. 2009. The MTERF family proteins: mitochondrial transcription regulators and beyond. Biochim. Biophys. Acta 1787:303–311.

    Article  PubMed  CAS  Google Scholar 

  • Roberti, M., Polosa, P. L., Bruni, F., Musicco, C., Gadaleta, M. N., Cantatore, P. 2003. DmTTF, a novel mitochondrial transcription termination factor that recognises two sequences of Drosophila melanogaster mitochondrial DNA. Nucleic Acids Res. 31:1597–1604.

    Article  PubMed  CAS  Google Scholar 

  • Rohe, M., Schründer, J., Tudzynski, P., Meinhardt, F. 1992. Phylogenetic relationships of linear, protein-primed replicating genomes. Curr. Genet. 21:173–176.

    Article  PubMed  CAS  Google Scholar 

  • Scarpulla, R. C. 2008. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiological Reviews 88:611–638.

    Article  PubMed  CAS  Google Scholar 

  • Schinkel, A. H., Koerkamp, M. J., Touw, E. P., Tabak, H. F. 1987. Specificity factor of yeast mitochondrial RNA polymerase. Purification and interaction with core RNA polymerase. J. Biol. Chem. 262:12785–12791.

    PubMed  CAS  Google Scholar 

  • Schinkel, A. H., Groot Koerkamp, M. J., Teunissen, A. W., Tabak, H. F. 1988. RNA polymerase induces DNA bending at yeast mitochondrial promoters. Nucleic Acids Res. 16:9147–9163.

    Article  PubMed  CAS  Google Scholar 

  • Schmitz-Linneweber, C., Small, I. 2008. Pentatricopeptide repeat proteins: a socket set for ­organelle gene expression. Trends Plant Sci. 13:663–670.

    Article  PubMed  CAS  Google Scholar 

  • Schönfeld, C., Wobbe, L., Borgstadt, R., Kienast, A., Nixon, P. J., Kruse, O. 2004. The ­nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J. Biol. Chem. 279:50366–50374.

    Article  PubMed  CAS  Google Scholar 

  • Schubot, F. D., Chen, C. J., Rose, J. P., Dailey, T. A., Dailey, H. A., Wang, B. C. 2001. Crystal structure of the transcription factor sc-mtTFB offers insights into mitochondrial transcription. Protein Sci. 10:1980–1988.

    Article  PubMed  CAS  Google Scholar 

  • Shadel, G. S., Clayton, D. A. 1993. Mitochondrial Transcription. J. Biol. Chem. 268:16083–16086.

    PubMed  CAS  Google Scholar 

  • Shadel, G. S., Clayton, D. A. 1995. A Saccharomyces cerevisiae mitochondrial transcription ­factor, sc-mtTFB, shares features with sigma factors but is functionally distinct. Mol. Cell. Biol. 15:2101–2108.

    PubMed  CAS  Google Scholar 

  • Shutt, T., Gray, M. 2006. Homologs of mitochondrial transcription factor B, sparsely distributed within the eukaryotic radiation, are likely derived from the dimethyladenosine ­methyltransferase of the mitochondrial endosymbiont. Mol. Biol. Evol. 23:1169–1179.

    Article  PubMed  CAS  Google Scholar 

  • Smart, C. J., Moneger, F., Leaver, C. J. 1994. Cell-specific regulation of gene expression in ­mitochondria during anther development in sunflower. Plant Cell 6:811–825.

    PubMed  CAS  Google Scholar 

  • Sousa, R. 1996. Structural and mechanistic relationships between nucleic acid polymerases. Trends Biochem. Sci. 21:186–190.

    PubMed  CAS  Google Scholar 

  • Sousa, R., Chung, Y. J., Rose, J. P., Wang, B. C. 1993. Crystal structure of bacteriophage T7 RNA polymerase at 3.3 A resolution. Nature 364:593–599.

    Article  PubMed  CAS  Google Scholar 

  • Steitz, T. A. 2004. The structural basis of the transition from initiation to elongation phases of transcription, as well as translocation and strand separation, by T7 RNA polymerase. Curr. Opin. Struct. Biol. 14:4–9.

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama, Y., Watase, Y., Nagase, M., Makita, N., Yagura, S., Hirai, A., Sugiura, M. 2005. The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol. Genet. Genomics 272:603.

    Article  PubMed  CAS  Google Scholar 

  • Swiatecka-Hagenbruch, M., Emanuel, C., Hedtke, B., Liere, K., Börner, T. 2008. Impaired function of the phage-type RNA polymerase RpoTp in transcription of chloroplast genes is compensated by a second phage-type RNA polymerase. Nucleic Acids Res. 36:785–792.

    Article  PubMed  CAS  Google Scholar 

  • Timmis, J. N., Ayliffe, M. A., Huang, C. Y., Martin, W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5:123–135.

    Article  PubMed  CAS  Google Scholar 

  • Tiranti, V., Savoia, A., Forti, F., D’Apolito, M. F., Centra, M., Rocchi, M., Zeviani, M. 1997. Identification of the gene encoding the human mitochondrial RNA polymerase (h-mtRPOL) by cyberscreening of the Expressed Sequence Tags database. Hum. Mol. Genet. 6:615–625.

    Article  PubMed  CAS  Google Scholar 

  • Topping, J., Leaver, C. 1990. Mitochondrial gene expression during wheat leaf development. Planta 182:399–407.

    Article  CAS  Google Scholar 

  • Tracy, R. L., Stern, D. B. 1995. Mitochondrial transcription initiation: promoter structures and RNA polymerases. Curr. Genet. 28:205–216.

    Article  PubMed  CAS  Google Scholar 

  • Unseld, M., Marienfeld, J. R., Brandt, P., Brennicke, A. 1997. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat. Genet. 15:57–61.

    Article  PubMed  CAS  Google Scholar 

  • Weihe, A. 2004. The transcription of plant organelle genomes. In Molecular Biology and Biotechnology of Plant Organelles, H. Daniell and C. D. Chase eds., pp. 213–237. Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Weihe, A., Hedtke, B., Börner, T. 1997. Cloning and characterization of a cDNA encoding a bacteriophage-type RNA polymerase from the higher plant Chenopodium album. Nucleic Acids Res. 25:2319–2325.

    Article  PubMed  CAS  Google Scholar 

  • Woody, A. Y. M., Eaton, S. S., Osumi-Davis, P. A., Woody, R. W. 1996. Asp537 and Asp812 in bacteriophage T7 RNA polymerase as metal ion-binding sites studied by EPR, flow-dialysis, and transcription. Biochemistry 35:144–152.

    Article  PubMed  CAS  Google Scholar 

  • Xu, B., Clayton, D. A. 1992. Assignment of a yeast protein necessary for mitochondrial transcription initiation. Nucleic Acids Res. 20:1053–1059.

    Article  PubMed  CAS  Google Scholar 

  • Yin, C., Richter, U., Börner, T., Weihe, A. 2009. Evolution of phage-type RNA polymerases in higher plants: characterization of the single phage-type RNA polymerase gene from Selaginella moellendorffii. J. Mol. Evol. 68:528–538.

    Article  PubMed  CAS  Google Scholar 

  • Young, D. A., Allen, R. L., Harvey, A. J., Lonsdale, D. M. 1998. Characterization of a gene encoding a single-subunit bacteriophage-type RNA polymerase from maize which is alternatively spliced. Mol. Gen. Genet. 260:30–37.

    Article  PubMed  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. 50:710–722.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The work of the authors is supported by Deutsche Forschungsgemeinschaft (SFB 429). We thank Uwe Richter for helpful discussions and Kristina Kühn for providing initial artwork.

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Glossary

Alloplasmic:

Describes an individual having a common nucleus, but an “alien” cytoplasm (e.g., alloplasmic rye containing a wheat cytoplasm); may lead to meiotic disturbances and male sterility (CMS).

Bacterial-type RNA polymerase:

RNA polymerase found in bacteria. The core enzyme has 4 subunits. α: two α-subunits assemble the enzyme and bind regulatory factors. β: catalyzes the RNA synthesis. β′: binds to DNA (nonspecifically). To bind promoter-specific regions, the core enzyme requires the sigma factor (σ), which together form the holoenzyme. Related RNA polymerases are found in plastids (β′ is split into two subunits in the cyanobacterial and plastid enzymes) and mitochondria of Jakobids.

Bryophyte:

Nonvascular, seedless plants. Bryophytes are among the simplest of the terrestrial plants and comprise mosses, hornworts, or liverworts; e.g., Physcomitrella, Marchantia.

Cis-element:

Defines a region of DNA or RNA that regulates the expression of genes located on the same strand. Cis-elements are often binding sites of one or more trans-factors.

CMS:

Cytoplasmic male sterility (see Sect.18.1).

GFP:

Green fluorescent protein; exhibits bright green fluorescence when exposed to blue light and is frequently used as a reporter of expression.

HSP:

Heavy-strand promoter; part of the bidirectional promoter in mammalian mitochondria initiating transcription of the heavy-strand (in opposite the light-strand, defined by their differing G + T content).

LSP:

Light-strand promoter; promoter in mammalian mitochondria initiating transcription of the light-strand.

Lycophyte:

Plantae subdivision comprising the oldest living vascular plants at around 410 million years old, e.g., Selaginella.

NEP:

Nuclear-encoded plastid RNA polymerase; a phage-type RNA polymerase that originated by gene duplication from the gene encoding the mitochondrial RNA polymerase.

PPR protein:

Pentatricopeptide repeat protein (see Chap. 4).

Promoter:

A region of DNA that facilitates the transcription of a particular gene. In plant mitochondria, most promoters were defined by mapping transcript initiation sites and identification of consensus motifs. Therefore, promoters are often specified by the gene’s name and position of the initiating nucleotide in respect to the start of the coding sequence or mature rRNA.

Prophage:

Latent form of a bacteriophage inserted as part of the chromosome of a bacterium.

Tracheophyte Vascular plants:

those plants that have lignified tissues for conducting water, minerals, and photosynthetic products. Tracheophytes include lycophytes, ferns, and seed plants.

Trans-factors:

Mostly a protein factor that binds to specific DNA or RNA sequences (cis-elements) thereby controlling the regulation/expression of a certain gene.

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Liere, K., Börner, T. (2011). Transcription in Plant Mitochondria. In: Kempken, F. (eds) Plant Mitochondria. Advances in Plant Biology, vol 1. Springer, New York, NY. https://doi.org/10.1007/978-0-387-89781-3_4

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