Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Jan 29;358(1429):181–189. doi: 10.1098/rstb.2002.1179

Gene expression in plant mitochondria: transcriptional and post-transcriptional control.

Stefan Binder 1, Axel Brennicke 1
PMCID: PMC1693100  PMID: 12594926

Abstract

The informational content of the mitochondrial genome in plants is, although small, essential for each cell. Gene expression in these organelles involves a number of distinct transcriptional and post-transcriptional steps. The complex post-transcriptional processes of plant mitochondria such as 5' and 3' RNA processing, intron splicing, RNA editing and controlled RNA stability extensively modify individual steady-state RNA levels and influence the mRNA quantities available for translation. In this overview of the processes in mitochondrial gene expression, we focus on confirmed and potential sites of regulatory interference and discuss the evolutionary origins of the transcriptional and post-transcriptional processes.

Full Text

The Full Text of this article is available as a PDF (216.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blanc V., Litvak S., Araya A. RNA editing in wheat mitochondria proceeds by a deamination mechanism. FEBS Lett. 1995 Oct 2;373(1):56–60. doi: 10.1016/0014-5793(95)00991-h. [DOI] [PubMed] [Google Scholar]
  2. Bonen L., Vogel J. The ins and outs of group II introns. Trends Genet. 2001 Jun;17(6):322–331. doi: 10.1016/s0168-9525(01)02324-1. [DOI] [PubMed] [Google Scholar]
  3. Brennicke A., Zabaleta E., Dombrowski S., Hoffmann M., Binder S. Transcription signals of mitochondrial and nuclear genes for mitochondrial proteins in dicot plants. J Hered. 1999 May-Jun;90(3):345–350. doi: 10.1093/jhered/90.3.345. [DOI] [PubMed] [Google Scholar]
  4. Cui X., Wise R. P., Schnable P. S. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science. 1996 May 31;272(5266):1334–1336. doi: 10.1126/science.272.5266.1334. [DOI] [PubMed] [Google Scholar]
  5. Dombrowski S., Brennicke A., Binder S. 3'-Inverted repeats in plant mitochondrial mRNAs are processing signals rather than transcription terminators. EMBO J. 1997 Aug 15;16(16):5069–5076. doi: 10.1093/emboj/16.16.5069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Däschner K., Couée I., Binder S. The mitochondrial isovaleryl-coenzyme a dehydrogenase of arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiol. 2001 Jun;126(2):601–612. doi: 10.1104/pp.126.2.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Faivre-Nitschke S. E., Grienenberger J. M., Gualberto J. M. A prokaryotic-type cytidine deaminase from Arabidopsis thaliana gene expression and functional characterization. Eur J Biochem. 1999 Aug;263(3):896–903. doi: 10.1046/j.1432-1327.1999.00591.x. [DOI] [PubMed] [Google Scholar]
  8. Farré J. C., Leon G., Jordana X., Araya A. cis Recognition elements in plant mitochondrion RNA editing. Mol Cell Biol. 2001 Oct;21(20):6731–6737. doi: 10.1128/MCB.21.20.6731-6737.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Farré Jean-Claude, Araya Alejandro. RNA splicing in higher plant mitochondria: determination of functional elements in group II intron from a chimeric cox II gene in electroporated wheat mitochondria. Plant J. 2002 Jan;29(2):203–213. doi: 10.1046/j.1365-313x.2002.01207.x. [DOI] [PubMed] [Google Scholar]
  10. Forde B. G., Oliver R. J., Leaver C. J. Variation in mitochondrial translation products associated with male-sterile cytoplasms in maize. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3841–3845. doi: 10.1073/pnas.75.8.3841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gagliardi D., Kuhn J., Spadinger U., Brennicke A., Leaver C. J., Binder S. An RNA helicase (AtSUV3) is present in Arabidopsis thaliana mitochondria. FEBS Lett. 1999 Sep 24;458(3):337–342. doi: 10.1016/s0014-5793(99)01168-0. [DOI] [PubMed] [Google Scholar]
  12. Gagliardi D., Leaver C. J. Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J. 1999 Jul 1;18(13):3757–3766. doi: 10.1093/emboj/18.13.3757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Giegé P., Hoffmann M., Binder S., Brennicke A. RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep. 2000 Aug;1(2):164–170. doi: 10.1093/embo-reports/kvd024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gray M. W. Evolution of organellar genomes. Curr Opin Genet Dev. 1999 Dec;9(6):678–687. doi: 10.1016/s0959-437x(99)00030-1. [DOI] [PubMed] [Google Scholar]
  15. Gray M. W., Lang B. F. Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol. 1998 Jan;6(1):1–3. doi: 10.1016/S0966-842X(97)01182-7. [DOI] [PubMed] [Google Scholar]
  16. Grohmann L., Thieck O., Herz U., Schröder W., Brennicke A. Translation of nad9 mRNAs in mitochondria from Solanum tuberosum is restricted to completely edited transcripts. Nucleic Acids Res. 1994 Aug 25;22(16):3304–3311. doi: 10.1093/nar/22.16.3304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hedtke B., Börner T., Weihe A. One RNA polymerase serving two genomes. EMBO Rep. 2000 Nov;1(5):435–440. doi: 10.1093/embo-reports/kvd086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hirose T., Sugiura M. Involvement of a site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system. EMBO J. 2001 Mar 1;20(5):1144–1152. doi: 10.1093/emboj/20.5.1144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hoffmann Michaela, Binder Stefan. Functional importance of nucleotide identities within the pea atp9 mitochondrial promoter sequence. J Mol Biol. 2002 Jul 26;320(5):943–950. doi: 10.1016/s0022-2836(02)00552-1. [DOI] [PubMed] [Google Scholar]
  20. Ikeda T. M., Gray M. W. Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol Cell Biol. 1999 Dec;19(12):8113–8122. doi: 10.1128/mcb.19.12.8113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kuhn J., Tengler U., Binder S. Transcript lifetime is balanced between stabilizing stem-loop structures and degradation-promoting polyadenylation in plant mitochondria. Mol Cell Biol. 2001 Feb;21(3):731–742. doi: 10.1128/MCB.21.3.731-742.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kunzmann A., Brennicke A., Marchfelder A. 5' end maturation and RNA editing have to precede tRNA 3' processing in plant mitochondria. Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):108–113. doi: 10.1073/pnas.95.1.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lang B. F., Burger G., O'Kelly C. J., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Gray M. W. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature. 1997 May 29;387(6632):493–497. doi: 10.1038/387493a0. [DOI] [PubMed] [Google Scholar]
  24. Lang B. F., Gray M. W., Burger G. Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet. 1999;33:351–397. doi: 10.1146/annurev.genet.33.1.351. [DOI] [PubMed] [Google Scholar]
  25. Liu F., Cui X., Horner H. T., Weiner H., Schnable P. S. Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell. 2001 May;13(5):1063–1078. doi: 10.1105/tpc.13.5.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lohrmann J., Sweere U., Zabaleta E., Bäurle I., Keitel C., Kozma-Bognar L., Brennicke A., Schäfer E., Kudla J., Harter K. The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Mol Genet Genomics. 2001 Mar;265(1):2–13. doi: 10.1007/s004380000400. [DOI] [PubMed] [Google Scholar]
  27. Lupold D. S., Caoile A. G., Stern D. B. The maize mitochondrial cox2 gene has five promoters in two genomic regions, including a complex promoter consisting of seven overlapping units. J Biol Chem. 1999 Feb 5;274(6):3897–3903. doi: 10.1074/jbc.274.6.3897. [DOI] [PubMed] [Google Scholar]
  28. Malek O., Lättig K., Hiesel R., Brennicke A., Knoop V. RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J. 1996 Mar 15;15(6):1403–1411. [PMC free article] [PubMed] [Google Scholar]
  29. Maloney A. P., Traynor P. L., Levings C. S., 3rd, Walbot V. Identification in maize mitochondrial 26S rRNA of a short 5'-end sequence possibly involved in transcription initiation and processing. Curr Genet. 1989 Mar;15(3):207–212. doi: 10.1007/BF00435507. [DOI] [PubMed] [Google Scholar]
  30. Marchfelder A., Brennicke A., Binder S. RNA editing is required for efficient excision of tRNA(Phe) from precursors in plant mitochondria. J Biol Chem. 1996 Jan 26;271(4):1898–1903. doi: 10.1074/jbc.271.4.1898. [DOI] [PubMed] [Google Scholar]
  31. Marchfelder A., Schuster W., Brennicke A. In vitro processing of mitochondrial and plastid derived tRNA precursors in a plant mitochondrial extract. Nucleic Acids Res. 1990 Mar 25;18(6):1401–1406. doi: 10.1093/nar/18.6.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Maréchal-Drouard L., Kumar R., Remacle C., Small I. RNA editing of larch mitochondrial tRNA(His) precursors is a prerequisite for processing. Nucleic Acids Res. 1996 Aug 15;24(16):3229–3234. doi: 10.1093/nar/24.16.3229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. McCulloch Vicki, Seidel-Rogol Bonnie L., Shadel Gerald S. A human mitochondrial transcription factor is related to RNA adenine methyltransferases and binds S-adenosylmethionine. Mol Cell Biol. 2002 Feb;22(4):1116–1125. doi: 10.1128/MCB.22.4.1116-1125.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Monéger F., Smart C. J., Leaver C. J. Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J. 1994 Jan 1;13(1):8–17. doi: 10.1002/j.1460-2075.1994.tb06230.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ohtani Kouhei, Yamamoto Hiroyuki, Akimitsu Kazuya. Sensitivity to Alternaria alternata toxin in citrus because of altered mitochondrial RNA processing. Proc Natl Acad Sci U S A. 2002 Feb 12;99(4):2439–2444. doi: 10.1073/pnas.042448499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Phreaner C. G., Williams M. A., Mulligan R. M. Incomplete editing of rps12 transcripts results in the synthesis of polymorphic polypeptides in plant mitochondria. Plant Cell. 1996 Jan;8(1):107–117. doi: 10.1105/tpc.8.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pring D. R., Mullen J. A., Kempken F. Conserved sequence blocks 5' to start codons of plant mitochondrial genes. Plant Mol Biol. 1992 May;19(2):313–317. doi: 10.1007/BF00027353. [DOI] [PubMed] [Google Scholar]
  38. Race H. L., Herrmann R. G., Martin W. Why have organelles retained genomes? Trends Genet. 1999 Sep;15(9):364–370. doi: 10.1016/s0168-9525(99)01766-7. [DOI] [PubMed] [Google Scholar]
  39. Rajasekhar V. K., Mulligan R. M. RNA Editing in Plant Mitochondria: [alpha]-Phosphate Is Retained during C-to-U Conversion in mRNAs. Plant Cell. 1993 Dec;5(12):1843–1852. doi: 10.1105/tpc.5.12.1843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rapp W. D., Stern D. B. A conserved 11 nucleotide sequence contains an essential promoter element of the maize mitochondrial atp1 gene. EMBO J. 1992 Mar;11(3):1065–1073. doi: 10.1002/j.1460-2075.1992.tb05145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sarria R., Lyznik A., Vallejos C. E., Mackenzie S. A. A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell. 1998 Jul;10(7):1217–1228. doi: 10.1105/tpc.10.7.1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schiffer Steffen, Rösch Sylvia, Marchfelder Anita. Assigning a function to a conserved group of proteins: the tRNA 3'-processing enzymes. EMBO J. 2002 Jun 3;21(11):2769–2777. doi: 10.1093/emboj/21.11.2769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Schuster W., Brennicke A. Conserved sequence elements at putative processing sites in plant mitochondria. Curr Genet. 1989 Mar;15(3):187–192. doi: 10.1007/BF00435505. [DOI] [PubMed] [Google Scholar]
  44. Schuster W., Hiesel R., Isaac P. G., Leaver C. J., Brennicke A. Transcript termini of messenger RNAs in higher plant mitochondria. Nucleic Acids Res. 1986 Aug 11;14(15):5943–5954. doi: 10.1093/nar/14.15.5943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Singh M., Brown G. G. Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell. 1991 Dec;3(12):1349–1362. doi: 10.1105/tpc.3.12.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Small I. D., Peeters N. The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci. 2000 Feb;25(2):46–47. doi: 10.1016/s0968-0004(99)01520-0. [DOI] [PubMed] [Google Scholar]
  47. Unseld M., Marienfeld J. R., Brandt P., Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997 Jan;15(1):57–61. doi: 10.1038/ng0197-57. [DOI] [PubMed] [Google Scholar]
  48. Williams M. A., Tallakson W. A., Phreaner C. G., Mulligan R. M. Editing and translation of ribosomal protein S13 transcripts: unedited translation products are not detectable in maize mitochondria. Curr Genet. 1998 Sep;34(3):221–226. doi: 10.1007/s002940050390. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES