Biopolym. Cell. 2012; 28(4):261-266 .
http://dx.doi.org/10.7124/bc.000058
Reviews
Mitochondrial genetic transformation via biotechnological approaches or natural competence mechanism: do we have a choice?
1Koulintchenko M. V., 2Dietrich A., 1Konstantinov Yu. M.
  1. Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch of the Russian Academy of Sciences
    132, Lermontova Str., Irkutsk, Russian Federation, 664033
  2. CNRS Institute of Plant Molecular Biology, University of Strasbourg
    12, General Zimmer Str., Strasbourg, France, 67084

Abstract

Regardless quite assertive proofs of horizontal gene transfer into plant mitochondria, the phenomenon existent in many organisms, this field of research still lacks comprehensive information about the mechanism of gene transfer into mitochondria. Up to now, such questions as how nucleic acids traverse mitochondrial membranes and maintain stability in the mitochondrial genome remain the focus of such researches. Circular and especially linear plasmids present in mitochondria of many plant species could be a convinient tool to investigate the mechanisms of mitochondrial membrane DNA transfer and serve as mitochondrial integrative vectors.
Keywords: mitochondrial transformation, DNA import, mitochondrial plasmids, mitochondrial membrane
Full text: (PDF, in English)

References

[1] Fox T. D., Sanford J. C., McMullin T. W. Plasmids can stably transform yeast mitochondria lacking endogenous mtDNA Proc. Natl Acad. Sci. USA 1988 85, N 19:7288–7292.
[2] Johnston S. A., Anziano P. Q., Shark K., Sanford J. C., Butow R. A. Mitochondrial transformation in yeast by bombardment with microprojectiles Science 1988 240, N 4858:1538–1541.
[3] Randolf-Anderson B. L., Boynton J. E., Gillham N. W., Harris E. H., Johnson A. M., Dorthu M. P., Matagne R. F. Further characterization of the respiratory deficient dum-1 mutantation of Chlamydomonas reinhardtii and its use as recipient for mitochondrial transformation Mol. Gen. Genet 1993 236, N 2– 3:235–244.
[4] Remacle C., Cardol P., Coosemans N., Gaisne M., Bonnefoy N. High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes Proc. Natl Acad. Sci. USA 2006 103, N 12:4771–4776.
[5] King M. P., Attardi G. Injection of mitochondria into human cells leads to a rapid replacement of the endogenous mitochondrial DNA Cell 1988 52, N 6:811–819.
[6] King M. P., Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation Science 1989 246, N 4929:500–503.
[7] Pinkert C. A., Irwin M. H., Johnson L. W., Moffatt R. J. Mitochondria transfer into mouse ova by microinjection Transgenic Res 1997 6, N 6:379–383.
[8] Pinkert C. A., Trounce I. A. Production of transmitochondrial mice Methods 2002 26, N 4:348–357.
[9] Clark M. A., Shay J. W. Mitochondrial transformation of mammalian cells Nature 1982 295, N 5850:605–607.
[10] Katrangi E., D'Souza G., Boddapati S. V., Kulawiec M., Singh K. K., Bigger B., Weissig V. Xenogenic transfer of isolated murine mitochondria into human rho0 cells can improve respiratory function Rejuvenation Res 2007 10, N 4:561–570.
[11] D'Souza G. G., Rammohan R., Cheng S. M., Torchilin V. P., Weissig V. DQAsome-mediated delivery of plasmid DNA toward mitochondria in living cells J. Control Release 2003 92, N 1–2:189–197.
[12] D'Souza G. G., Boddapati S. V., Weissig V. Mitochondrial leader sequence-plasmid DNA conjugates delivered into mammalian cells by DQAsomes co-localize with mitochondria Mitochondrion 2005 5, N 5:352–358.
[13] Iyer S., Thomas R. R., Portell F. R., Dunham L. D., Quigley C. K., Bennett J. P. Jr. Recombinant mitochondrial transcription factor A with N-terminal mitochondrial transduction domain increases respiration and mitochondrial gene expression Mitochondrion 2009 9, N 3:196–203.
[14] Keeney P. M., Quigley C. K., Dunham L. D., Papageorge C. M., Iyer S., Thomas R. R., Schwarz K. M., Trimmer P. A., Khan S. M., Portell F. R., Bergquist K. E., Bennett J. P. Jr. Mitochondrial gene therapy augments mitochondrial physiology in a Parkinson's disease cell model Hum. Gene Ther 2009 20, N 8:897– 907.
[15] Khan S. M., Bennett J. P. Development of mitochondrial gene replacement therapy J. Bioenerg. Biomembr 2004 36, N 4:387–393.
[16] Seibel P., Trappe J., Villani G., Klopstock T., Papa S., Reichmann H. Transfection of mitochondria: strategy tomards a gene therapy of mitochondrial DNA diseases Nucleic Acids Res 1995 23, N 1:10–17.
[17] Vestweber D., Schatz G. DNA-protein conjugates can enter mitochondria via the protein import pathway Nature 1989 338, N 6211:170–172.
[18] Flierl A., Jackson C., Cottrell B., Murdock D., Seibel P., Wallace D. C. Targeted delivery of DNA to the mitochondrial compartment via import sequence-conjugated peptide nucleic acid Mol. Ther 2003 7, N 4:550–557.
[19] Collombet J. M., Wheeler V. C., Vogel F., Coutelle C. Introduction of plasmid DNA into isolated mitochondria by electroporation. A novel approach toward gene correction for mitochondrial desordes J. Biol. Chem 1997 272, N 8:5342–5347.
[20] Estevez A. M., Thiemann O. H., Alfonzo J. D., Simpson L. T7 RNA polymerase-driven transcription in mitochondria of Leishmania tarentolae and Trypanosoma brucei Mol. Biochem. Parasitol 1999 103, N 2:251–259.
[21] Farre J. C., Araya A. Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles Nucleic Acids Res 2001 29, N 12:2484–2491.
[22] Staudinger M., Kempken F. Electroporation of isolated higherplant mitochondria: transcripts of an introduced cox2 gene, but not an atp6 gene, are edited in organello Mol. Genet. Genomics 2003 269, N 4:553–561.
[23] Yoon Y. G., Koob M. D. Efficient cloning and engineering of entire mitochondrial genomes in Escherichia coli and transfer into transcriptionally active mitochondria Nucleic Acids Res 2003 31, N 5:1407–1415.
[24] Yoon Y. G., Koob M. D. Transformation of isolated mammalian mitochondria by bacterial conjugation Nucleic Acids Res 2005 33, N 16 e139.
[25] Koulintchenko M., Konstantinov Y., Dietrich A. Plant mitochondria actively import DNA via the permeability transition pore complex EMBO J 2003 22, N 6:1245–1254.
[26] Koulintchenko M., Temperley R. J., Mason P. A., Dietrich A., Lightowlers R. N. Natural competence of mammalian mitochondria allows the molecular investigation of mitochondrial gene expression Hum. Mol. Genet 2006 15, N 1:143–154.
[27] Weber-Lotfi F., Ibrahim N., Boesch P., Paulus F., Cosset A., Konstantinov Y., Lightowlers R. N., Dietrich A. Developing a genetic approach to investigate the mechanism of mitochondrial competence for DNA import Biochim. Biophys. Acta 2009 1787, N 5:320–327.
[28] Marechal-Drouard L., Weil J. H., Dietrich A. Transfer RNAs and transfer RNA genes in plants Annu. Rev. Plant Physiol. Plant Mol. Biol 1993 44:13–32.
[29] Tarassov I., Entelis N., Martin R. P. Mitochondrial import of a cytoplasmic lysine-tRNA in yeast is mediated by cooperation of cytoplasmic and mitochondrial lysyl-tRNA synthetases EMBO J 1995 14, N 14:3461–3471.
[30] Delage L., Dietrich A., Cosset A., Marechal-Drouard L. In vitro import of a nuclearly encoded tRNA into mitochondria of Solanum tuberosum Mol. Cell Biol 2003 23, N 11:4000–4012.
[31] Magalhaes P. J., Andreu A. L., Schon E. A. Evidence for the presence of 5S rRNA in mammalian mitochondria Mol. Biol. Cell 1998 9, N 9:2375–2382.
[32] Kolesnikova O. A., Entelis R. N., Jacquin-Becker C., Goltzene F., Chrzanowska-Lightowlers Z. M., Lightowlers R. N., Martin R. P., Tarassov I. Nuclear DNA-encoded tRNAs targeted into mitochondria can rescue a mitochondrial DNA mutation associated with the MERRF syndrome in cultured human cells Hum. Mol. Genet 2004 13, N 20:2519–2534.
[33] Thomas C. M. The nucleotide sequence and transcription of minicircular mitochondrial DNA's associated with fertile and cytoplasmic male-sterile lines of sugar beet Nucleic Acids Res 1986 14, N 23:9353–9370.
[34] Saumitou-Laprade P., Pannenbecker G., Maggouta F., Jean R., Michaelis G. A linear 10.4 kb plasmid in the mitochondria of Beta maritime Curr. Genet 1989 16, N 3:181–186.
[35] Backert S. Strand switching during rolling circle replication of plasmid-like DNA circles in the mitochondria of the higher plant Chenopodium album (L.) Plasmid 2000 43, N 2:166–170.
[36] Turpen T., Garger S. J., Marks M. D., Grill L. K. Molecular cloning and physical characterization of a Brassica linear mitochondrial plasmid Mol. Gen. Genet 1987 209, N 2:227–233.
[37] Handa H., Itani K., Sato H. Structural features and expression analysis of a linear mitochondrial plasmid in rapeseed (Brassica napus L.) Mol. Genet. Genomnics 2002 267, N 6:797–805.
[38] Robison M. M., Wolyn D. J. A mitochondrial plasmid and plasmid-like RNA and DNA polymerases encoded within the mitochondrial genome of carrot (Daucus carota L.) Curr. Genet 2005 47, N 1:57–66.
[39] Usupov T. U., Guzalova A. G., Ibragimov A. P. Discovery and characterization of plasmid-like DNA in cotton-plant Thesis of Seventh Symposium «Molecular mechanisms of genetic processes» of USSR (Moscow, 27–30 March, 1990) Moscow, 1990:187.
[40] Crouzillat D., Gentzbittel L., de la Canal L., Vaury C., Perrault A., Nicolas P., Ledoigt G. Properties and nucleotide sequence of a mitochondrial plasmid from sunflower Curr. Genet 1989 15, N 4:283–289.
[41] Goraczniak R. M., Augustyniak H. Characterization and sequence of lupin mitochondrial plasmid-like DNA Curr. Genet 1989 16, N 5–6:469–471.
[42] Esser K., Kuck V., Lemke P. A., Osiewaez H. D., Stahl P., Tudzynski U. Plasmids of eukaryotes. Fundamentals and applications Heidelberg: Springer, 1986 124 p.
[43] Shikanai T., Yang Z. Q., Yamada Y. Nucleotide sequence and molecular characterization of plasmid-like DNAs from mitochondria of cytoplasmic male-sterile rice Curr. Genet 1989 15, N 5:349–354.
[44] Benslimane A. A., Hartmann C., Ouenzar B., Rode A. Intramolecular recombination of a mitochondrial minicircular plasmid-like DNA of date-palm mediated by a set of short direct-repeat sequences Curr. Genet 1996 29, N 6:591–593.
[45] Pring D. R., Conde M. F., Schertz K. F., Levings C. S. Plasmidlike DNAs associated with mitochondria of cytoplasmic male-sterile Sorghum Mol. Gen. Genet 1982 186, N 2:180–184.
[46] Chase C. D., Pring D. R. Properties of the linear N1 and N2 plasmid-like DNAs from mitochondria of cytoplasmic male-sterile Sorghum bicolor Plant Mol. Biol 1986 6, N 1:53–64.
[47] Nikiforova I., Negruk V. Comparative electrophoretical analysis of plasmid-like mitochondrial DNAs in Vicia faba and some other legumes Planta 1983 157, N 1:81–84.
[48] Paillard A., Sederoff R. R., Levings C. S. Nucleotide sequence of the S-1 mitochondrial DNA from the cytoplasm of maize EMBO J 1985 4, N 5:1125–1128.
[49] Weissinger A. K., Timothy D. H., Levings C. S., Hu W. W., Goodman, M. M. Unique plasmid-like mitochondrial DNAs from indigenous maize races of Latin America Proc. Natl Acad. Sci. USA 1982 79, N 1:1–5.
[50] Houchins J. P., Ginsburg H., Rohrbaugh M., Dale, R. M. K., Schardl C. L., Hodge T. P., Lonsdale D. M. DNA sequence analysis of a 5.27-kb direct repeat occurring adjacent to the regions of S-episome homology in maize mitochondria EMBO J 1986 5, N 11:2781–2788.
[51] O'Brien C., Zabala G., Walbot V. Integrated R2 sequence in mitochondria of fertile B37N maize encodes and expresses a 130 kDa polypeptide similar to that encoded by the S2 episome of S-type male sterile plants Nucleic Acids Res 1989 17, N 1:405–422.
[52] Kemble R. J., Gunn R. E., Flavell R. B. Classification of normal and male-sterile cytoplasm in maize. II. Electrophoretic analysis of DNA species in mitochondria Genetics 1980 95, N 2:451–458.
[53] Bedinger P., de Hostos E. L., Leon P., Walbot V. Cloning and characterization of a linear 2,3 kb mitochondrial plasmid of maize Mol. Gen. Genet 1986 205, N 2:206–212.
[54] Leon P., Walbot V., Bedinger P. Molecular analysis of the linear 2,3 kb plasmide of maize mitochondria: apparent capture of tRNA genes Nucleic Acids Res 1989 17, N 11:4089–4099.
[55] Smith A. G., Chourey P. S., Pring D. R. Replication and amplification of the small mitochondrial DNAs in a cell suspension of Black Mexican Sweet maize Plant Mol. Biol 1987 10, N 2:83–90.
[56] Timothy D., Levings C. S., Hu W. W. L., Goodman M. M. Plasmid-like mitochondrial DNAs in diploperenial teosinte Maydica 1983 28, N 2:139–149.
[57] Grace K. S., Allen J. O., Newton K. J. R-type plasmids in mitochondria from a single source of Zea luxerians teosinte Curr. Genet 1994 25, N 3:258–264.
[58] Konstantinov Yu. M., Podsosonny V. A., Lutsenko G. N. DNA synthesis in intact maize mitochondria treated by pBR bacterial vector plasmids Biopolym. Cell 1989 5, N 4:98–102.
[59] Konstantinov Yu. M., Podsosonny V. A., Lutsenko G. N. Rivkin M. I. Translocation of bacterial vector plasmids into intact corn shoot mitochondria Biochemistry (Russian) 1989 54, N 1:154–158.
[60] Mileshina D., Koulintchenko M., Konstantinov Y., Dietrich A. Transfection of plant mitochondria and in organello gene integration Nucleic Acids Res 2011 39, N 17 e115.
[61] Boesch P., Ibrahim N., Paulus F., Cosset A., Tarasenko V., Dietrich A. Plant mitochondria possess a short-patch base excision DNA repair pathway Nucleic Acids Res 2009 37, N 17:5690–5700.
[62] Boesch P., Ibrahim N., Dietrich A., Lightowlers R. N. Membrane association of mitochondrial DNA facilitates base excision repair in mammalian mitochondria Nucleic Acids Res 2010 38, N 5:1478–1488.
[63] Weber-Lotfi F., Ibrahim N., Boesch P., Cosset A., Konstantinov Y., Lightowlers R. N., Dietrich A. Developing a genetic approach to investigate the mechanism of mitochondrial competence for DNA import Biochim. Biophys. Acta 2009 1787, N 5:320–327.
[64] Inrahim N., Handa H., Cosset A., Koulintchenko M., Konstantinov Y., Lightowlers R. N., Dietrich A., Weber-Lotfi F. DNA delivery to mitochondria: sequence specificity and energy enhancement Pharm. Res 2011 28, N 11:2871–2882.