Summary
Genomic, transcriptomic and proteomic approaches have yielded considerable information, which impacted our understanding of the interactions between the nucleus and the mitochondria. Plant mitochondrial (mt) genomes are very large (220–2,000 kb) and often occur as complex pools of recombined molecules whose stoichiometry is tightly controlled by the nucleus. Unlike their mammalian and fungal counterparts, plant mt transcripts undergo complex post-transcriptional modifications such as editing and trans-splicing. Due to the impossibility to stably transform plant mitochondria and hence to manipulate mt gene expression, the genetic regulation of plant mt genomes has remained poorly understood. In this chapter, we will review the experimental data concerning the unicellular green alga Chlamydomonas reinhardtii, the only photosynthetic organism for which mt transformation has been achieved. Although Chlamydomonas harbors an extremely compact linear mt genome (15.8 kb) that differs from the one typically found in vascular plants, this system could bring novel insights on the role of the few subunits of the respiratory chain that are encoded in the mt genome. This is particularly relevant for the nd genes, which encode subunits of complex I since the yeast Saccharomyces cerevisiae, the other unicellular organism where mt transformation is performed nearly at will, is deprived of complex I. Moreover, because the Chlamydomonas mt genome only encodes three tRNAs, genetic manipulation of the organellar genome is a promising avenue to dissect the import of cytosolic tRNAs, a process that is now known to take place in plant and also human mitochondria. We also present alternative approaches such as the in vitro import of DNA or RNA and electroporation of isolated mitochondria followed by in organello synthesis that have been developed. These approaches have generated fruitful information about transcription and post-transcriptional processing of plant mt RNAs.
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Abbreviations
- mt:
-
Mitochondrial;
- tRNA:
-
Transfer RNA;
- VDAC:
-
Voltage-dependent anion channel
References
Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci USA 100:5968–5973
Adams CC, Stern DB (1990) Control of mRNA stability in chloroplasts by 3′ inverted repeats: effects of stem and loop mutations on degradation of psbA mRNA in vitro. Nucleic Acids Res 18:6003–6010
Alfonzo JD, Soll D (2009) Mitochondrial tRNA import – the challenge to understand has just begun. Biol Chem 390:717–722
Arnal N, Alban C, Quadrado M, Grandjean O, Mireau H (2006) The Arabidopsis Bio2 protein requires mitochondrial targeting for activity. Plant Mol Biol 62:471–479
Arrieta-Montiel MP, Shedge V, Davila J, Christensen AC, Mackenzie SA (2009) Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183:1261–1268
Backert S, Meißen K, Börner T (1997) Unique features of the mitochondrial rolling circle-plasmid mp1 from the higher plant Chenopodium album (L.). Nucleic Acid Res 25:582–589
Bedinger P, Walbot V (1986) DNA synthesis in purified maize mitochondria. Curr Genet 10:631–637
Bennoun P, Delosme M, Kuck U (1991) Mitochondrial genetics of Chlamydomonas reinhardtii: resistance mutations marking the cytochrome b gene. Genetics 127:335–343
Boer PH, Gray MW (1988) Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell 55:399–411
Bolle N, Kempken F (2006) Mono- and dicotyledonous plant-specific RNA editing sites are correctly edited in both in organello systems. FEBS Lett 580:4443–4448
Bolle N, Hinrichsen I, Kempken F (2007) Plastid mRNAs are neither spliced nor edited in maize and cauliflower mitochondrial in organello systems. RNA 13:2061–2065
Bonnefoy N, Remacle C, Fox TD (2007) Genetic transformation of Saccharomyces cerevisiae and Chlamydomonas reinhardtii mitochondria. Methods Cell Biol 80:525–548
Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW (1987) Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci USA 84:2391–2395
Bruhs A, Kempken F (2010) RNA editing in higher plant mitochondria. In: Kempken F (ed) Plant mitochondria. Springer, New York/Dordrecht/Heidelberg/London, pp 157–176
Cardol P, Matagne RF, Remacle C (2002) Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas. Implication for the structural organization of the enzyme. J Mol Biol 319:1211–1221
Carlson JE, Brown GL, Kemble RJ (1986) In organello mitochondrial DNA and RNA synthesis in fertile and cytoplasmic sterile Zea mays L. Curr Genet 11:151–160
Castandet B, Choury D, Bégu D, Jordana X, Araya A (2010) Intron RNA editing is essential for splicing in plant mitochondria. Nucleic Acids Res 38:7112–7121
Chaumont F, Bernier B, Buxant R, Williams ME, Levings CS III, Boutry M (1995) Targeting the maize T-urf13 product into tobacco mitochondria confers methomyl sensitivity to mitochondrial respiration. Proc Natl Acad Sci USA 92:1167–1171
Choury D, Farre JC, Jordana X, Araya A (2004) Different patterns in the recognition of editing sites in plant mitochondria. Nucleic Acids Res 32:6397–6406
Choury D, Farré JC, Jordana X, Araya A (2005) Gene expression studies in isolated mitochondria: Solanum tuberosum rps10 is recognized by cognate potato but not by the transcription, splicing and editing machinery of wheat mitochondria. Nucleic Acids Res 33:7058–7065
Colin M, Dorthu MP, Duby F, Remacle C, Dinant M, Wolwertz MR, Duyckaerts C, Sluse F, Matagne RF (1995) Mutations affecting the mitochondrial genes encoding the cytochrome oxidase subunit I and apocytochrome b of Chlamydomonas reinhardtii. Mol Gen Genet 249:179–184
Collombet J-M, Wheeler VC, Vogel F, Coutelle C (1997) Introduction of plasmid DNA into isolated mitochondria by electroporation. J Biol Chem 272:5342–5347
Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666
Cwerman-Thibault H, Sahel JA, Corral-Debrinski M (2010) Mitochondrial medicine: to a new era of gene therapy for mitochondrial DNA mutations. J Inherit Metab Dis 34:327–344
Delage L, Dietrich A, Cosset A, Maréchal-Drouard L (2003a) In vitro import of a nuclearly encoded tRNA into mitochondria of Solanum tuberosum. Mol Cell Biol 23:4000–4012
Delage L, Duchene AM, Zaepfel M, Maréchal-Drouard L (2003b) The anticodon and the D-domain sequences are essential determinants for plant cytosolic tRNA(Val) import into mitochondria. Plant J 34:623–633
Dietrich A, Maréchal-Drouard L, Carneiro V, Cosset A, Small I (1996) A single base change prevents import of cytosolic tRNA(Ala) into mitochondria in transgenic plants. Plant J 10:913–918
Dorthu MP, Remy S, Michel-Wolwertz MR, Colleaux L, Breyer D, Beckers MC, Englebert S, Duyckaerts C, Sluse FE, Matagne RF (1992) Biochemical, genetic and molecular characterization of new respiratory-deficient mutants in Chlamydomonas reinhardtii. Plant Mol Biol 18:759–772
Duby F, Matagne RF (1999) Alteration of dark respiration and reduction of phototrophic growth in a mitochondrial DNA deletion mutant of Chlamydomonas lacking cob, nd4, and the 3′ end of nd5. Plant Cell 11:115–125
Ehara T, Osafune T, Hase E (1995) Behavior of mitochondria in synchronized cells of Chlamydomonas reinhardtii (Chlorophyta). J Cell Sci 108(Pt 2):499–507
Esser AT, Smith KC, Gowrishankar TR, Vasilkoski Z, Weaver JC (2010) Mechanisms for the intracellular manipulation of organelles by conventional electroporation. Biophys J 98:2506–2514
Farré J-C, Araya A (2001) Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles. Nucleic Acids Res 29:2484–2491
Farré JC, Araya A (2002) 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 29:203–213
Farré JC, Leon G, Jordana X, Araya A (2001) cis recognition elements in plant mitochondrion RNA editing. Mol Cell Biol 21:6731–6737
Farré JC, Choury D, Araya A (2007) In organello gene expression and RNA editing studies by electroporation-mediated transformation of isolated plant mitochondria. Methods Enzymol 424:483–500
Fox TD, Sanford JC, McMullin TW (1988) Plasmids can stably transform yeast mitochondria lacking endogenous mtDNA. Proc Natl Acad Sci USA 85:7288–7292
Glab N, Wise RP, Pring DR, Jacq C, Slonimski P (1990) Expression in Saccharomyces cerevisiae of a gene associated with cytoplasmic male sterility from maize: respiratory dysfunction and uncoupling of yeast mitochondria. Mol Gen Genet 223:24–32
Glover KE, Spencer DF, Gray MW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276:639–648
Grewe F, Herres S, Viehöver P, Polsakiewicz M, Weisshaar B, Knoop V (2011) A unique transcriptome: 1782 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii. Nucleic Acids Res 39:2890–2902
Grohmann L (1995) In organello protein synthesis. Methods Mol Biol 49:391–397
Grohmann L, Thieck O, Herz U, Schröder W, Brennicke A (1994) Translation of nad9 mRNAs in mitochondria from Solanum tuberosum is restricted to completely edited transcripts. Nucleic Acids Res 22:3304–3311
Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341:660–662
Gutierres S, Sabar M, Lelandais C, Chetrit P, Diolez P, Degand H, Boutry M, Vedel F, de Kouchkovsky Y, De Paepe R (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 94:3436–3441
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
Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25:461–486
Havey MJ, Lilly JW, Bohanec B, Bartoszewski G, Malepszy S (2002) Cucumber: a model angiosperm for mitochondrial transformation? J Appl Genet 43:1–17
Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246:1632–1634
Hinrichsen I, Bolle N, Paun L, Kempken F (2009) RNA processing in plant mitochondria is independent of transcription. Plant Mol Biol 70:663–668
Hiramatsu T, Nakamura S, Misumi O, Kuroiwa T, Nakamura S (2006) Morphological changes in mitochondrial and chloroplast nucleoids and mitochondria during the Chlamydomonas reinhardtii (Chlorophyceae) cell cycle. J Phycol 42:1048–1058
Horn R, Kohler RH, Zetsche K (1991) A mitochondrial 16 kDa protein is associated with cytoplasmic male sterility in sunflower. Plant Mol Biol 17:29–36
Huang J, Lee SH, Lin C, Medici R, Hack E, Myers AM (1990) Expression in yeast of the T-urf13 protein from Texas male-sterile maize mitochondria confers sensitivity to methomyl and to Texas-cytoplasm-specific fungal toxins. EMBO J 9:339–347
Johnston SA, Anziano PQ, Shark K, Sanford JC, Butow RA (1988) Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240:1538–1541
Karpova OV, Newton KJ (1999) A partially assembled complex I in ND4-deficient mitochondria of maize. Plant J 17:511–521
Kempken F, Meinhardt F, Esser K (1989) In organello replication and viral affinity of linear, extrachromosomal DNA of the ascomycete Ascobolus immersus. Mol Gen Genet 218:523–530
Kempken F, Hermanns J, Osiewacz HD (1992) Evolution of linear plasmids. J Mol Evol 35:502–513
Kempken F, Bolle N, Forner J, Binder S (2007) Transcript end mapping and analysis of RNA editing in plant mitochondria. Methods Mol Biol 372:177–192
Kempken F, Bolle N, Bruhs A (2009) Higher plant in organello systems as a model for RNA editing. Endocyt Cell Res 19:1–10
Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139
Knoop V (2010) When you can’t trust the DNA: RNA editing changes transcript sequences. Cell Mol Life Sci 68:567–586
Koulintchenko M, Konstantinov Y, Dietrich A (2003) Plant mitochondria actively import DNA via the permeability transition pore complex. EMBO J 22:1245–1254
Koulintchenko M, Temperley RJ, Mason PA, Dietrich A, Lightowlers RN (2006) Natural competence of mammalian mitochondria allows the molecular investigation of mitochondrial gene expression. Hum Mol Genet 15:143–154
Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14
Kühn K, Weihe A, Börner T (2005) Multiple promoters are a common feature of mitochondrial genes in Arabidopsis. Nucleic Acids Res 33:337–346
Leon P, Walbot V, Bedinger P (1989) Molecular analysis of the linear 2.3 kb plasmid of maize mitochondria: apparent capture of tRNA genes. Nucleic Acids Res 17:4089–4099
Levings CS III, Siedow JN (1992) Molecular basis of disease susceptibility in the Texas cytoplasm of maize. Plant Mol Biol 19:135–147
Li C, Hu LN, Dong XJ, Sun CX, Mi Y (2008) High-intensity electric pulses induce mitochondria-dependent apoptosis in ovarian cancer xenograft mice. Int J Gynecol Cancer 18:1258–1261
Li L, Wang B, Liu Y, Qiu YL (2009) The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes. J Mol Evol 68:665–678
Lithgow T, Schneider A (2010) A Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond B Biol Sci 365:799–817
Mackenzie SA (2007) The unique biology of mitochondrial genome instability in plants. In: Logan DC (ed) Plant mitochondria. Blackwell Publishing, Singapore
Matagne RF, Michel-Wolwertz MR, Munaut C, Duyckaerts C, Sluse F (1989) Induction and characterization of mitochondrial DNA mutants in Chlamydomonas reinhardtii. J Cell Biol 108:1221–1226
McGregor A, Temperley R, Chrzanowska-Lightowlers ZM, Lightowlers RN (2001) Absence of expression from RNA internalised into electroporated mammalian mitochondria. Mol Genet Genomics 265:721–729
Meinhardt F, Kempken F, Kämper J, Esser K (1990) Linear plasmids among eukaryotes: fundamentals and application. Curr Genet 17:89–95
Moneger F, Smart CJ, Leaver CJ (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
Mulligan RM, Leon P, Calvin N, Walbot V (1989) Introduction of DNA into maize and rice mitochondria by electroporation. Maydica 34:207–216
Nishimura Y, Higashiyama T, Suzuki L, Misumi O, Kuroiwa T (1998) The biparental transmission of the mitochondrial genome in Chlamydomonas reinhardtii visualized in living cells. Eur J Cell Biol 77:124–133
O’Brien EA, Zhang Y, Wang E, Marie V, Badejoko W, Lang BF, Burger G (2009) GOBASE: an organelle genome database. Nucleic Acids Res 37:D946–D950
Patton DA, Schetter AL, Franzmann LH, Nelson K, Ward ER, Meinke DW (1998) An embryo-defective mutant of arabidopsis disrupted in the final step of biotin synthesis. Plant Physiol 116:935–946
Pineau B, Mathieu C, Gerard-Hirne C, De Paepe R, Chetrit P (2005) Targeting the NAD7 subunit to mitochondria restores a functional complex I and a wild type phenotype in the Nicotiana sylvestris CMS II mutant lacking nad7. J Biol Chem 280:25994–26001
Pla M, Mathieu C, De Paepe R, Chetrit P, Vedel F (1995) Deletion of the last two exons of the mitochondrial nad7 gene results in lack of the NAD7 polypeptide in a Nicotiana sylvestris CMS mutant. Mol Gen Genet 248:79–88
Rajasekhar VK, Mulligan RM (1993) RNA editing in plant mitochondria: α-phosphate is retained during C-to-U conversion in mRNAs. Plant Cell 5:1843–1852
Randolph-Anderson BL, Boynton JE, Gillham NW, Harris EH, Johnson AM, Dorthu MP, Matagne RF (1993) Further characterization of the respiratory deficient dum-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Mol Gen Genet 236:235–244
Rao AQ, Bakhsh A, Kiani S, Shahzad K, Shahid AA, Husnain T, Riazuddin S (2009) The myth of plant transformation. Biotechnol Adv 27:753–763
Remacle C, Matagne RF (1993) Transmission, recombination and conversion of mitochondrial markers in relation to the mobility of a group I intron in Chlamydomonas. Curr Genet 23:518–525
Remacle C, Bovie C, Michel-Wolwertz MR, Loppes R, Matagne RF (1990) Mitochondrial genome transmission in Chlamydomonas diploids obtained by sexual crosses and artificial fusions: role of the mating type and of a 1 kb intron. Mol Gen Genet 223:180–184
Remacle C, Baurain D, Cardol P, Matagne RF (2001a) Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I: characterization of two mutations affecting the nd1 coding sequence. Genetics 158:1051–1060
Remacle C, Duby F, Cardol P, Matagne RF (2001b) Mutations inactivating mitochondrial genes in Chlamydomonas reinhardtii. Biochem Soc Trans 29:442–446
Remacle C, Cardol P, Coosemans N, Gaisne M, Bonnefoy N (2006) High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc Natl Acad Sci USA 103:4771–4776
Remacle C, Cline S, Boutaffala L, Gabilly S, Larosa V, Barbieri RM, Coosemans N, Hamel PP (2009) The ARG9 gene encodes the plastid-resident N-acetyl ornithine aminotransferase in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 8:1460–1463
Rhoads DM, Levings CS III, Siedow JN (1995) URF13, a ligand-gated, pore-forming receptor for T-toxin in the inner membrane of cms-T mitochondria. J Bioenerg Biomembr 27:437–445
Salinas T, Schaeffer C, Maréchal-Drouard L, Duchene AM (2005) Sequence dependence of tRNA(Gly) import into tobacco mitochondria. Biochimie 87:863–872
Salinas T, Duchene AM, Delage L, Nilsson S, Glaser E, Zaepfel M, Maréchal-Drouard L (2006) The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. Proc Natl Acad Sci USA 103:18362–18367
Salinas T, Duchene AM, Maréchal-Drouard L (2008) Recent advances in tRNA mitochondrial import. Trends Biochem Sci 33:320–329
Shikanai T (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci 63:698–708
Small ID, Isaac PG, Leaver CJ (1987) Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J 6:865–869
Small I, Suffolk R, Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58:69–76
Soderholm J, Bevis BJ, Glick BS (2001) Vector for pop-in/pop-out gene replacement in Pichia pastoris. Biotechniques 31:306–310
Staudinger M, Kempken F (2003) Electroporation of isolated higher-plant mitochondria: transcripts of an introduced cox2 gene, but not an atp6 gene, are edited in organello. Mol Genet Genomics 269:553–561
Staudinger M, Kempken F (2004) In organello editing of mitochondrial atp9, cox2, and nad9 transcripts. Endocyt Cell Res 15:551–560
Steele DF, Butler CA, Fox TD (1996) Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc Natl Acad Sci USA 93:5253–5257
Takenaka M, Neuwirt J, Brennicke A (2004) Complex cis-elements determine an RNA editing site in pea mitochondria. Nucleic Acids Res 32:4137–4144
Takenaka M, Verbitskiy D, van der Merwe JA, Zehrmann A, Brennicke A (2008) The process of RNA editing in plant mitochondria. Mitochondrion 8:35–46
Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G (1993) Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet 24:241–247
Verbitskiy D, Zehrmann A, van der Merwe JA, Brennicke A, Takenaka M (2009) The PPR protein encoded by the LOVASTATIN INSENSITIVE 1 gene is involved in RNA editing at three sites in mitochondria of Arabidopsis thaliana. Plant J 61:446–455
Vinogradova E, Salinas T, Cognat V, Remacle C, Maréchal-Drouard L (2009) Steady-state levels of imported tRNAs in Chlamydomonas mitochondria are correlated with both cytosolic and mitochondrial codon usages. Nucleic Acids Res 37:1521–1528
von Allmen JM, Rottmann WH, Gengenbach BG, Harvey AJ, Lonsdale DM (1991) Transfer of methomyl and HmT-toxin sensitivity from T-cytoplasm maize to tobacco. Mol Gen Genet 229:405–412
Wang B, Xue J, Li L, Liu Y, Qiu YL (2009) The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts. Curr Genet 55:601–609
Ward BL, Anderson RS, Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25:793–803
Weber-Lotfi F, Ibrahim N, Boesch P, Cosset A, Konstantinov Y, Lightowlers RN, Dietrich A (2009) Developing a genetic approach to investigate the mechanism of mitochondrial competence for DNA import. Biochim Biophys Acta 1787:320–327
Wintz H, Dietrich A (1996) Electroporation of small RNAs into plant protoplasts: mitochondrial uptake of transfer RNAs. Biochem Biophys Res Commun 223:204–210
Yamasaki T, Kurokawa S, Watanabe KI, Ikuta K, Ohama T (2005) Shared molecular characteristics of successfully transformed mitochondrial genomes in Chlamydomonas reinhardtii. Plant Mol Biol 58:515–527
Yu W, Schuster W (1995) Evidence for a site-specific cytidine deamination reaction involved in C-to-U RNA editing of plant mitochondria. J Biol Chem 270:18227–18233
Zamzami N, Kroemer G (2001) The mitochondrion in apoptosis: how Pandora’s box opens. Nat Rev Mol Cell Biol 2:67–71
Zehrmann A, Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21:558–567
Acknowledgements
Work in the lab of C. Remacle is supported by ‘Fonds National de la Recherche Scientifique’ from Belgium (F.R.S.-FNRS) 1.5.255.08 and 2.4601.08 and by Action de Recherche Concertée ARC07/12 04 and a joint United Mitochondrial Disease Foundation Grant (UMDF) to C. Remacle and P. Hamel. T. Salinas is supported by the European Community’s Seventh Framework Programme (FP7/2007–2013) under grant agreement n° 220808 (Marie Curie Fellowship). V. Larosa is supported by ‘Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture’ (FRIA). Work in the lab of F. Kempken its supported by the German Research Foundation (DFG). N. Bonnefoy is the recipient of an ANR contract (JC-JC-06-0163). We warmly thank Dr R. Lamb (Ohio State University, OH) for careful reading of the manuscript.
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Remacle, C. et al. (2012). Transformation and Nucleic Acid Delivery to Mitochondria. In: Bock, R., Knoop, V. (eds) Genomics of Chloroplasts and Mitochondria. Advances in Photosynthesis and Respiration, vol 35. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2920-9_19
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