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Import of RNAs into Plant Mitochondria

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Plant Mitochondria

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

Abstract

The plant mitochondrial genetic system has to provide about 35 ­polypeptides, which are essential for cell survival as they are components of the respiratory chain or contribute to its biogenesis. Thus, an active mitochondrial translation system is an absolute requisite. With the exception of a few ribosomal proteins, all protein factors involved in plant mitochondrial translation are nuclear-encoded and imported via the classical protein import channel. At the RNA level, the three ribosomal RNAs are encoded by the mitochondrial genome. In contrast, the transfer RNA (tRNA) population encoded by the plant mitochondrial genome is not sufficient to decode the 61 sense codons of the universal genetic code used by plant mitochondria. It is now well established that to compensate for the lack of tRNAs, several nuclear-encoded tRNAs used by the cytosolic translation machi-nery are also found in the mitochondrion. In this review, evolutionary aspects and functions of imported tRNAs are presented. Then, the basic questions on the tRNA mitochondrial import selectivity, regulation, targeting, and translocation in plants are discussed and compared to what has been discovered in tRNA mitochondrial import in evolutionary divergent organisms.

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Abbreviations

aaRS:

Aminoacyl-tRNA synthetase

cp-like:

Chloroplast-like

eEF1a:

Elongation factor 1A

RIC:

RNA import complex

TOM :

Translocase of the outer mitochondrial membrane

VDAC :

Voltage-dependent anion channel

References

  • Akashi, K., Sakurai, K., Hirayama, J., Fukuzama, H., Ohyama, K. 1996. Occurence of nuclear-encoded tRNAIle in mitochondria of the liverwort Marchantia polymorpha. Curr. Genet. 30:181–185.

    Article  PubMed  CAS  Google Scholar 

  • Akashi, K., Takenaka, M., Yamaoka, S., Suyama, Y., Fukuzawa, H., Ohyama, K. 1998. Coexistence of nuclear DNA-encoded tRNAVal(AAC) and mitochondrial DNA-encoded tRNAVal(UAC) in mitochondria of a liverwort Marchantia polymorpha. Nucleic Acids Res. 26:2168–2172.

    Article  PubMed  CAS  Google Scholar 

  • Alfonzo, J. D., Söll, D. 2009. Mitochondrial tRNA import-the challenge to understand has just begun. Biol. Chem. 390:717–722.

    Article  PubMed  CAS  Google Scholar 

  • Boer, P. H., Gray, M. W. 1988. Transfer RNA genes and the genetic code in Chlamydomonas reinhardtii mitochondria. Curr. Genet. 14:583–590.

    Article  PubMed  CAS  Google Scholar 

  • Bouzaidi-Tiali, N., Aeby, E., Charriere, F., Pusnik, M., Schneider, A. 2007. Elongation factor 1a mediates the specificity of mitochondrial tRNA import in T. brucei. EMBO. J. 26:4302–4312.

    Article  PubMed  CAS  Google Scholar 

  • Brubacher-Kauffmann, S., Maréchal-Drouard, L., Cosset, A., Dietrich, A., Duchêne, A. M. 1999. Differential import of nuclear-encoded tRNAGly isoacceptors into solanum Tuberosum ­mitochondria. Nucleic Acids Res. 27:2037–2042.

    Article  PubMed  CAS  Google Scholar 

  • Burger, G., Saint-Louis, D., Gray, M. W., Lang, B. F. 1999. Complete sequence of the ­mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell. 11:1675–1694.

    PubMed  CAS  Google Scholar 

  • Chacinska, A., Koehler, C. M., Milenkovic, D., Lithgow, T., Pfanner, N. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–644.

    Article  PubMed  CAS  Google Scholar 

  • Chen, H. C., Viry-Moussaid, M., Dietrich, A., Wintz, H. 1997. Evolution of a mitochondrial tRNA PHE gene in A. thaliana: import of cytosolic tRNA PHE into mitochondria. Biochem. Biophys. Res. Commun. 237:432–437.

    Article  PubMed  CAS  Google Scholar 

  • Clifton, S. W., Minx, P., Fauron, C. M., 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Delage, L., Duchêne, A. M., 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Duchêne, A. M., Maréchal-Drouard, L. 2001. The chloroplast-derived trnW and trnM-e genes are not expressed in Arabidopsis mitochondria. Biochem. Biophys. Res. Comm. 285:1213–1216.

    Article  PubMed  Google Scholar 

  • Duchêne, A. M., Peeters, N., Dietrich, A., Cosset, A., Small, I. D., Wintz, H. 2001. Overlapping destinations for two dual targeted glycyl-tRNA synthetases in Arabidopsis thaliana and Phaseolus vulgaris. J. Biol. Chem. 276:15275–15283.

    Article  PubMed  Google Scholar 

  • Duchêne, A. M., Giritch, A., Hoffmann, B., Cognat, V., Lancelin, D., Peeters, N. M., Zaepfel, M., Maréchal-Drouard, L., Small, I. D. 2005. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 102:16484–16489.

    Article  PubMed  Google Scholar 

  • Duchêne, A. M., Pujol, C., Maréchal-Drouard, L. 2009. Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr. Genet. 55:1–18.

    Article  PubMed  Google Scholar 

  • Entelis, N. S., Kolesnikova, O. A., Dogan, S., Martin, R. P., Tarassov, I. A. 2001. 5 S rRNA and tRNA import into human mitochondria. Comparison of in vitro requirements. J. Biol. Chem. 276:45642–45653.

    Article  PubMed  CAS  Google Scholar 

  • Entelis, N., Brandina, I., Kamenski, P., Krasheninnikov, I. A., Martin, R. P., Tarassov, I. 2006.A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev. 20:1609–1620.

    Article  PubMed  CAS  Google Scholar 

  • Fey, J., Dietrich, A., Cosset, A., Desprez, T., Maréchal-Drouard, L. 1997. Evolutionary aspects of “chloroplast-like” trnN and trnH expression in higher-plant mitochondria. Curr. Genet. 32:358–360.

    Article  PubMed  CAS  Google Scholar 

  • Frechin, M., Senger, B., Braye, M., Kern, D., Martin, R. P., Becker, H. D. 2009. Yeast mitochondrial Gln-tRNA(Gln) is generated by a GatFAB-mediated transamidation pathway involving Arc1p-controlled subcellular sorting of cytosolic GluRS. Genes Dev. 23:1119–1130.

    Article  PubMed  CAS  Google Scholar 

  • Glover, K. E., Spencer, D. F., Gray, M. W. 2001. Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J. Biol. Chem. 276:639–648.

    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 

  • Kamenski, P., Kolesnikova, O., Jubenot, V., Entelis, N., Krasheninnikov, I. A., Martin, R. P., Tarassov, I. 2007. Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol. Mol. Cell. 26:625–637.

    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 tRNA(Cys)(GCA). Nucleic Acids Res. 28:2571–2576.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, R., Maréchal-Drouard, L., Akama, K., Small, I. 1996. Striking differences in ­mitochondrial tRNA import between different plant species. Mol. Gen. Genet. 252:404–411.

    Article  PubMed  CAS  Google Scholar 

  • Leblanc, C., Boyen, C., Richard, O., Bonnard, G., Grienenberger, J. M., Kloareg, B. 1995. Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization. J. Mol. Biol. 250:484–495.

    Article  PubMed  CAS  Google Scholar 

  • Maréchal-Drouard, L., Weil, J. H., Guillemaut, P. 1988. Import of several tRNAs from the cytoplasm into the mitochondria in bean Phaseolus vulgaris. Nucleic Acids Res. 16:4777–4788.

    Article  PubMed  Google Scholar 

  • Maréchal-Drouard, L., Guillemaut, P., Cosset, A., Arbogast, M., Weber, F., Weil, J. H., Dietrich, A. 1990. Transfer RNAs of potato (Solanum tuberosum) mitochondria have different genetic origins. Nucleic Acids Res. 18:3689–3696.

    Article  PubMed  Google Scholar 

  • Marienfeld, J., Unseld, M., Brennicke, A. 1999. The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci. 4:495–502.

    Article  PubMed  Google Scholar 

  • Maul, J. E., Lilly, J. W., Cui, L., dePamphilis, C. W., Miller, W., Harris, E. H., Stern, D. B. 2002. The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659–2679.

    Article  PubMed  CAS  Google Scholar 

  • Michaelis, G., Vahrenholtz, C., Pratje, E. 1990. Mitochondrial DNA of Chlamydomonas ­reinhardtii: the gene for apocytochrome b and the complete functional map of the 15.8 kb DNA. Mol. Gen. Genet. 223:211–216.

    PubMed  CAS  Google Scholar 

  • Mireau, H., Cosset, A., Maréchal-Drouard, L., Fox, T. D., Small, I. D., Dietrich, A. 2000. Expression of Arabidopsis thaliana mitochondrial alanyl-tRNA synthetase is not sufficient to trigger mitochondrial import of tRNAAla in yeast. J. Biol. Chem. 275:13291–13296.

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee, S., Basu, S., Home, P., Dhar, G., Adhya, S. 2007. Necessary and sufficient factors for the import of transfer RNA into the kinetoplast mitochondrion. EMBO Rep. 8:589–595.

    Article  PubMed  CAS  Google Scholar 

  • Nagao, A., Suzuki, T., Katoh, T., Sakaguchi, Y. 2009. Biogenesis of glutaminyl-mt tRNAGln in human mitochondria. Proc. Natl. Acad. Sci. U.S.A. 106:16209–16214.

    Article  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 

  • Oda, K., Yamato, K., Ohta, E., Nakamura, Y., Takemura, M., Nozato, N., Akashi, K., Kanegae, T., Ogura, Y., Kohchi, T., et al. 1992a. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant ­mitochondrial genome. J. Mol. Biol. 223:1–7.

    Article  PubMed  CAS  Google Scholar 

  • Oda, K., Yamato, K., Ohta, E., Nakamura, Y., Takemura, M., Nozato, N., Akashi, K., Ohyama, K. 1992b. Transfer RNA genes in the mitochondrial genome from a liverwort, Marchantia ­polymorpha: the absence of chloroplast-like tRNAs. Nucleic Acids Res. 20:3773–3777.

    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 

  • Paris, Z., Rubio, M. A., Lukes, J., Alfonzo, J. D. 2009. Mitochondrial tRNA import in Trypanosoma brucei is independent of thiolation and the Rieske protein. RNA 15:1398–1406.

    Article  PubMed  CAS  Google Scholar 

  • Pfitzinger, H., Guillemaut, P., Weil, J. H., Pillay, D. T. N. 1987. Adjustment of the tRNA ­population to the codon usage in chloroplasts. Nucleic Acids Res. 15:1377–1386.

    Article  PubMed  CAS  Google Scholar 

  • Pusnik, M., Charriere, F., Maser, P., Waller, R. F., Dagley, M. J., Lithgow, T., Schneider, A. 2009. The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Mol. Biol. Evol. 26:671–680.

    Article  PubMed  CAS  Google Scholar 

  • Rinehart, J., Krett, B., Rubio, M. A., Alfonzo, J. D., Söll, D. 2005. Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev. 19:583–592.

    Article  PubMed  CAS  Google Scholar 

  • Robbens, S., Derelle, E., Ferraz, C., Wuyts, J., Moreau, H., Van de Peer, Y. 2007. The complete chloroplast and mitochondrial DNA sequence of Ostreococcus tauri: organelle genomes of the smallest eukaryote are examples of compaction. Mol. Biol. Evol. 24:956–968.

    Article  PubMed  CAS  Google Scholar 

  • Rubio, M. A., Rinehart, J. J., Krett, B., Duvezin-Caubet, S., Reichert, A. S., Söll, D., Alfonzo, J. D. 2008. Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import. Proc. Natl. Acad. Sci. U.S.A. 105:9186–9191.

    Article  PubMed  CAS  Google Scholar 

  • Salinas, T., Schaeffer, C., Maréchal-Drouard, L., Duchêne, A. M. 2005. Sequence dependence of tRNA(Gly) import into tobacco mitochondria. Biochimie. 87:863–872.

    Article  PubMed  CAS  Google Scholar 

  • Salinas, T., Duchêne, A. M., 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. U.S.A. 103:18362–18367.

    Article  PubMed  CAS  Google Scholar 

  • Salinas, T., Duchêne, A. M., Maréchal-Drouard, L. 2008. Recent advances in tRNA mitochondrial import. Trends Biochem. Sci. 33:320–329.

    Article  PubMed  CAS  Google Scholar 

  • Schneider, A., Maréchal-Drouard, L. 2000. Mitochondrial tRNA import: are there distinct mechanisms? Trends Cell Biol. 10:509–513.

    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 272:603–615.

    Article  PubMed  CAS  Google Scholar 

  • Tarassov, I., Entelis, N., Martin, R. P. 1995. An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA. J. Mol. Biol. 245:315–323.

    Article  PubMed  CAS  Google Scholar 

  • Terasawa, K., Odahara, M., Kabeya, Y., Kikugawa, T., Sekine, Y., Fujiwara, M., Sato, N. 2007. The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol. Biol. Evol. 24:699–709.

    Article  PubMed  CAS  Google Scholar 

  • Turmel, M., Otis, C., Lemieux, C. 2002. The complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants. Mol. Biol. Evol. 19:24–38.

    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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Weber, F., Dietrich, A., Weil, J. H., Maréchal-Drouard, L. 1990. A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucleic Acids Res. 18:5027–5030.

    Article  PubMed  CAS  Google Scholar 

  • Wolfe, K. H., Morden, C. W., Palmer, J. D. 1992. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl. Acad. Sci. U.S.A. 89:10648–10652.

    Article  PubMed  CAS  Google Scholar 

  • Wolff, G., Plante, I., Lang, B. F., Kuck, U., Burger, G. 1994. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. Gene content and genome organization. J. Mol. Biol. 237:75–86.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Laurence Maréchal-Drouard .

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Glossary

Aminoacyl-tRNA synthetase:

enzyme that catalyzes the amino acid attachment at the 3′ extremity of a tRNA molecule.

Angiosperm:

the flowering plants.

Bryophyte:

embryophytes (often called “land plants”) that are nonvascular. They neither have flowers nor produce seeds and reproduce via spores.

Cytochromec:

a small heme (an iron atom contained in a large heterocyclic ring called porphyrin) protein associated with the inner mitochondrial membrane that is an essential component for the electron transport chain.

D-arm:

in the secondary structure of a “classical” tRNA molecule, the D-arm is usually a 4 bp stem ending in a loop that often contains dihydrouridine.

Enolase:

a metalloenzyme of the glycolysis that converts the 2-phosphoglycerate to phosphoenolpyruvate.

Gymnosperm:

a group of spermatophyte seed-bearing plants with ovules on scales of a cone or similar structure.

Lysidine:

a derivative of cytidine in which the carbonyl is replaced by the amino acid lysine. Lysidine typically occurs in the anticodon of a tRNA molecule.

Oxidative phosphorylation:

in mitochondria, a metabolic pathway that uses energy released by the oxidation of NADH and succinate to produce ATP.

Selenocysteine:

an amino acid. It has a structure similar to cysteine, but with an atom of selenium taking the place of the sulfur. Often abbreviated Sec.

Translocase of the outer mitochondrial membrane:

a protein complex located in the outer mitochondrial membrane of mitochondria and involved in the translocation of nuclear-encoded proteins from the cytosol to the inter membrane space of mitochondria.

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Duchêne, AM., El Farouk-Ameqrane, S., Sieber, F., Maréchal-Drouard, L. (2011). Import of RNAs into 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_10

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