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Co-Evolution of Mitochondrial tRNA Import and Codon Usage Determines Translational Efficiency in the Green Alga
Mitochondria from diverse phyla, including protozoa, fungi, higher plants, and humans, import tRNAs from the cytosol in order to ensure proper mitochondrial translation. Despite the broad occurrence of this process, our understanding of tRNA import mechanisms is fragmentary, and crucial questions about their regulation remain unanswered. In the unicellular green alga Chlamydomonas, a precise correlation was found between the mitochondrial codon usage and the nature and amount of imported tRNAs. This led to the hypothesis that tRNA import might be a dynamic process able to adapt to the mitochondrial genome content. By manipulating the Chlamydomonas mitochondrial genome, we introduced point mutations in order to modify its codon usage. We find that the codon usage modification results in reduced levels of mitochondrial translation as well as in subsequent decreased levels and activities of respiratory complexes. These effects are linked to the consequential limitations of the pool of tRNAs in mitochondria. This indicates that tRNA mitochondrial import cannot be rapidly regulated in response to a novel genetic context and thus does not appear to be a dynamic process. It rather suggests that the steady-state levels of imported tRNAs in mitochondria result from a co-evolutive adaptation between the tRNA import mechanism and the requirements of the mitochondrial translation machinery.
Vyšlo v časopise: Co-Evolution of Mitochondrial tRNA Import and Codon Usage Determines Translational Efficiency in the Green Alga. PLoS Genet 8(9): e32767. doi:10.1371/journal.pgen.1002946
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002946Souhrn
Mitochondria from diverse phyla, including protozoa, fungi, higher plants, and humans, import tRNAs from the cytosol in order to ensure proper mitochondrial translation. Despite the broad occurrence of this process, our understanding of tRNA import mechanisms is fragmentary, and crucial questions about their regulation remain unanswered. In the unicellular green alga Chlamydomonas, a precise correlation was found between the mitochondrial codon usage and the nature and amount of imported tRNAs. This led to the hypothesis that tRNA import might be a dynamic process able to adapt to the mitochondrial genome content. By manipulating the Chlamydomonas mitochondrial genome, we introduced point mutations in order to modify its codon usage. We find that the codon usage modification results in reduced levels of mitochondrial translation as well as in subsequent decreased levels and activities of respiratory complexes. These effects are linked to the consequential limitations of the pool of tRNAs in mitochondria. This indicates that tRNA mitochondrial import cannot be rapidly regulated in response to a novel genetic context and thus does not appear to be a dynamic process. It rather suggests that the steady-state levels of imported tRNAs in mitochondria result from a co-evolutive adaptation between the tRNA import mechanism and the requirements of the mitochondrial translation machinery.
Zdroje
1. Cavalier-SmithT (1987) Eukaryotes with no mitochondria. Nature 326 : 332–333.
2. LithgowT, SchneiderA (2010) Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond B Biol Sci 365 : 799–817.
3. O'BrienEA, ZhangY, YangL, WangE, MarieV, et al. (2006) GOBASE–a database of organelle and bacterial genome information. Nucleic Acids Res 34: D697–699.
4. KamenskiP, KolesnikovaO, JubenotV, EntelisN, KrasheninnikovIA, et al. (2007) Evidence for an adaptation mechanism of mitochondrial translation via tRNA import from the cytosol. Mol Cell 26 : 625–637.
5. RubioMA, RinehartJJ, KrettB, Duvezin-CaubetS, ReichertAS, et al. (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.
6. DuchêneAM, PujolC, Maréchal-DrouardL (2009) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 55 : 1–18.
7. SieberF, DuchêneAM, Maréchal-DrouardL (2011) Mitochondrial RNA import: from diversity of natural mechanisms to potential applications. Int Rev Cell Mol Biol 287 : 145–190.
8. SchneiderA (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 80 : 1033–1053.
9. SalinasT, DuchêneAM, Maréchal-DrouardL (2008) Recent advances in tRNA mitochondrial import. Trends Biochem Sci 33 : 320–329.
10. RubioMA, HopperAK (2011) Transfer RNA travels from the cytoplasm to organelles. Wiley Interdiscip Rev RNA 2 : 802–817.
11. KapushocST, AlfonzoJD, SimpsonL (2002) Differential localization of nucleus-encoded tRNAs between the cytosol and mitochondrion in Leishmania tarentolae. Rna 8 : 57–68.
12. SuyamaY, WongS, CampbellDA (1998) Regulated tRNA import in Leishmania mitochondria. Biochim Biophys Acta 1396 : 138–142.
13. TanTH, PachR, CrausazA, IvensA, SchneiderA (2002) tRNAs in Trypanosoma brucei: genomic organization, expression, and mitochondrial import. Mol Cell Biol 22 : 3707–3717.
14. SalinasT, SchaefferC, Maréchal-DrouardL, DuchêneAM (2005) Sequence dependence of tRNA(Gly) import into tobacco mitochondria. Biochimie 87 : 863–872.
15. GloverKE, SpencerDF, GrayMW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276 : 639–648.
16. Duchêne AM, El Farouk-Ameqrane S, Sieber F, Maréchal-Drouard L (2011) Import of RNAs into plant mitochondria; Kempken F, editor: Springer. 535 p.
17. IkemuraT (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2 : 13–34.
18. KanayaS, YamadaY, KudoY, IkemuraT (1999) Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238 : 143–155.
19. MichaelisG, VahrenholzC, PratjeE (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.
20. VinogradovaE, SalinasT, CognatV, RemacleC, Maréchal-DrouardL (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.
21. RemacleC, CardolP, CoosemansN, GaisneM, BonnefoyN (2006) High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc Natl Acad Sci U S A 103 : 4771–4776.
22. LarosaV, CoosemansN, MotteP, BonnefoyN, RemacleC (2012) Reconstruction of a human mitochondrial complex I mutation in the unicellular green alga Chlamydomonas. Plant J 70 : 759–768.
23. RemacleC, BaurainD, CardolP, MatagneRF (2001) Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I: characterization of two mutations affecting the nd1 coding sequence. Genetics 158 : 1051–1060.
24. CardolP, MatagneRF, RemacleC (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.
25. CardolP, BoutaffalaL, MemmiS, DevreeseB, MatagneRF, et al. (2008) In Chlamydomonas, the loss of ND5 subunit prevents the assembly of whole mitochondrial complex I and leads to the formation of a low abundant 700 kDa subcomplex. Biochim Biophys Acta 1777 : 388–396.
26. DubyF, MatagneRF (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.
27. QianW, YangJR, PearsonNM, MacleanC, ZhangJ (2012) Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet 8: e1002603 doi:10.1371/journal.pgen.1002603.
28. CognatV, DeragonJM, VinogradovaE, SalinasT, RemacleC, et al. (2008) On the evolution and expression of Chlamydomonas reinhardtii nucleus-encoded transfer RNA genes. Genetics 179 : 113–123.
29. GrosjeanH, de Crecy-LagardV, MarckC (2010) Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett 584 : 252–264.
30. RogalskiM, KarcherD, BockR (2008) Superwobbling facilitates translation with reduced tRNA sets. Nat Struct Mol Biol 15 : 192–198.
31. Brubacher-KauffmannS, Maréchal-DrouardL, CossetA, DietrichA, DuchêneAM (1999) Differential import of nucleus-encoded tRNAGly isoacceptors into Solanum tuberosum mitochondria. Nucleic Acids Res 27 : 2037–2042.
32. LeihneV, KirpekarF, VagboCB, van den BornE, KrokanHE, et al. (2011) Roles of Trm9 - and ALKBH8-like proteins in the formation of modified wobble uridines in Arabidopsis tRNA. Nucleic Acids Res 39 : 7688–7701.
33. Harris EH (1989) The Chlamydomonas Sourcebook. San Diego: Academic Press.
34. NewmanSM, BoyntonJE, GillhamNW, Randolph-AndersonBL, JohnsonAM, et al. (1990) Transformation of chloroplast ribosomal RNA genes in Chlamydomonas: molecular and genetic characterization of integration events. Genetics 126 : 875–888.
35. Randolph-AndersonBL, BoyntonJE, GillhamNW, HarrisEH, JohnsonAM, et al. (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.
36. BradfordMM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 : 248–254.
37. SchaggerH, von JagowG (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199 : 223–231.
38. LeaverCJ, HackE, FordeBG (1983) Protein synthesis by isolated plant mitochondria. Methods Enzymol 97 : 476–484.
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