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Volume 164, Issue 3

The fission yeast Mtf2 is required for mitochondrial gene expression Free

Abstract

Mitochondrial gene expression is essential for adenosine triphosphate synthesis via oxidative phosphorylation, which is the universal energy currency of cells. Here, we report the identification and characterization of a homologue of Mtf2 (also called Nam1) in . The Δ mutant with the intron-containing mitochondrial DNA (mtDNA) exhibited impaired growth on a rich medium containing the non-fermentable carbon source glycerol, suggesting that is involved in mitochondrial function. deletion in a mitochondrial intron-containing background resulted in a barely detectable level of the mRNA and a reduction in the level of the mRNA, and severely impaired translation. In contrast, deletion in a mitochondrial intron-less background did not affect the levels of and mRNAs. However, Cox1 synthesis could not be restored to the control level in the Δ mutant with intron-less mtDNA. Our results suggest that unlike its counterpart in which plays a general role in synthesis of mtDNA-encoded proteins, Mtf2 primarily functions in translation and the effect of deletion on splicing of introns in mtDNA is likely due to a deficiency in the synthesis of intron-encoded maturases.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): mitochondrial translation , Mtf2 , respiratory deficiency and Schizosaccharomyces pombe
© 2018 The Authors
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2018-03-01
2024-04-23
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References

  1. Kauppila TES, Kauppila JHK, Larsson NG. Mammalian mitochondria and aging: an update. Cell Metab 2017; 25:57–71 [View Article][PubMed]
     [Google Scholar]
  2. Vakifahmetoglu-Norberg H, Ouchida AT, Norberg E. The role of mitochondria in metabolism and cell death. Biochem Biophys Res Commun 2017; 482:426–431 [View Article][PubMed]
     [Google Scholar]
  3. Forsburg SL. The best yeast?. Trends Genet 1999; 15:340–344 [View Article][PubMed]
     [Google Scholar]
  4. Schäfer B. RNA maturation in mitochondria of S. cerevisiae and S. pombe . Gene 2005; 354:80–85 [View Article][PubMed]
     [Google Scholar]
  5. Schäfer B, Hansen M, Lang BF. Transcription and RNA-processing in fission yeast mitochondria. RNA 2005; 11:785–795 [View Article][PubMed]
     [Google Scholar]
  6. Bendich AJ. The end of the circle for yeast mitochondrial DNA. Mol Cell 2010; 39:831–832 [View Article][PubMed]
     [Google Scholar]
  7. Gerhold JM, Aun A, Sedman T, Jõers P, Sedman J. Strand invasion structures in the inverted repeat of Candida albicans mitochondrial DNA reveal a role for homologous recombination in replication. Mol Cell 2010; 39:851–861 [View Article][PubMed]
     [Google Scholar]
  8. Anziano PQ, Perlman PS, Lang BF, Wolf K. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe : I. isolation and physical mapping of mitochondrial DNA. Curr Genet 1983; 7:273–284 [View Article][PubMed]
     [Google Scholar]
  9. Bullerwell CE, Leigh J, Forget L, Lang BF. A comparison of three fission yeast mitochondrial genomes. Nucleic Acids Res 2003; 31:759–768 [View Article][PubMed]
     [Google Scholar]
  10. Trinkl H, Lang BF, Wolf K. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe. 7. Continuous gene for apocytochrome b in strain EF1 (CBS 356) and sequence variation in the region of intron insertion in strain ade 7-50h . Mol Gen Genet 1985; 198:360–363[PubMed] [Crossref]
     [Google Scholar]
  11. Gan X, Yang J, Li J, Yu H, Dai H et al. The fission yeast Schizosaccharomyces pombe has two distinct tRNase ZLs encoded by two different genes and differentially targeted to the nucleus and mitochondria. Biochem J 2011; 435:103–111 [View Article][PubMed]
     [Google Scholar]
  12. Zhang X, Zhao Q, Huang Y. Partitioning of the nuclear and mitochondrial tRNA 3'-end processing activities between two different proteins in Schizosaccharomyces pombe . J Biol Chem 2013; 288:27415–27422 [View Article][PubMed]
     [Google Scholar]
  13. Zhao Z, Su W, Yuan S, Huang Y. Functional conservation of tRNase ZL among Saccharomyces cerevisiae, Schizosaccharomyces pombe and humans. Biochem J 2009; 422:483–492 [View Article][PubMed]
     [Google Scholar]
  14. Liu J, Huang L, Wang Y, Huang Y. Characterization of cis-elements in the promoter of trz2 encoding Schizosaccharomyces pombe mitochondrial tRNA 3'-end processing enzyme. Microbiology 2016; 163:75–85 [View Article][PubMed]
     [Google Scholar]
  15. Hoffmann B, Nickel J, Speer F, Schafer B. The 3' ends of mature transcripts are generated by a processosome complex in fission yeast mitochondria. J Mol Biol 2008; 377:1024–1037 [View Article][PubMed]
     [Google Scholar]
  16. Foury F, Roganti T, Lecrenier N, Purnelle B. The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae . FEBS Lett 1998; 440:325–331 [View Article][PubMed]
     [Google Scholar]
  17. Lang BF, Laforest MJ, Burger G. Mitochondrial introns: a critical view. Trends Genet 2007; 23:119–125 [View Article][PubMed]
     [Google Scholar]
  18. Tzagoloff A, Myers AM. Genetics of mitochondrial biogenesis. Annu Rev Biochem 1986; 55:249–285 [View Article][PubMed]
     [Google Scholar]
  19. Lambowitz AM, Belfort M. Introns as mobile genetic elements. Annu Rev Biochem 1993; 62:587–622 [View Article][PubMed]
     [Google Scholar]
  20. Pellenz S, Harington A, Dujon B, Wolf K, Schäfer B. Characterization of the I-Spom I endonuclease from fission yeast: insights into the evolution of a group I intron-encoded homing endonuclease. J Mol Evol 2002; 55:302–313 [View Article][PubMed]
     [Google Scholar]
  21. Schäfer B, Gan L, Perlman PS. Reverse transcriptase and reverse splicing activities encoded by the mobile group II intron cobI1 of fission yeast mitochondrial DNA. J Mol Biol 2003; 329:191–206 [View Article][PubMed]
     [Google Scholar]
  22. Lipinski KA, Kaniak-Golik A, Golik P. Maintenance and expression of the S. cerevisiae mitochondrial genome–from genetics to evolution and systems biology. Biochim Biophys Acta 2010; 1797:1086–1098 [View Article][PubMed]
     [Google Scholar]
  23. Bousquet I, Dujardin G, Poyton RO, Slonimski PP. Two group I mitochondrial introns in the cob-box and coxI genes require the same MRS1/PET157 nuclear gene product for splicing. Curr Genet 1990; 18:117–124 [View Article][PubMed]
     [Google Scholar]
  24. de Silva D, Poliquin S, Zeng R, Zamudio-Ochoa A, Marrero N et al. The DEAD-box helicase Mss116 plays distinct roles in mitochondrial ribogenesis and mRNA-specific translation. Nucleic Acids Res 2017; 45:6628–6643 [View Article][PubMed]
     [Google Scholar]
  25. Potratz JP, del Campo M, Wolf RZ, Lambowitz AM, Russell R. ATP-dependent roles of the DEAD-box protein Mss116p in group II intron splicing in vitro and in vivo . J Mol Biol 2011; 411:661–679 [View Article][PubMed]
     [Google Scholar]
  26. Conrad-Webb H, Perlman PS, Zhu H, Butow RA. The nuclear SUV3-1 mutation affects a variety of post-transcriptional processes in yeast mitochondria. Nucleic Acids Res 1990; 18:1369–1376 [View Article][PubMed]
     [Google Scholar]
  27. Watts T, Khalimonchuk O, Wolf RZ, Turk EM, Mohr G et al. Mne1 is a novel component of the mitochondrial splicing apparatus responsible for processing of a COX1 group I intron in yeast. J Biol Chem 2011; 286:10137–10146 [View Article][PubMed]
     [Google Scholar]
  28. Turk EM, Caprara MG. Splicing of yeast aI5β group I intron requires SUV3 to recycle MRS1 via mitochondrial degradosome-promoted decay of excised intron ribonucleoprotein (RNP). J Biol Chem 2010; 285:8585–8594 [View Article][PubMed]
     [Google Scholar]
  29. Sarkar J, Poruri K, Boniecki MT, McTavish KK, Martinis SA. Yeast mitochondrial leucyl-tRNA synthetase CP1 domain has functionally diverged to accommodate RNA splicing at expense of hydrolytic editing. J Biol Chem 2012; 287:14772–14781 [View Article][PubMed]
     [Google Scholar]
  30. Ott M, Amunts A, Brown A. Organization and regulation of mitochondrial protein synthesis. Annu Rev Biochem 2016; 85:77–101 [View Article][PubMed]
     [Google Scholar]
  31. Herrmann JM, Woellhaf MW, Bonnefoy N. Control of protein synthesis in yeast mitochondria: the concept of translational activators. Biochim Biophys Acta 2013; 1833:286–294 [View Article][PubMed]
     [Google Scholar]
  32. Smits P, Smeitink J, van den Heuvel L. Mitochondrial translation and beyond: processes implicated in combined oxidative phosphorylation deficiencies. J Biomed Biotechnol 2010; 2010:1–24 [View Article][PubMed]
     [Google Scholar]
  33. Kuzmenko A, Atkinson GC, Levitskii S, Zenkin N, Tenson T et al. Mitochondrial translation initiation machinery: conservation and diversification. Biochimie 2014; 100:132–140 [View Article][PubMed]
     [Google Scholar]
  34. Kühl I, Dujeancourt L, Gaisne M, Herbert CJ, Bonnefoy N. A genome wide study in fission yeast reveals nine PPR proteins that regulate mitochondrial gene expression. Nucleic Acids Res 2011; 39:8029–8041 [View Article][PubMed]
     [Google Scholar]
  35. Sasarman F, Brunel-Guitton C, Antonicka H, Wai T, Shoubridge EA. LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol Biol Cell 2010; 21:1315–1323 [View Article][PubMed]
     [Google Scholar]
  36. Ruzzenente B, Metodiev MD, Wredenberg A, Bratic A, Park CB et al. LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J 2012; 31:443–456 [View Article][PubMed]
     [Google Scholar]
  37. Chujo T, Ohira T, Sakaguchi Y, Goshima N, Nomura N et al. LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Res 2012; 40:8033–8047 [View Article][PubMed]
     [Google Scholar]
  38. Weraarpachai W, Antonicka H, Sasarman F, Seeger J, Schrank B et al. Mutation in TACO1, encoding a translational activator of COX I, results in cytochrome c oxidase deficiency and late-onset Leigh syndrome. Nat Genet 2009; 41:833–837 [View Article][PubMed]
     [Google Scholar]
  39. Richman TR, Spåhr H, Ermer JA, Davies SM, Viola HM et al. Loss of the RNA-binding protein TACO1 causes late-onset mitochondrial dysfunction in mice. Nat Commun 2016; 7:11884 [View Article][PubMed]
     [Google Scholar]
  40. Asher EB, Groudinsky O, Dujardin G, Altamura N, Kermorgant M et al. Novel class of nuclear genes involved in both mRNA splicing and protein synthesis in Saccharomyces cerevisiae mitochondria. Mol Gen Genet 1989; 215:517–528 [View Article][PubMed]
     [Google Scholar]
  41. Rodeheffer MS, Shadel GS. Multiple interactions involving the amino-terminal domain of yeast mtRNA polymerase determine the efficiency of mitochondrial protein synthesis. J Biol Chem 2003; 278:18695–18701 [View Article][PubMed]
     [Google Scholar]
  42. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie A et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe . Yeast 1998; 14:943–951 [View Article][PubMed]
     [Google Scholar]
  43. Wang Y, Yan J, Zhang Q, Ma X, Zhang J et al. The Schizosaccharomyces pombe PPR protein Ppr10 associates with a novel protein Mpa1 and acts as a mitochondrial translational activator. Nucleic Acids Res 2017; 45:3323–3340 [View Article][PubMed]
     [Google Scholar]
  44. Chiron S, Gaisne M, Guillou E, Belenguer P, Clark-Walker GD et al. Studying mitochondria in an attractive model: Schizosaccharomyces pombe . Methods Mol Biol 2007; 372:91–105 [View Article][PubMed]
     [Google Scholar]
  45. Su Y, Yang Y, Huang Y. Loss of ppr3, ppr4, ppr6, or ppr10 perturbs iron homeostasis and leads to apoptotic cell death in Schizosaccharomyces pombe . Febs J 2017; 284:324–337 [View Article][PubMed]
     [Google Scholar]
  46. Moreno S, Klar A, Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe . Methods Enzymol 1991; 194:795–823[PubMed] [Crossref]
     [Google Scholar]
  47. Gouget K, Verde F, Barrientos A. In vivo labeling and analysis of mitochondrial translation products in budding and in fission yeasts. Methods Mol Biol 2008; 457:113–124[PubMed] [Crossref]
     [Google Scholar]
  48. Meisinger C, Pfanner N, Truscott KN. Isolation of yeast mitochondria. Methods Mol Biol 2006; 313:33–39 [View Article][PubMed]
     [Google Scholar]
  49. Zuin A, Gabrielli N, Calvo IA, García-Santamarina S, Hoe KL et al. Mitochondrial dysfunction increases oxidative stress and decreases chronological life span in fission yeast. PLoS One 2008; 3:e2842 [View Article][PubMed]
     [Google Scholar]
  50. Kühl I, Fox TD, Bonnefoy N. Schizosaccharomyces pombe homologs of the Saccharomyces cerevisiae mitochondrial proteins Cbp6 and Mss51 function at a post-translational step of respiratory complex biogenesis. Mitochondrion 2012; 12:381–390 [View Article][PubMed]
     [Google Scholar]
  51. Dujeancourt L, Richter R, Chrzanowska-Lightowlers ZM, Bonnefoy N, Herbert CJ. Interactions between peptidyl tRNA hydrolase homologs and the ribosomal release factor Mrf1 in S. pombe mitochondria. Mitochondrion 2013; 13:871–880 [View Article][PubMed]
     [Google Scholar]
  52. Wiley DJ, Catanuto P, Fontanesi F, Rios C, Sanchez N et al. Bot1p is required for mitochondrial translation, respiratory function, and normal cell morphology in the fission yeast Schizosaccharomyces pombe . Eukaryot Cell 2008; 7:619–629 [View Article][PubMed]
     [Google Scholar]
  53. Clark TA, Sugnet CW, Ares M. Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 2002; 296:907–910 [View Article][PubMed]
     [Google Scholar]
  54. Schäfer B, Merlos-Lange AM, Anderl C, Welser F, Zimmer M et al. The mitochondrial genome of fission yeast: inability of all introns to splice autocatalytically, and construction and characterization of an intronless genome. Mol Gen Genet 1991; 225:158–167 [View Article][PubMed]
     [Google Scholar]
  55. Contamine V, Picard M. Maintenance and integrity of the mitochondrial genome: a plethora of nuclear genes in the budding yeast. Microbiol Mol Biol Rev 2000; 64:281–315 [View Article][PubMed]
     [Google Scholar]
  56. Groudinsky O, Bousquet I, Wallis MG, Slonimski PP, Dujardin G. The NAM1/MTF2 nuclear gene product is selectively required for the stability and/or processing of mitochondrial transcripts of the atp6 and of the mosaic, cox1 and cytb genes in Saccharomyces cerevisiae . Mol Gen Genet 1993; 240:419–427[PubMed]
     [Google Scholar]
  57. Rodeheffer MS, Boone BE, Bryan AC, Shadel GS. Nam1p, a protein involved in RNA processing and translation, is coupled to transcription through an interaction with yeast mitochondrial RNA polymerase. J Biol Chem 2001; 276:8616–8622 [View Article][PubMed]
     [Google Scholar]
  58. Bryan AC, Rodeheffer MS, Wearn CM, Shadel GS. Sls1p is a membrane-bound regulator of transcription-coupled processes involved in Saccharomyces cerevisiae mitochondrial gene expression. Genetics 2002; 160:75–82[PubMed]
     [Google Scholar]
  59. Barrientos A, Zambrano A, Tzagoloff A. Mss51p and Cox14p jointly regulate mitochondrial Cox1p expression in Saccharomyces cerevisiae . EMBO J 2004; 23:3472–3482 [View Article][PubMed]
     [Google Scholar]
  60. Perez-Martinez X, Broadley SA, Fox TD. Mss51p promotes mitochondrial Cox1p synthesis and interacts with newly synthesized Cox1p. EMBO J 2003; 22:5951–5961 [View Article][PubMed]
     [Google Scholar]
  61. Roloff GA, Henry MF. Mam33 promotes cytochrome c oxidase subunit I translation in Saccharomyces cerevisiae mitochondria. Mol Biol Cell 2015; 26:2885–2894 [View Article][PubMed]
     [Google Scholar]
  62. Kim DU, Hayles J, Kim D, Wood V, Park HO et al. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe . Nat Biotechnol 2010; 28:617–623 [View Article][PubMed]
     [Google Scholar]
  63. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article][PubMed]
     [Google Scholar]
  64. van Horn DJ, Yoo CJ, Xue D, Shi H, Wolin SL. The La protein in Schizosaccharomyces pombe: a conserved yet dispensable phosphoprotein that functions in tRNA maturation. RNA 1997; 3:1434–1443[PubMed]
     [Google Scholar]
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The fission yeast Schizosaccharomyces pombe Mtf2 is required for mitochondrial cox1 gene expression
Microbiology 164, 400 (2018); https://doi.org/10.1099/mic.0.000602
/content/journal/micro/10.1099/mic.0.000602
/content/journal/micro/10.1099/mic.0.000602
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