Molecular Genetics and Genomics

, Volume 286, Issue 5–6, pp 359–369 | Cite as

A functional RNase P protein subunit of bacterial origin in some eukaryotes

  • Lien B. Lai
  • Pilar Bernal-Bayard
  • Gireesha Mohannath
  • Stella M. Lai
  • Venkat Gopalan
  • Agustín Vioque
Original Paper

Abstract

RNase P catalyzes 5′-maturation of tRNAs. While bacterial RNase P comprises an RNA catalyst and a protein cofactor, the eukaryotic (nuclear) variant contains an RNA and up to ten proteins, all unrelated to the bacterial protein. Unexpectedly, a nuclear-encoded bacterial RNase P protein (RPP) homolog is found in several prasinophyte algae including Ostreococcus tauri. We demonstrate that recombinant O. tauri RPP can functionally reconstitute with bacterial RNase P RNAs (RPRs) but not with O. tauri organellar RPRs, despite the latter’s presumed bacterial origins. We also show that O. tauri PRORP, a homolog of Arabidopsis PRORP-1, displays tRNA 5′-processing activity in vitro. We discuss the implications of the striking diversity of RNase P in O. tauri, the smallest known free-living eukaryote.

Keywords

RNase P diversity Prasinophyte pre-tRNA processing 

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Brown JW (1999) The ribonuclease P database. Nucleic Acids Res 27:314PubMedCrossRefGoogle Scholar
  3. Chen JL, Pace NR (1997) Identification of the universally conserved core of ribonuclease P RNA. RNA 3:557–560PubMedGoogle Scholar
  4. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500PubMedCrossRefGoogle Scholar
  5. De la Cruz J, Vioque A (2003) A structural and functional study of plastid RNAs homologous to catalytic bacterial RNase P RNA. Gene 321:47–56CrossRefGoogle Scholar
  6. Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652PubMedCrossRefGoogle Scholar
  7. Esakova O, Krasilnikov AS (2010) Of proteins and RNA: the RNase P/MRP family. RNA 16:1725–1747PubMedCrossRefGoogle Scholar
  8. Evans D, Marquez SM, Pace NR (2006) RNase P: interface of the RNA and protein worlds. Trends Biochem Sci 31:333–341PubMedCrossRefGoogle Scholar
  9. Gobert A, Gutmann B, Taschner A, Gossringer M, Holzmann J, Hartmann RK, Rossmanith W, Giege P (2010) A single Arabidopsis organellar protein has RNase P activity. Nat Struct Mol Biol 17:740–744PubMedCrossRefGoogle Scholar
  10. Gopalan V (2007) Uniformity amid diversity in RNase P. Proc Natl Acad Sci USA 104:2031–2032PubMedCrossRefGoogle Scholar
  11. Guerrier-Takada C, Li Y, Altman S (1995) Artificial regulation of gene expression in Escherichia coli by RNase P. Proc Nat Acad Sci USA 92:11115–11119PubMedCrossRefGoogle Scholar
  12. Hardy E, Castellanos-Serra LR (2004) “Reverse-staining” of biomolecules in electrophoresis gels: analytical and micropreparative applications. Anal Biochem 328:1–13PubMedCrossRefGoogle Scholar
  13. Harlow E, Lane D (1988) Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  14. Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C, Rossmanith W (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135:462–474PubMedCrossRefGoogle Scholar
  15. Jarrous N, Gopalan V (2010) Archaeal/eukaryal RNase P: subunits, functions and RNA diversification. Nucleic Acids Res 38:7885–7894PubMedCrossRefGoogle Scholar
  16. Jovanovic M, Sanchez R, Altman S, Gopalan V (2002) Elucidation of structure-function relationships in the protein subunit of bacterial RNase P using a genetic complementation approach. Nucleic Acids Res 23:5065–5073Google Scholar
  17. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638CrossRefGoogle Scholar
  18. Kirsebom LA (2007) RNase P RNA mediated cleavage: substrate recognition and catalysis. Biochimie 89:1183–1194PubMedCrossRefGoogle Scholar
  19. Kirsebom LA, Svard SG (1994) Base pairing between Escherichia coli RNase P RNA and its substrate. EMBO J 13:4870–4876PubMedGoogle Scholar
  20. Lai LB, Vioque A, Kirsebom LA, Gopalan V (2010) Unexpected diversity of RNase P, an ancient tRNA processing enzyme: challenges and prospects. FEBS Lett 584:287–296PubMedCrossRefGoogle Scholar
  21. Li D, Willkomm DK, Schön A, Hartmann RK (2007) RNase P of the Cyanophora paradoxa cyanelle: a plastid ribozyme. Biochimie 89:1528–1538PubMedCrossRefGoogle Scholar
  22. Liu F, Altman S (2010) Ribonuclease P. Springer-Verlag, New YorkCrossRefGoogle Scholar
  23. Marquez SM, Harris JK, Kelley ST, Brown JW, Dawson SC, Roberts EC, Pace NR (2005) Structural implications of novel diversity in eucaryal RNase P RNA. RNA 11:739–751PubMedCrossRefGoogle Scholar
  24. Maruyama S, Sugahara J, Kanai A, Nozaki H (2010) Permuted tRNA genes in the nuclear and nucleomorph genomes of photosynthetic eukaryotes. Mol Biol Evol 27:1070–1076PubMedCrossRefGoogle Scholar
  25. McClain WH, Lai LB, Gopalan V (2010) Trials, travails and triumphs: an account of RNA catalysis in RNase P. J Mol Biol 397:627–646PubMedCrossRefGoogle Scholar
  26. McDonald SM, Plant JN, Worden AZ (2010) The mixed lineage nature of nitrogen transport and assimilation in marine eukaryotic phytoplankton: a case study of Micromonas. Mol Biol Evol 27:2268–2283PubMedCrossRefGoogle Scholar
  27. Morales MJ, Dang YL, Lou YC, Sulo P, Martin NC (1992) A 105 kDa protein is required for yeast mitochondrial RNase P activity. Proc Natl Acad Sci USA 89:9875–9879PubMedCrossRefGoogle Scholar
  28. Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Jancek S, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H, Grigoriev IV (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 104:7705–7710PubMedCrossRefGoogle Scholar
  29. Pascual A, Vioque A (1996) Cloning, purification and characterization of the protein subunit of ribonuclease P from the cyanobacterium Synechocystis sp. PCC 6803. Eur J Biochem 241:17–24PubMedCrossRefGoogle Scholar
  30. Pascual A, Vioque A (1999a) Functional reconstitution of RNase P activity from a plastid RNA subunit and a cyanobacterial protein subunit. FEBS Lett 442:7–10PubMedCrossRefGoogle Scholar
  31. Pascual A, Vioque A (1999b) Substrate binding and catalysis by ribonuclease P from cyanobacteria and Escherichia coli are affected differently by the 3′ terminal CCA in tRNA precursors. Proc Natl Acad Sci USA 96:6672–6677PubMedCrossRefGoogle Scholar
  32. Pomeranz Krummel DA, Altman S (1999) Verification of phylogenetic predictions in vivo and the importance of the tetraloop motif in a catalytic RNA. Proc Natl Acad Sci USA 96:11200–11205PubMedCrossRefGoogle Scholar
  33. Reiner R, Ben-Asouli Y, Krilovetzky I, Jarrous N (2006) A role for the catalytic ribonucleoprotein RNase P in RNA polymerase III transcription. Genes Dev 20:1621–1635PubMedCrossRefGoogle Scholar
  34. Reiner R, Krasnov-Yoeli N, Dehtiar Y, Jarrous N (2008) Function and assembly of a chromatin-associated RNase P that is required for efficient transcription by RNA polymerase I. PLoS One 3:e4072PubMedCrossRefGoogle Scholar
  35. Reiter NJ, Osterman A, Torres-Larios A, Swinger KK, Pan T, Mondragon A (2010) Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature 468:784–789PubMedCrossRefGoogle Scholar
  36. Rosenblad MA, Lopez MD, Piccinelli P, Samuelsson T (2006) Inventory and analysis of the protein subunits of the ribonucleases P and MRP provides further evidence of homology between the yeast and human enzymes. Nucleic Acids Res 34:5145–5156PubMedCrossRefGoogle Scholar
  37. Schedl P, Primakoff P (1973) Mutants of Escherichia coli thermosensitive for the synthesis of transfer RNA. Proc Natl Acad Sci USA 70:2091–2095PubMedCrossRefGoogle Scholar
  38. Tsai HY, Lai LB, Gopalan V (2002) A modified pBluescript-based vector for facile cloning and transcription of RNAs. Anal Biochem 303:214–217PubMedCrossRefGoogle Scholar
  39. Turmel M, Lemieux C, Burger G, Lang BF, Otis C, Plante I, Gray MW (1999a) The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor. Two radically different evolutionary patterns within green algae. Plant Cell 11:1717–1730PubMedCrossRefGoogle Scholar
  40. Turmel M, Otis C, Lemieux C (1999b) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96:10248–10253PubMedCrossRefGoogle Scholar
  41. Vioque A (1992) Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucleic Acids Res 20:6331–6337PubMedCrossRefGoogle Scholar
  42. Vioque A, Arnez J, Altman S (1988) Protein-RNA interactions in the RNase P holoenzyme from Escherichia coli. J Mol Biol 202:835–848PubMedCrossRefGoogle Scholar
  43. Walker SC, Engelke DR (2006) Ribonuclease P: the evolution of an ancient RNA enzyme. Crit Rev Biochem Mol Biol 41:77–102PubMedCrossRefGoogle Scholar
  44. Wang G, Chen HW, Oktay Y, Zhang J, Allen EL, Smith GM, Fan KC, Hong JS, French SW, McCaffery JM, Lightowlers RN, Morse HC 3rd, Koehler CM, Teitell MA (2010) PNPASE regulates RNA import into mitochondria. Cell 142:456–467PubMedCrossRefGoogle Scholar
  45. Worden AZ, Lee JH, Mock T, Rouze P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV, Foulon E, Grimwood J, Gundlach H, Henrissat B, Napoli C, McDonald SM, Parker MS, Rombauts S, Salamov A, Von Dassow P, Badger JH, Coutinho PM, Demir E, Dubchak I, Gentemann C, Eikrem W, Gready JE, John U, Lanier W, Lindquist EA, Lucas S, Mayer KF, Moreau H, Not F, Otillar R, Panaud O, Pangilinan J, Paulsen I, Piegu B, Poliakov A, Robbens S, Schmutz J, Toulza E, Wyss T, Zelensky A, Zhou K, Armbrust EV, Bhattacharya D, Goodenough UW, Van de Peer Y, Grigoriev IV (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Lien B. Lai
    • 1
    • 2
  • Pilar Bernal-Bayard
    • 3
  • Gireesha Mohannath
    • 1
    • 2
  • Stella M. Lai
    • 1
    • 2
  • Venkat Gopalan
    • 1
    • 2
  • Agustín Vioque
    • 3
  1. 1.Department of BiochemistryThe Ohio State UniversityColumbusUSA
  2. 2.Center for RNA BiologyThe Ohio State UniversityColumbusUSA
  3. 3.Instituto de Bioquímica Vegetal y FotosíntesisUniversidad de Sevilla and CSICSevillaSpain

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