Advertisement

Journal of Plant Biology

, Volume 59, Issue 1, pp 44–54 | Cite as

Exclusive cytosolic localization and broad tRNASer specificity of Arabidopsis thaliana seryl-tRNA synthetase

  • Mario Kekez
  • Natasa Bauer
  • Ela Saric
  • Jasmina Rokov-Plavec
Original Article

Abstract

Aminoacyl-tRNA synthetases (aaRSs) decipher the genetic code, covalently linking amino acids to cognate tRNAs, thus preparing substrates for the process of translation. Although aaRSs funtion primarily in translation and are localized in cytosol, mitochondria and chloroplasts there are many reports on their additional functions and subcellular destinations beyond translation. However, data on plant aaRSs are scarce. Initial analysis of amino acid sequence of Arabidopsis thaliana seryl-tRNA synthetase (SerRS) suggested that protein contains putative nuclear localization signals. GFP-localization experiments in transiently transformed epidermal onion cells and Arabidopsis protoplasts gave ambiguous results because in some cells SerRS appeared to be dually localized to both cytosol and nucleus. However, data obtained on transgenic lines expressing SerRS-TAP and GFP-SerRS revealed exclusive cytosolic location of SerRS. Subcellular distribution of SerRS did not change during stress. Cytosolic Arabidopsis SerRS was expressed and purified. The enzyme efficiently aminoacylated eukaryotic and bacterial tRNAsSer, that are structurally very different. Given the fact that the same behavior was previously shown for monocot maize SerRS, it seems that plant SerRSs exhibit unusually broad tRNASer specificity, unlike SerRSs from other organisms. Possible functional implications of this unique characteristic of plant SerRSs are discussed.

Key words

Aminoacyl-tRNA synthetase Arabidopsis plant seryl-tRNA synthetase Subcellular localization tRNA 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12374_2016_370_MOESM1_ESM.docx (1.3 mb)
Supplementary material, approximately 1.28 MB.

References

  1. Alinsug MV, Chen FF, Luo M, Tai R, Jiang L, Wu K (2012) Subcellular localization of class II HDAs in Arabidopsis thaliana: nucleocytoplasmic shuttling of HDA15 is driven by light. PLoS One 7:e30846PubMedCentralCrossRefPubMedGoogle Scholar
  2. Asahara H, Himeno H, Tamura K, Nameki N, Hasegawa T, Shimizu M (1994) Escherichia coli seryl-tRNA synthetase recognizes tRNA(Ser) by its characteristic tertiary structure. J Mol Biol 236:738–748CrossRefPubMedGoogle Scholar
  3. Audhya A, Emr SD (2003) Regulation of PI4,5P2 synthesis by nuclear-cytoplasmic shuttling of the Mss4 lipid kinase. EMBO J. 22:4223–4236PubMedCentralCrossRefPubMedGoogle Scholar
  4. Berg M, Rogers R, Muralla R, Meinke D (2005) Requirement of aminoacyl-tRNA synthetases for gametogenesis and embryo development in Arabidopsis. Plant J 44:866–878CrossRefPubMedGoogle Scholar
  5. Bilokapic S, Ivic N, Godinic-Mikulcic V, Piantanida I, Ban N, Weygand-Durasevic I (2009) Idiosyncratic helix-turn-helix motif in Methanosarcina barkeri seryl-tRNA synthetase has a critical architectural role. J Biol Chem 284:10706–10713PubMedCentralCrossRefPubMedGoogle Scholar
  6. Bilokapic S, Maier T, Ahel D, Gruic-Sovulj I, Söll D, Weygand-Durasevic I, Ban N (2006) Structure of the unusual seryl-tRNA synthetase reveals a distinct zinc-dependent mode of substrate recognition. EMBO J 25:2498–2509PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bosco D, Meda P, Iynedjian PB (2000) Glucokinase and glucokinase regulatory protein: mutual dependence for nuclear localization. Biochem J 348:215–222PubMedCentralCrossRefPubMedGoogle Scholar
  8. Brãndao MM, Silva-Filho MC (2011) Evolutionary history of Arabidopsis thaliana aminoacyl-tRNA synthetase dual-targeted proteins. Mol Biol Evol 28:79–85CrossRefPubMedGoogle Scholar
  9. Bullwinkle TJ, Ibba M (2014) Emergence and evolution. Top Curr Chem 344:43–87PubMedCentralCrossRefPubMedGoogle Scholar
  10. Chan PP, Lowe TM (2009) GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37(Database issue):D93–97PubMedCentralCrossRefPubMedGoogle Scholar
  11. Chen M, Tao Y, Lim J, Shaw A, Chory J (2005) Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals. Curr Biol 15:637–642CrossRefPubMedGoogle Scholar
  12. Citovsky V, Zupan J, Warnick D, Zambryski P (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256:1802–1805CrossRefPubMedGoogle Scholar
  13. Clough SJ, Bent AJ (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  14. Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peters NM, Zaepfel M, Marechal-Drouard L, Small ID (2005) Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:16484–16489PubMedCentralCrossRefPubMedGoogle Scholar
  15. Duchêne AM, Pujol C, Maréchal-Drouard L (2009) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet 55:1–18CrossRefPubMedGoogle Scholar
  16. Enninga J, Levay A, Fontoura BM (2003) Sec13 shuttles between the nucleus and the cytoplasm and stably interacts with Nup96 at the nuclear pore complex. Mol Cell Biol 23:7271–7284PubMedCentralCrossRefPubMedGoogle Scholar
  17. Godinic V, Mocibob M, Rocak S, Ibba M, Weygand-Durasevic I (2007) Peroxin Pex21p interacts with the C-terminal noncatalytic domain of yeast seryl-tRNA synthetase and forms a specific ternary complex with tRNA(Ser). FEBS J 274:2788–2799CrossRefPubMedGoogle Scholar
  18. Godinic-Mikulcic V, Jaric J, Greber BJ, Franke V, Hodnik V, Anderluh G, Ban N, Weygand-Durasevic I (2014) Archaeal aminoacyltRNA synthetases interact with the ribosome to recycle tRNAs. Nucleic Acids Res 42:5191–5201PubMedCentralCrossRefPubMedGoogle Scholar
  19. Guo M, Schimmel P (2013) Essential nontranslational functions of tRNA synthetases. Nat Chem Biol 9:145–153PubMedCentralCrossRefPubMedGoogle Scholar
  20. Guo M, Yang XL (2014) Architecture and metamorphosis. Top Curr Chem 344:89–118PubMedCentralCrossRefPubMedGoogle Scholar
  21. Härtlein M, Cusack S (1995) Structure, function and evolution of seryl-tRNA synthetases: implications for the evolution of aminoacyltRNA synthetases and the genetic code. J Mol Evol 40:519–530CrossRefPubMedGoogle Scholar
  22. Inzé A, Vanderauwera S, Hoeberichts FA, Vandorpe M, Van Gaever T, Van Breusegem F (2012) A subcellular localization compendium of hydrogen peroxide-induced proteins. Plant Cell Environ 35:308–320CrossRefPubMedGoogle Scholar
  23. Kato A, Maki K, Ebina T, Kuwajima K, Soda K, Kuroda Y (2007) Mutational analysis of protein solubility enhancement using short peptide tags. Biopolymers 85:12–18CrossRefPubMedGoogle Scholar
  24. Kim JH, Han JM, Kim S (2014) Protein-protein interactions and multi-component complexes of aminoacyl-tRNA synthetases Top Curr Chem 344:119–144CrossRefPubMedGoogle Scholar
  25. Kim YK, Lee JY, Cho HS, Lee SS, Ha HJ, Kim S, Choi D, Pai HS (2005) Inactivation of organellar glutamyl-and seryl-tRNA synthetases leads to developmental arrest of chloroplasts and mitochondria in higher plants. J Biol Chem 280:37098–37106CrossRefPubMedGoogle Scholar
  26. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:1202–1210CrossRefGoogle Scholar
  27. Leljak Levanic D, Horvat T, Martincic J, Bauer N (2012) A novel bipartite nuclear localization signal guides BPM1 protein to nucleolus suggesting its Cullin3 independent function. PLoS One 7:e51184PubMedCentralCrossRefPubMedGoogle Scholar
  28. Lenhard B, Praetorius-Ibba M, Filipic S, Söll D, Weygand-Durasevic I (1998) C-terminal truncation of yeast SerRS is toxic for Saccharomyces cerevisiae due to altered mechanism of substrate recognition. FEBS Lett 439:235–240CrossRefPubMedGoogle Scholar
  29. Luna E, van Hulten M, Zhang Y, Berkowitz O, López A, Pétriacq P, Sellwood MA, Chen B, Burrell M, van de Meene A, Pieterse CM, Flors V, Ton J (2014) Plant perception of ß-aminobutyric acid is mediated by an aspartyl-tRNA synthetase. Nat Chem Biol 10:450–456PubMedCentralCrossRefPubMedGoogle Scholar
  30. McLane LM, Corbett AH (2009) Nuclear localization signals and human disease. IUBMB Life 61:697–706CrossRefPubMedGoogle Scholar
  31. Michaud M, Cognat V, Duchêne AM, Maréchal-Drouard L (2011) A global picture of tRNA genes in plant genomes. Plant J 66:80–93CrossRefPubMedGoogle Scholar
  32. Mocibob M, Ivic N, Bilokapic S, Maier T, Luic M, Ban N, Weygand-Durasevic I (2010) Homologs of aminoacyl-tRNA synthetases acylate carrier proteins and provide a link between ribosomal and nonribosomal peptide synthesis. Proc Natl Acad Sci USA 107:14585–14590PubMedCentralCrossRefPubMedGoogle Scholar
  33. Mocibob M, Weygand-Durasevic I (2008) The proximal region of a noncatalytic eucaryotic seryl-tRNA synthetase extension is required for protein stability in vitro and in vivo. Arch Biochem Biophys 470:129–138CrossRefPubMedGoogle Scholar
  34. Pang SZ, DeBoer DL, Wan Y, Ye G, Layton JG, Neher MK, Armstrong CL, Fry JE, Hinchee MA, Fromm ME (1996) An improved green fluorescent protein gene as a vital marker in plants. Plant Physiol 112:893–900PubMedCentralCrossRefPubMedGoogle Scholar
  35. Perona JJ, Gruic-Sovulj I (2014) Synthetic and editing mechanisms of aminoacyl-tRNA synthetases. Top Curr Chem 344:1–41CrossRefPubMedGoogle Scholar
  36. Rokov J, Söll D, Weygand-Durasevic I (1998) Maize mitochondrial seryl-tRNA synthetase recognizes Escherichia coli tRNA(Ser) in vivo and in vitro. Plant Mol Biol 38:497–502CrossRefPubMedGoogle Scholar
  37. Rokov J, Weygand-Durasevic I (1999) Seryl-tRNA synthesis in maize. Period Biol 101:137–142Google Scholar
  38. Rokov-Plavec J, Bilokapic S, Gruic-Sovulj I, Mocibob M, Glavan F, Brgles M, Weygand-Durasevic I (2004) Unilateral flexibility in tRNASer recognition by heterologuous seryl-tRNA synthetase. Period Biol 106:147–154Google Scholar
  39. Rokov-Plavec J, Dulic M, Duchêne AM, Weygand-Durasevic I (2008) Dual targeting of organellar seryl-tRNA synthetase to maize mitochondria and chloroplasts. Plant Cell Rep 27:1157–1168CrossRefPubMedGoogle Scholar
  40. Rokov-Plavec J, Lesjak S, Gruic-Sovulj I, Mocibob M, Dulic M, Weygand-Durasevic I (2013) Substrate recognition and fidelity of maize seryl-tRNA synthetases. Arch Biochem Biophys 129:122–130CrossRefGoogle Scholar
  41. Rokov-Plavec J, Lesjak S, Landeka I, Mijakovic I, Weygand-Durasevic I (2002) Maize seryl-tRNA synthetase: specificity of substrate recognition by the organellar enzyme. Arch Biochem Biophys 397:40–50CrossRefPubMedGoogle Scholar
  42. Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugovieux V, Jourdain A, Bastien O, Fievet JB, Valihen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure by protein and metabolite profiling analyses. Proteomics 6:2180–2198CrossRefPubMedGoogle Scholar
  43. Saslowsky DE, Warek U, Winkel BS (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740CrossRefPubMedGoogle Scholar
  44. Shi Y, Xu X, Zhang Q, Fu G, Mo Z, Wang GS, Kishi S, Yang XL (2014) tRNA synthetase counteracts c-Myc to develop functional vasculature. Elife 3:e02349PubMedCentralPubMedGoogle Scholar
  45. Smirnova EV, Lakunina VA, Tarassov I, Krasheninnikov IA, Kamenski PA (2012) Noncanonical functions of aminoacyl-tRNA synthetases. Biochemistry (Mosc) 77:15–25CrossRefGoogle Scholar
  46. Soma A, Himeno H (1998) Cross-species aminoacylation of tRNA with a long variable arm between Escherichia coli and Saccharomyces cerevisiae. Nucleic Acids Res 26:4374–4381PubMedCentralCrossRefPubMedGoogle Scholar
  47. Son SH, Park MC, Kim S (2014) Extracellular activities of aminoacyltRNA synthetases: new mediators for cell-cell communication. Top Curr Chem 344:145–166CrossRefPubMedGoogle Scholar
  48. Steinmetz A, Weil JH (1986) Isolation and characterization of chloroplast and cytoplasmic transfer RNAs. Meth Enzymol 118:212–231CrossRefGoogle Scholar
  49. Tian X, Zheng J, Hu S, Yu J (2007) The discriminatory transfer routes of tRNA genes among organellar and nuclear genomes in flowering plants: a genome-wide investigation of indica rice. J Mol Evol 64:299–307CrossRefPubMedGoogle Scholar
  50. Vasina JA, Baneyx F (1997) Expression of aggregation-prone recombinant proteins at low temperatures: a comparative study of the Escherichia coli cspA and tac promoter systems. Protein Expr Purif 9:211–218CrossRefPubMedGoogle Scholar
  51. Wang W, Ye R, Xin Y, Fang X, Li C, Shi H, Zhou X, Qi Y (2011) An importin ß protein negatively regulates MicroRNA activity in Arabidopsis. Plant Cell 23:3565–3576PubMedCentralCrossRefPubMedGoogle Scholar
  52. Wei N, Shi Y, Truong LN, Fisch KM, Xu T, Gardiner E, Fu G, Hsu YS, Kishi S, Su AI, Wu X, Yang XL (2014) Oxidative stress diverts tRNA synthetase to nucleus for protection against DNA damage. Mol Cell 56:323–332PubMedCentralCrossRefPubMedGoogle Scholar
  53. Weygand-Durasevic I, Ban N, Jahn D, Söll D (1993) Yeast seryltRNA synthetase expressed in Escherichia coli recognizes bacterial serine-specific tRNAs in vivo. Eur J Biochem 214:869–877CrossRefPubMedGoogle Scholar
  54. Wu XQ, Gross HJ (1993) The long extra arms of human tRNA((Ser)Sec) and tRNA(Ser) function as major identify elements for serylation in an orientation-dependent, but not sequence-specific manner. Nucleic Acids Res 21:5589–5594PubMedCentralCrossRefPubMedGoogle Scholar
  55. Xu X, Shi Y, Yang XL (2013) Crystal structure of human Seryl-tRNA synthetase and Ser-SA complex reveals a molecular lever specific to higher eukaryotes. Structure. 21:2078–2086CrossRefPubMedGoogle Scholar
  56. Xu XL, Shi Y, Zhang HM, Swindell EC, Marshall AG, Guo M, Kishi S, Yang XL (2012) Unique domain appended to vertebrate tRNA synthetase is essential for vascular development. Nat Commun 3:681PubMedCentralCrossRefPubMedGoogle Scholar
  57. Yang O, Popova OV, Süthoff U, Lüking I, Dietz KJ, Golldack D (2009) The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436:45–55CrossRefPubMedGoogle Scholar
  58. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572CrossRefPubMedGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Mario Kekez
    • 1
  • Natasa Bauer
    • 2
  • Ela Saric
    • 1
  • Jasmina Rokov-Plavec
    • 1
  1. 1.Division of Biochemistry, Chemistry Department, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  2. 2.Division of Molecular Biology, Biology Department, Faculty of ScienceUniversity of ZagrebZagrebCroatia

Personalised recommendations