Loss of a Conserved tRNA Anticodon Modification Perturbs Plant Immunity
Numerous studies revealed the existence of nearly 110 ribonucleoside structures incorporated as post-transcriptional modifications in tRNA, with 25–30 modifications present in any one organism. Emerging evidence points to the critical role of tRNA modifications in various cellular responses to stimuli, including transcription of stress response genes and control of cell viability and growth. The primary function of tRNA modifications, and in particular tRNA methylations, are linked to different steps in protein synthesis including stabilization of tRNA structures, reinforcement of the codon-anticodon interaction, regulation of wobble base pairing, and prevention of frameshift errors. Furthermore, tRNA methylations are involved in the RNA quality control system and regulation of tRNA localization in the cell, all of which affect translation rate, but modifications in the anti-codon, which exhibit important roles in decoding mRNA are particularly important. We identified that the SCS9 gene from Arabidopsis encodes a tRNA 2´-O-ribose methyltransferase homologous to the TRM7 methyltransferase from yeast. We identify that SCS9 is crucial for the 2´-O-ribose methylation of nucleotides 32 and 34 of the tRNAs anticodon loop of certain tRNA molecules. We show that SCS9 is required for effectiveness of plant immunity and suggest the importance of precise tRNA modifications in this process.
Vyšlo v časopise:
Loss of a Conserved tRNA Anticodon Modification Perturbs Plant Immunity. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005586
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005586
Souhrn
Numerous studies revealed the existence of nearly 110 ribonucleoside structures incorporated as post-transcriptional modifications in tRNA, with 25–30 modifications present in any one organism. Emerging evidence points to the critical role of tRNA modifications in various cellular responses to stimuli, including transcription of stress response genes and control of cell viability and growth. The primary function of tRNA modifications, and in particular tRNA methylations, are linked to different steps in protein synthesis including stabilization of tRNA structures, reinforcement of the codon-anticodon interaction, regulation of wobble base pairing, and prevention of frameshift errors. Furthermore, tRNA methylations are involved in the RNA quality control system and regulation of tRNA localization in the cell, all of which affect translation rate, but modifications in the anti-codon, which exhibit important roles in decoding mRNA are particularly important. We identified that the SCS9 gene from Arabidopsis encodes a tRNA 2´-O-ribose methyltransferase homologous to the TRM7 methyltransferase from yeast. We identify that SCS9 is crucial for the 2´-O-ribose methylation of nucleotides 32 and 34 of the tRNAs anticodon loop of certain tRNA molecules. We show that SCS9 is required for effectiveness of plant immunity and suggest the importance of precise tRNA modifications in this process.
Zdroje
1. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, Olchowik A, et al. MODOMICS: a database of RNA modification pathways–2013 update. Nucleic Acids Res. 2013;41: D262–267. doi: 10.1093/nar/gks1007 23118484
2. Hori H. Methylated nucleosides in tRNA and tRNA methyltransferases. Front Genet. 2014;5: 144. doi: 10.3389/fgene.2014.00144 eCollection 2014. 24904644
3. El Yacoubi B, Bailly M, de Crécy-Lagard V. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet. 2012;46: 69–95. doi: 10.1146/annurev-genet-110711-155641 22905870
4. Phizicky EM, Hopper AK. tRNA biology charges to the front. Genes Dev. 2010;24: 1832–1860. doi: 10.1101/gad.1956510 20810645
5. Novoa EM, Pavon-Eternod M, Pan T, Ribas De Pouplana L. A role for tRNA modifications in genome structure and codon usage. Cell. 2012;149: 202–213. doi: 10.1016/j.cell.2012.01.050 22464330
6. Chen P, Jäger G, Zheng B. Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana. BMC Plant Biol. 2010;10: 201. doi: 10.1186/1471-2229-10-201 20836892
7. Walden TL Jr, Howes N, Farkas WR. Purification and properties of guanine, queuine-tRNA transglycosylase from wheat germ. J Biol Chem. 1982;257: 13218–13222. 7142141
8. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, et al. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA. 2006;103: 16598–16603. 17062755
9. Kalhor HR, Clarke S. Novel methyltransferase for modified uridine residues at the wobble position of tRNA. Mol Cell Biol. 2003;23: 9283–9292. 14645538
10. Jühling F, Mörl M, Hartmann RK, Sprinzl M, Stadler PF, Pütz J. tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res. 2009;37: D159–162. doi: 10.1093/nar/gkn772 18957446
11. Thompson DM, Parker R. Stressing out over tRNA cleavage. Cell. 2009;138: 215–219. doi: 10.1016/j.cell.2009.07.001 19632169
12. Agris PF, Vendeix FA, Graham WD. tRNA’s wobble decoding of the genome: 40 years of modification. J Mol Biol. 2007;366: 1–13. 17187822
13. Pintard L, Lecointe F, Bujnicki JM, Bonnerot C, Grosjean H, Lapeyre B. Trm7p catalyses the formation of two 2′-O-methylriboses in yeast tRNA anticodon loop. EMBO J. 2002;21: 1811–1820. 11927565
14. Takano K, Nakagawa E, Inoue K, Kamada F, Kure S, Goto Y. A loss-of-function mutation in the FTSJ1 gene causes nonsyndromic X-linked mental retardation in a Japanese family. Am J Med Genet B Neuropsychiatr Genet. 2008;147B: 479–484. 18081026
15. Kuchino Y, Borek E, Grunberger D, Mushinski JF, Nishimura S. Changes of post-transcriptional modification of wye base in tumor-specific tRNAPhe. Nucleic Acids Res. 1982;10: 6421–6432. 6924749
16. Gil MJ, Coego A, Mauch-Mani B, Jordá L, Vera P. The Arabidopsis csb3 mutant reveals a regulatory link between salicylic acid-mediated disease resistance and the methyl-erythritol 4-phosphate pathway. Plant J. 2005;44: 155–166. 16167903
17. Jorda L, Vera P. Local and systemic induction of two defense-related subtilisin-like protease promoters in transgenic Arabidopsis plants. Plant Physiol. 2000;124: 1049–1058. 11080282
18. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science. 2009;323: 95–101. doi: 10.1126/science.1164627 19095898
19. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002;415: 977–983. 11875555
20. Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, et al. Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA. 2009;106: 8067–8072.
21. Nawrath C, Métraux JP. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell. 1999;11: 1393–1404. 10449575
22. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997;88: 57–63. 9019406
23. Ramírez V, López A, Mauch-Mani B, Gil MJ, Vera P. An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathog. 2013;9: e1003445. doi: 10.1371/journal.ppat.1003445 23818851
24. Austin RS, Vidaurre D, Stamatiou G, Breit R, Provart NJ, Bonetta D, et al. Next-generation mapping of Arabidopsis genes. Plant J. 2011;67: 715–725. doi: 10.1111/j.1365-313X.2011.04619.x 21518053
25. Caldas T, Binet E, Bouloc P, Costa A, Desgres J, Richarme G. The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23S ribosomal RNA methyltransferase. J Biol Chem. 2000;275: 16414–16419. 10748051
26. Bügl H, Fauman EB, Staker BL, Zheng F, Kushner SR, Saper MA, et al. RNA methylation under heat shock control. Mol Cell. 2000;6: 349–360. 10983982
27. Pósfai J, Bhagwat AS, Pósfai G, Roberts RJ. Predictive motifs derived from cytosine methyltransferases. Nucleic Acids Res. 1989;17: 2421–2435. 2717398
28. Bujnicki JM, Rychlewski L. Reassignment of specificities of two cap methyltransferase domains in the reovirus λ2 protein. Genome Biol. 2001;2, RESEARCH0038. 11574057
29. Chernoff YO, Vincent A, Liebman SW. Mutations in eukaryotic 18S ribosomal RNA affect translational fidelity and resistance to aminoglycoside antibiotics. EMBO J. 1994;13: 906–913. 8112304
30. Khoury CM, Yang Z, Li XY, Vignali M, Fields S, Greenwood MT. A TSC22-like motif defines a novel antiapoptotic protein family. FEMS Yeast Res. 2008;8: 540–563. doi: 10.1111/j.1567-1364.2008.00367.x 18355271
31. Rózanowska M, Ciszewska J, Korytowski W, Sarna T. Rose-bengal-photosensitized formation of hydrogen peroxide and hydroxyl radicals. J Photochem Photobiol B. 1995;29: 71–77.
32. Kramer EB, Hopper AK. Retrograde transfer RNA nuclear import provides a new level of tRNA quality control in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2013;110: 21042–21047. doi: 10.1073/pnas.1316579110 24297920
33. Wilkinson ML, Crary SM, Jackman JE, Grayhack EJ, Phizicky EM. The 2′-O-methyltransferase responsible for modification of yeast tRNA at position 4. RNA. 2007;13: 404–413. 17242307
34. Ellis SR, Morales MJ, Li JM, Hopper AK, Martin NC. Isolation and characterization of the TRM1 locus, a gene essential for the N2,N2-dimethylguanosine modification of both mitochondrial and cytoplasmic tRNA in Saccharomyces cerevisiae. J Biol Chem. 1986;261: 9703–9709. 2426253
35. Motorin Y, Grosjean H. Multisite-specific tRNA:m5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: Identification of the gene and substrate specificity of the enzyme. RNA. 1999;5: 1105–1118. 10445884
36. Gerber A, Grosjean H, Melcher T, Keller W. Tad1p, a yeast tRNA-specific adenosine deaminase, is related to the mammalian pre-mRNA editing enzymes ADAR1 and ADAR2. EMBO J. 1998;17: 4780–4789. 9707437
37. Anderson J, Phan L, Hinnebusch AG. The Gcd10p/Gcd14p complex is the essential two-subunit tRNA(1-methyladenosine) methyltransferase of Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2000;97: 5173–5178. 10779558
38. Jackman JE, Montange RK, Malik HS, Phizicky EM. Identification of the yeast gene encoding the tRNA m1G methyltransferase responsible for modification at position 9. RNA. 2003;9: 574–585. 12702816
39. Yan S, Dong X. Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol. 2014;20: 64–68. doi: 10.1016/j.pbi.2014.04.006 24840293
40. Pajerowska-Mukhtar KM, Wang W, Tada Y, Oka N, Tucker C, Fonseca JP, et al. The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Curr Biol. 2012;22:103–112. doi: 10.1016/j.cub.2011.12.015 22244999
41. Chan CT, Dyavaiah M, DeMott MS, Taghizadeh K, Dedon PC, Begley TJ. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet. 2010;6: e1001247. doi: 10.1371/journal.pgen.1001247 21187895
42. Wang X, He C. Dynamic RNA modifications in posttranscriptional regulation. Mol Cell. 2014;56: 5–12. doi: 10.1016/j.molcel.2014.09.001 25280100
43. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, Young CM, et al. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell. 2007;28: 860–870. 18082610
44. Chan CT, Pang YL, Deng W, Babu IR, Dyavaiah M, Begley TJ, et al. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun. 2012;3: 937. doi: 10.1038/ncomms1938 22760636
45. Mauro VP, Edelman GM. The ribosome filter redux. Cell Cycle. 2007;6: 2246–2251. 17890902
46. Yewdell JW, Antón LC, Bennink JR. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J Immunol. 1996;157: 1823–1826. 8757297
47. Lapin D, Van den Ackerveken G. Susceptibility to plant disease: more than a failure of host immunity. Trends Plant Sci. 2013;18: 546–554. doi: 10.1016/j.tplants.2013.05.005 23790254
48. Lu J, Huang B, Esberg A, Johansson MJ, Byström AS. The Kluyveromyces lactis γ-toxin targets tRNA anticodons. RNA. 2005;11: 1648–1654. 16244131
49. Kadaba S, Krueger A, Trice T, Krecic AM, Hinnebusch AG, Anderson J. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 2004;18: 1227–1240. 15145828
50. Motorin Y, Helm M. tRNA stabilization by modified nucleotides. Biochemistry. 2010;49: 4934–4944. doi: 10.1021/bi100408z 20459084
51. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev. 2009;23: 2639–2649. doi: 10.1101/gad.1837609 19933153
52. Pederson T. Regulatory RNAs derived from transfer RNA? RNA. 2010;16: 1865–1869. doi: 10.1261/rna.2266510 20719919
53. Maute RL, Schneider C, Sumazin P, Holmes A, Califano A, Basso K, et al. tRNA-derived microRNA modulates prolifertion and the DNA damage response and is down-regulated in B cell lymphoma. Proc Natl Acad Sci USA. 2013;110: 1404–1409. doi: 10.1073/pnas.1206761110 23297232
54. Raina M, Ibba M. tRNAs as regulators of biological processes. Front Genet. 2014;5: 171. doi: 10.3389/fgene.2014.00171 24966867
55. Thompson DM, Lu C, Green PJ, Parker R. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA. 2008;14: 2095–2103. doi: 10.1261/rna.1232808 18719243
56. López A, Ramírez V, García-Andrade J, Flors V, Vera P. The RNA silencing enzyme RNA polymerase V is required for plant immunity. PLoS Genet. 2011;7: e1002434. doi: 10.1371/journal.pgen.1002434 22242006
57. García-Andrade J, Ramírez V, López A, Vera P. Mediated plastid RNA editing in plant immunity. PLoS Pathog. 2013;9: e1003713. doi: 10.1371/journal.ppat.1003713 24204264
58. Bell CJ, Ecker JR. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994;19: 137–144. 8188214
59. Castelló MJ, Carrasco JL, Navarrete-Gómez M, Daniel J, Granot D, Vera P. A plant small polypeptide is a novel component of DNA-binding protein phosphatase 1 (DBP1)-mediated resistance to Plum pox virus in Arabidopsis. Plant Physiol. 2011;157: 2206–2215. doi: 10.1104/pp.111.188953 22021419
60. Ramírez V, Van der Ent S, García-Andrade J, Coego A, Pieterse CM, Vera P. OCP3 is an important modulator of NPR1-mediated jasmonic acid-dependent induced defenses in Arabidopsis. BMC Plant Biol. 2010;10: 199. doi: 10.1186/1471-2229-10-199 20836879
61. Huang WE, Wang H, Zheng H, Huang L, Singer AC, Thompson I, et al. Chromosomally located gene fusions constructed in Acinetobacter sp. ADP1 for the detection of salicylate. Environ Microbiol. 2005;7: 1339–1348. 16104857
62. Defraia CT, Schmelz EA, Mou Z. A rapid biosensor-based method for quantification of free and glucose-conjugated salicylic acid. Plant Methods. 2008;4: 28. doi: 10.1186/1746-4811-4-28 19117519
63. Coego A, Ramírez V, Ellul P, Mayda E, Vera P. The H2O2-regulated Ep5C gene encodes a peroxidase required for bacterial speck susceptibility in tomato. Plant J. 2005;42: 283–293. 15807789
64. Garcia-Andrade J, Ramirez V, Flors V, Vera P. Arabidopsis ocp3 mutant reveals a potentiation mechanism linking ABA and JA for pathogen-induced callose deposition. Plant J. 2011;67: 783–794. doi: 10.1111/j.1365-313X.2011.04633.x 21564353
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 10
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Single Strand Annealing Plays a Major Role in RecA-Independent Recombination between Repeated Sequences in the Radioresistant Bacterium
- The Rise and Fall of an Evolutionary Innovation: Contrasting Strategies of Venom Evolution in Ancient and Young Animals
- Genome Wide Identification of SARS-CoV Susceptibility Loci Using the Collaborative Cross
- DCA1 Acts as a Transcriptional Co-activator of DST and Contributes to Drought and Salt Tolerance in Rice