Conservation of tRNA and rRNA 5-methylcytosine in the kingdom Plantae

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Burgess, Alice Louise ^a   David, Rakesh ^a   Searle, Iain Robert ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Arabidopsis thaliana; DNMT2; Non coding RNA; NOP2; NSUN5; Ribosomal RNA (rRNA); RNA 5 methylcytosine; Transfer RNA (tRNA); TRDMT1; TRM4

Indexed keywords

ALGAE; ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA RAPA; CAULERPA TAXIFOLIA; EMBRYOPHYTA; EUKARYOTA; GINKGO BILOBA; NANNOCHLOROPSIS OCULATA; PLANTAE; PROKARYOTA; TRITICUM TURGIDUM SUBSP. DURUM;

5 METHYLCYTOSINE; METHYLTRANSFERASE; TRANSCRIPTOME; TRANSFER RNA; UNTRANSLATED RNA;

CELL NUCLEUS; CHLOROPLAST; GENETICS; METABOLISM; METHYLATION; MITOCHONDRION; MOLECULAR EVOLUTION; PHYLOGENY; PLANT;

5-METHYLCYTOSINE; CELL NUCLEUS; CHLOROPLASTS; EVOLUTION, MOLECULAR; METHYLATION; METHYLTRANSFERASES; MITOCHONDRIA; PHYLOGENY; PLANTS; RNA, TRANSFER; RNA, UNTRANSLATED; TRANSCRIPTOME;

EID: 84939191187     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0580-8     Document Type: Article

References (73)

1. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet. 2008;9:465-76.
2. Motorin Y, Lyko F, Helm M. 5-methylcytosine in RNA: detection, enzymatic formation and biological functions. Nucleic Acids Res. 2010;38:1415-30.
3. Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R. Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs. PLoS Genet. 2013;9, e1003602.
4. Jackman JE, Alfonzo JD. Transfer RNA modifications: nature's combinatorial chemistry playground. Wires RNA. 2013;4:35-48.
5. Motorin Y, Helm M. tRNA Stabilization by modified nucleotides. Biochemistry. 2010;49:4934-44.
6. Alexandrov A, Chernyakov I, Gu WF, Hiley SL, Hughes TR, Grayhack EJ, et al. Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell. 2006;21:87-96.
7. Agris PF. Bringing order to translation: the contributions of transfer RNA anticodon-domain modifications. EMBO Rep. 2008;9:629-35.
8. Helm M. Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res. 2006;34:721-33.
9. 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.
10. Chan CTY, Pang YLJ, Deng WJ, 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.
11. Tuorto F, Liebers R, Musch T, Schaefer M, Hofmann S, Kellner S, et al. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol. 2012;19:900-5.
12. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, et al. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev. 2010;24:1590-5.
13. Gigova A, Duggimpudi S, Pollex T, Schaefer M, Kos M. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability. RNA. 2014;20:1632-44.
14. Hong B, Brockenbrough JS, Wu P, Aris JP. Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast. Mol Cell Biol. 1997;17:378-88.
15. Sharma S, Yang J, Watzinger P, Kotter P, Entian KD. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res. 2013;41:9062-76.
16. Motorin Y, Grosjean H. Multisite-specific tRNA: m(5)C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: Identification of the gene and substrate specificity of the enzyme. RNA. 1999;5:1105-18.
17. Auxilien S, Guerineau V, Szweykowska-Kulinska Z, Golinelli-Pimpaneau B. The Human tRNA m(5)C methyltransferase Misu is multisite-specific. RNA Biol. 2012;9:1331-8.
18. Blanco S, Dietmann S, Flores JV, Hussain S, Kutter C, Humphreys P, et al. Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders. EMBO J. 2014;33:2020-39.
19. Khan MA, Rafiq MA, Noor A, Hussain S, Flores JV, Rupp V, et al. Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability. Am J Hum Genet. 2012;90:856-63.
20. Abbasi-Moheb L, Mertel S, Gonsior M, Nouri-Vahid L, Kahrizi K, Cirak S, et al. Mutations in NSUN2 cause autosomal-recessive intellectual disability. Am J Hum Genet. 2012;90:847-55.
21. Martinez FJ, Lee JH, Lee JE, Blanco S, Nickerson E, Gabriel S, et al. Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome. Journal of Medical Genetics. 2012;49:380-5.
22. Fahiminiya S, Almuriekhi M, Nawaz Z, Staffa A, Lepage P, Ali R, et al. Whole exome sequencing unravels disease-causing genes in consanguineous families in Qatar. Clin Genet. 2014;86:134-41.
23. Blanco S, Kurowski A, Nichols J, Watt FM, Benitah SA, Frye M. The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet. 2011;7, e1002403.
24. Hussain S, Tuorto F, Menon S, Blanco S, Cox C, Flores JV, et al. The mouse cytosine-5 RNA methyltransferase NSun2 is a component of the chromatoid body and required for testis differentiation. Mol Cell Biol. 2013;33:1561-70.
25. Pavlopoulou A, Kossida S. Phylogenetic analysis of the eukaryotic RNA (cytosine-5)-methyltransferases. Genomics. 2009;93:350-7.
26. Chen P, Jager G, Zheng B. Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana. BMC Plant Biol. 2010;10:201.
27. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang XY, et al. Methylation of tRNA(AsP) by the DNA methyltransferase homolog Dnmt2. Science. 2006;311:395-8.
28. Rai K, Chidester S, Zavala CV, Manos EJ, James SR, Karpf AR, et al. Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebrafish. Genes Dev. 2007;21:261-6.
29. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, et al. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res. 2012;40:5023-33.
30. Khoddami V, Cairns BR. Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol. 2013;31:458-64.
31. Hussain S, Sajini AA, Blanco S, Dietmann S, Lombard P, Sugimoto Y, et al. NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep. 2013;4:255-61.
32. Suzuki T, Suzuki T. A complete landscape of post-transcriptional modifications in mammalian mitochondrial tRNAs. Nucleic Acids Res. 2014;42:7346-57.
33. Sugiura M, Hirose T, Sugita M. Evolution and mechanism of translation in chloroplasts. Annu Rev Genet. 1998;32:437-59.
34. Granneman S, Baserga SJ. Ribosome biogenesis: of knobs and RNA processing. Exp Cell Res. 2004;296:43-50.
35. Lindahl L, Zengel JM. Ribosomal genes in Escherichia coli. Annu Rev Genet. 1986;20:297-326.
36. Maden BE. Locations of methyl groups in 28 S rRNA of Xenopus laevis and man. Clustering in the conserved core of molecule. J Mol Biol. 1988;201:289-314.
37. Purta E, O'Connor M, Bujnicki JM, Douthwaite S. YccW is the m5C methyltransferase specific for 23S rRNA nucleotide 1962. J Mol Biol. 2008;383:641-51.
38. Gu XR, Gustafsson C, Ku J, Yu M, Santi DV. Identification of the 16S rRNA m5C967 methyltransferase from Escherichia coli. Biochemistry. 1999;38:4053-7.
39. Andersen NM, Douthwaite S. YebU is a m5C methyltransferase specific for 16 S rRNA nucleotide 1407. J Mol Biol. 2006;359:777-86.
40. Baer RJ, Dubin DT. Methylated regions of hamster mitochondrial ribosomal RNA: structural and functional correlates. Nucleic Acids Res. 1981;9:323-37.
41. Metodiev MD, Spahr H, Loguercio Polosa P, Meharg C, Becker C, Altmueller J, et al. NSUN4 is a dual function mitochondrial protein required for both methylation of 12S rRNA and coordination of mitoribosomal assembly. PLoS Genet. 2014;10, e1004110.
42. Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H. Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J. 2009;59:499-508.
43. Hebrard C, Trap-Gentil MV, Lafon-Placette C, Delaunay A, Joseph C, Lefebvre M, et al. Identification of differentially methylated regions during vernalization revealed a role for RNA methyltransferases in bolting. J Exp Bot. 2013;64:651-63.
44. Duchene AM, Pujol C, Marechal-Drouard L. Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet. 2009;55:1-18.
45. Marechaldrouard L, Weil JH, Dietrich A. Transfer-Rnas and Transfer-Rna Genes in Plants. Annu Rev Plant Phys. 1993;44:13-32.
46. Adams KL, Palmer JD. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol. 2003;29:380-95.
47. Michaud M, Cognat V, Duchene AM, Marechal-Drouard L. A global picture of tRNA genes in plant genomes. Plant J. 2011;66:80-93.
48. Yukawa Y, Mizutani T, Akama K, Sugiura M. A survey of expressed tRNA genes in the chromosome I of Arabidopsis using an RNA polymerase III-dependent in vitro transcription system. Gene. 2007;392:7-13.
49. Cognat V, Pawlak G, Duchene AM, Daujat M, Gigant A, Salinas T, et al. PlantRNA, a database for tRNAs of photosynthetic eukaryotes. Nucleic Acids Res. 2013;41:D273-279.
50. Zhou W, Karcher D, Fischer A, Maximova E, Walther D, Bock R. Multiple RNA processing defects and impaired chloroplast function in plants deficient in the organellar protein-only RNase P enzyme. PLoS One. 2015;10, e0120533.
51. Schaefer M, Pollex T, Hanna K, Lyko F. RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res. 2009;37, e12.
52. Bujnicki JM, Feder M, Ayres CL, Redman KL. Sequence-structure-function studies of tRNA: m(5)C methyltransferase Trm4p and its relationship to DNA: m(5)C and RNA: m(5)U methyltransferases. Nucleic Acids Res. 2004;32:2453-63.
53. Borovinskaya MA, Shoji S, Fredrick K, Cate JHD. Structural basis for hygromycin B inhibition of protein biosynthesis. RNA. 2008;14:1590-9.
54. King MY, Redman KL. RNA methyltransferases utilize two cysteine residues in the formation of 5-methylcytosine. Biochemistry. 2002;41:11218-25.
55. Liu YQ. Santi DV: m(5)C RNA and m(5)C DNA methyl transferases use different cysteine residues as catalysts. Proc Natl Acad Sci. 2000;97:8263-5.
56. Foster PG, Nunes CR, Greene P, Moustakas D, Stroud RM. The first structure of an RNA m(5)C methyltransferase, Fmu, provides insight into catalytic mechanism and specific binding of RNA substrate. Structure. 2003;11:1609-20.
57. Zhang SD, Sun L, Kragler F. The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation. Plant Physiol. 2009;150:378-87.
58. Loss-Morais G, Waterhouse PM, Margis R. Description of plant tRNA-derived RNA fragments (tRFs) associated with argonaute and identification of their putative targets. Biol Direct. 2013;8.
59. Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA. 2010;16:673-95.
60. Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, et al. Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol. 2011;8:158-77.
61. Sobala A, Hutvagner G. Small RNAs derived from the 5 end of tRNA can inhibit protein translation in human cells. RNA Biol. 2013;10:553-63.
62. Gray MW, Burger G, Lang BF. Mitochondrial evolution. Science. 1999;283:1476-81.
63. Rodriguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Loffelhardt W, et al. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol. 2005;15:1325-30.
64. Suzuki T, Nagao A, Suzuki T. Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu Rev Genet. 2011;45:299-329.
65. Wu P, Brockenbrough JS, Paddy MR, Aris JP. NCL1, a novel gene for a non-essential nuclear protein in Saccharomyces cerevisiae. Gene. 1998;220:109-17.
66. Merret R, Nagarajan VK, Carpentier MC, Park S, Favory JJ, Descombin J, et al. Heat-induced ribosome pausing triggers mRNA co-translational decay in Arabidopsis thaliana. Nucleic Acids Res. 2015;43:4121-32.
67. King M, Ton D, Redman KL. A conserved motif in the yeast nucleolar protein Nop2p contains an essential cysteine residue. Biochem J. 1999;337(Pt 1):29-35.
68. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012;40:D1202-1210.
69. Sprinzl M, Horn C, Brown M, Ioudovitch A, Steinberg S. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1998;26:148-53.
70. R Core Team. R: A language and environment for statistical computing. R version 3.1.0 edition. Vienna, Austria: R Foundation for Statistical Computing; 2014.
71. Kolde R. pheatmap: Pretty Heatmaps. R package version 0.7.7 edition; 2013.
72. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, et al. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 2010;38:W695-699.
73. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, et al. Genome-wide Insertional mutagenesis of Arabidopsis thaliana. Science. 2003;5633:653-7.