tRNA gene diversity in the three domains of life

Frontiers in Genetics

Volumn 5, Issue MAY, 2014, Pages

  Fujishima, Kosuke ^a,b   Kanai, Akio ^b  

^a NASA AMES RESEARCH CENTER   (United States)

^b KEIO UNIVERSITY   (Japan)

Author keywords

Armless tRNA; Co evolution; Intron containing tRNA; Nev tRNA; Permuted tRNA; RNA splicing endonuclease; Split tRNA

Indexed keywords

EID: 84905644629     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00142     Document Type: Review

References (81)

1. Abelson, J., Trotta, C. R., and Li, H. (1998). tRNA splicing. J. Biol. Chem. 273, 12685-12688. doi: 10.1074/jbc.273.21.12685
2. Andersen, G. R., Thirup, S., Spremulli, L. L., and Nyborg, J. (2000). High resolution crystal structure of bovine mitochondrial EF-tu in complex with GDP. J. Mol. Biol. 297, 421-436. doi: 10.1006/jmbi.2000.3564
3. Arita, M., Suematsu, T., Osanai, A., Inaba, T., Kamiya, H., Kita, K., et al. (2006). An evolutionary 'intermediate state' of mitochondrial translation systems found in Trichinella species of parasitic nematodes: co-evolution of tRNA and EF-Tu. Nucleic Acids Res. 34, 5291-5299. doi: 10.1093/nar/gkl526
4. Boore, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767-1780. doi: 10.1093/nar/27.8.1767
5. Brennan, T., and Sundaralingam, M. (1976). Structure, of transfer RNA molecules containing the long variable loop. Nucleic Acids Res. 3, 3235-3252. doi: 10.1093/nar/3.11.3235
6. Calvin, K., and Li, H. (2008). RNA-splicing endonuclease structure and function. Cell. Mol. Life Sci. 65, 1176-1185. doi: 10.1007/s00018-008-7393-y
7. Chan, P. P., Cozen, A. E., and Lowe, T. M. (2011). Discovery of permuted and recently split transfer RNAs in Archaea. Genome Biol. 12:R38. doi: 10.1186/gb-2011-12-4-r38
8. Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R., and Embley, T. M. (2008). The archaebacterial origin of eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 105, 20356-20361. doi: 10.1073/pnas.0810647105
9. Di Giulio, M. (2006). The non-monophyletic origin of the tRNA molecule and the origin of genes only after the evolutionary stage of the last universal common ancestor (LUCA). J. Theor. Biol. 240, 343-352. doi: 10.1016/j.jtbi.2005.09.023
10. Di Giulio, M. (2009). Formal proof that the split genes of tRNAs of Nanoarchaeum equitans are an ancestral character. J. Mol. Evol. 69, 505-511. doi: 10.1007/s00239-009-9280-z
11. Di Giulio, M. (2012). The 'recently' split transfer RNA genes may be close to merging the two halves of the tRNA rather than having just separated them. J. Theor. Biol. 310, 1-2. doi: 10.1016/j.jtbi.2012.06.022
12. Dreher, T. W. (2009). Role of tRNA-like structures in controlling plant virus replication. Virus Res. 139, 217-229. doi: 10.1016/j.virusres.2008.06.010
13. Dreher, T. W. (2010). Viral tRNAs and tRNA-like structures. Wiley Interdiscip. Rev. RNA 1, 402-414. doi: 10.1002/wrna.42
14. Francklyn, C., and Schimmel, P. (1989). Aminoacylation of RNA minihelices with alanine. Nature 337, 478-481. doi: 10.1038/337478a0
15. Francklyn, C., and Schimmel, P. (1990). Enzymatic aminoacylation of an eight-base-pair microhelix with histidine. Proc. Natl. Acad. Sci. U.S.A. 87, 8655-8659. doi: 10.1073/pnas.87.21.8655
16. Fujishima, K., Sugahara, J., Kikuta, K., Hirano, R., Sato, A., Tomita, M., et al. (2009). Tri-split tRNA is a transfer RNA made from 3 transcripts that provides insight into the evolution of fragmented tRNAs in archaea. Proc. Natl. Acad. Sci. U.S.A. 106, 2683-2687. doi: 10.1073/pnas.0808246106
17. Fujishima, K., Sugahara, J., Miller, C. S., Baker, B. J., Di Giulio, M., Takesue, K., et al. (2011). A novel three-unit tRNA splicing endonuclease found in ultrasmall Archaea possesses broad substrate specificity. Nucleic Acids Res. 39, 9695-9704. doi: 10.1093/nar/gkr692
18. Fujishima, K., Sugahara, J., Tomita, M., and Kanai, A. (2008). Sequence evidence in the archaeal genomes that tRNAs emerged through the combination of ancestral genes as 5' and 3' tRNA halves. PLoS ONE 3:e1622. doi: 10.1371/journal.pone.0001622
19. Fujishima, K., Sugahara, J., Tomita, M., and Kanai, A. (2010). Large-scale tRNA intron transposition in the archaeal order Thermoproteales represents a novel mechanism of intron gain. Mol. Biol. Evol. 27, 2233-2243. doi: 10.1093/molbev/msq111
20. Gray, M. W. (2012). Mitochondrial evolution. Cold Spring Harb. Perspect. Biol. 4:a011403. doi: 10.1101/cshperspect.a011403
21. Hamashima, K., Fujishima, K., Masuda, T., Sugahara, J., Tomita, M., and Kanai, A. (2012). Nematode-specific tRNAs that decode an alternative genetic code for leucine. Nucleic Acids Res. 40, 3653-3662. doi: 10.1093/nar/gkr1226
22. Hamashima, K., and Kanai, A. (2013). Alternative genetic code for amino acids and transfer RNA revisited. Biomol. Concepts. 4, 309-318. doi: 10.1515/bmc-2013-0002
23. Haugen, P., Simon, D. M., and Bhattacharya, D. (2005). The natural history of group I introns. Trends Genet. 21, 111-119. doi: 10.1016/j.tig.2004.12.007
24. Hirata, A., Fujishima, K., Yamagami, R., Kawamura, T., Banfield, J. F., Kanai, A., et al. (2012). X-ray structure of the fourth type of archaeal tRNA splicing endonuclease: insights into the evolution of a novel three-unit composition and a unique loop involved in broad substrate specificity. Nucleic Acids Res. 40, 10554-10566. doi: 10.1093/nar/gks826
25. Hori, Y., Baba, H., Ueda, R., Tanaka, T., and Kikuchi, Y. (2000). In vitro hyperprocessing of Drosophila tRNAs by the catalytic RNA of RNase P the cloverleaf structure of tRNA is not always stable? Eur. J. Biochem. 267, 4781-4788. doi: 10.1046/j.1432-1327.2000.01534.x
26. Jühling, F., Mörl, M., Hartmann, R. K., Sprinzl, M., Stadler, P. F., and Pütz, J. (2009). tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res. 37, D159-D162. doi: 10.1093/nar/gkn772
27. Kanai, A. (2013). "Molecular evolution of disrupted transfer rna genes and their introns in archaea," in Evolutionary Biology: Exobiology and Evolutionary Mechanisms, ed P. Pontarotti (Berlin, Heidelberg: Springer), 181-193.
28. Knight, R. D., Freeland, S. J., and Landweber, L. F. (2001). Rewiring the keyboard: evolvability of the genetic code. Nat. Rev. Genet. 2, 49-58. doi: 10.1038/35047500
29. Lee, N., Bessho, Y., Wei, K., Szostak, J. W., and Suga, H. (2000). Ribozyme-catalyzed tRNA aminoacylation. Nat. Struct. Biol. 7, 28-33. doi: 10.1038/71225
30. Le Grice, S. F.J. (2003). 'In the Beginning': initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42, 14349-14355. doi: 10.1021/bi030201q
31. Li, H., and Abelson, J. (2000). Crystal structure of a dimeric archaeal splicing endonuclease. J. Mol. Biol. 302, 639-648. doi: 10.1006/jmbi.2000.3941
32. Li, H., Trotta, C. R., and Abelson, J. (1998). Crystal structure and evolution of a transfer RNA splicing enzyme. Science 280, 279-284. doi: 10.1126/science.280.5361.279
33. Lowe, T. M., and Eddy, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964. doi: 10.1093/nar/25.5.0955
34. Marck, C., and Grosjean, H. (2003). Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: evolutionary implications. RNA 9, 1516-1531. doi: 10.1261/rna.5132503
35. Maruyama, S., Sugahara, J., Kanai, A., and Nozaki, H. (2010). Permuted tRNA genes in the nuclear and nucleomorph genomes of photosynthetic eukaryotes. Mol. Biol. Evol. 27, 1070-1076. doi: 10.1093/molbev/msp313
36. Masta, S. E., and Boore, J. L. (2008). Parallel evolution of truncated transfer RNA genes in arachnid mitochondrial genomes. Mol. Biol. Evol. 25, 949-959. doi: 10.1093/molbev/msn051
37. Ohtsuki, T., Kawai, G., and Watanabe, K. (2002). The minimal tRNA: unique structure of Ascaris suum mitochondrial tRNA(Ser)(UCU) having a short T arm and lacking the entire D arm. FEBS Lett. 514, 37-43. doi: 10.1016/S0014-5793(02)02328-1
38. Ohtsuki, T., and Watanabe, Y.-I. (2007). T-armless tRNAs and elongated elongation factor Tu. IUBMB Life 59, 68-75. doi: 10.1080/15216540701218722
39. Okimoto, R., and Wolstenholme, D. R. (1990). A set of tRNAs that lack either the T psi C arm or the dihydrouridine arm: towards a minimal tRNA adaptor. EMBO J. 9, 3405-3411.
40. Paecht-Horowitz, M., and Katchalsky, A. (1973). Synthesis of amino acyl-adenylates under prebiotic conditions. J. Mol. Evol. 2, 91-98. doi: 10.1007/BF01653989
41. Paquin, B., Kathe, S. D., Nierzwicki-Bauer, S. A., and Shub, D. A. (1997). Origin and evolution of group I introns in cyanobacterial tRNA genes. J. Bacteriol. 179, 6798-6806.
42. Pleij, C. W., Rietveld, K., and Bosch, L. (1985). A new principle of RNA folding based on pseudoknotting. Nucleic Acids Res. 13, 1717-1731. doi: 10.1093/nar/13.5.1717
43. Podar, M., Makarova, K. S., Graham, D. E., Wolf, Y. I., Koonin, E. V., and Reysenbach, A.-L. (2013). Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol. Direct 8:9. doi: 10.1186/1745-6150-8-9
44. Randau, L., Calvin, K., Hall, M., Yuan, J., Podar, M., Li, H., et al. (2005c). The heteromeric Nanoarchaeum equitans splicing endonuclease cleaves noncanonical bulge-helix-bulge motifs of joined tRNA halves. Proc. Natl. Acad. Sci. U.S.A. 102, 17934-17939. doi: 10.1073/pnas.0509197102
45. Randau, L., Münch, R., Hohn, M. J., Jahn, D., and Söll, D. (2005a). Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5'- and 3'-halves. Nature 433, 537-541. doi: 10.1038/nature03233
46. Randau, L., Pearson, M., and Söll, D. (2005b). The complete set of tRNA species in Nanoarchaeum equitans. FEBS Lett. 579, 2945-2947. doi: 10.1016/j.febslet.2005.04.051
47. Randau, L., and Söll, D. (2008). Transfer RNA genes in pieces. EMBO Rep. 9, 623-628. doi: 10.1038/embor.2008.101
48. Reinhold-Hurek, B., and Shub, D. A. (1992). Self-splicing introns in tRNA genes of widely divergent bacteria. Nature 357, 173-176. doi: 10.1038/357173a0
49. Reyes, V. M., and Abelson, J. (1988). Substrate recognition and splice site determination in yeast tRNA splicing. Cell 55, 719-730. doi: 10.1016/0092-8674(88)90230-9
50. Rogers, H. H., and Griffiths-Jones, S. (2014). tRNA anticodon shifts in eukaryotic genomes. RNA 20, 269-281. doi: 10.1261/rna.041681.113
51. Salinas, T., Duby, F., Larosa, V., Coosemans, N., Bonnefoy, N., Motte, P., et al. (2012). Co-evolution of mitochondrial tRNA import and codon usage determines translational efficiency in the green alga chlamydomonas. PLoS Genet. 8:e1002946. doi: 10.1371/journal.pgen.1002946
52. Schimmel, P., Giegé, R., Moras, D., and Yokoyama, S. (1993). An operational RNA code for amino acids and possible relationship to genetic code. Proc. Natl. Acad. Sci. U.S.A. 90, 8763-8768. doi: 10.1073/pnas.90.19.8763
53. Schimmel, P., and Ribas de Pouplana, L. (1995). Transfer RNA: from minihelix to genetic code. Cell 81, 983-986. doi: 10.1016/S0092-8674(05)80002-9
54. Soma, A., Onodera, A., Sugahara, J., Kanai, A., Yachie, N., Tomita, M., et al. (2007). Permuted tRNA genes expressed via a circular RNA intermediate in Cyanidioschyzon merolae. Science 318, 450-453. doi: 10.1126/science.1145718
55. Soma, A., Sugahara, J., Onodera, A., Yachie, N., Kanai, A., Watanabe, S., et al. (2013). Identification of highly-disrupted tRNA genes in nuclear genome of the red alga, Cyanidioschyzon merolae 10D. Sci. Rep. 3:2321. doi: 10.1038/srep02321
56. Song, J., and Markley, J. L. (2007). Three-dimensional structure determined for a subunit of human tRNA splicing endonuclease (Sen15) reveals a novel dimeric fold. J. Mol. Biol. 366, 155-164. doi: 10.1016/j.jmb.2006.11.024
57. Sugahara, J., Fujishima, K., Morita, K., Tomita, M., and Kanai, A. (2009). Disrupted tRNA gene diversity and possible evolutionary scenarios. J. Mol. Evol. 69, 497-504. doi: 10.1007/s00239-009-9294-6
58. Sugahara, J., Fujishima, K., Nunoura, T., Takaki, Y., Takami, H., Takai, K., et al. (2012). Genomic heterogeneity in a natural archaeal population suggests a model of tRNA gene disruption. PLoS ONE 7:e32504. doi: 10.1371/journal.pone.0032504
59. Sugahara, J., Kikuta, K., Fujishima, K., Yachie, N., Tomita, M., and Kanai, A. (2008). Comprehensive analysis of archaeal tRNA genes reveals rapid increase of tRNA introns in the order thermoproteales. Mol. Biol. Evol. 25, 2709-2716. doi: 10.1093/molbev/msn216
60. Sugahara, J., Yachie, N., Arakawa, K., and Tomita, M. (2007). In silico screening of archaeal tRNA-encoding genes having multiple introns with bulge-helix-bulge splicing motifs. RNA 13, 671-681. doi: 10.1261/rna.309507
61. Sugahara, J., Yachie, N., Sekine, Y., Soma, A., Matsui, M., Tomita, M., et al. (2006). SPLITS: a new program for predicting split and intron-containing tRNA genes at the genome level. In Silico Biol. (Gedrukt) 6, 411-418.
62. Sun, F.-J., and Caetano-Anollés, G. (2007). The origin and evolution of tRNA inferred from phylogenetic analysis of structure. J. Mol. Evol. 66, 21-35. doi: 10.1007/s00239-007-9050-8
63. Tamura, K., and Schimmel, P. (2004). Chiral-selective aminoacylation of an RNA minihelix. Science 305, 1253-1253. doi: 10.1126/science.1099141
64. Tanaka, T., and Kikuchi, Y. (2001). Origin of the cloverleaf shape of transfer RNA-the double-hairpin model: implication for the role of tRNA intron and the long extra loop. Viva Origino. 29, 134-142.
65. Tang, T. H., Rozhdestvensky, T. S., d'Orval, B. C., Bortolin, M.-L., Huber, H., Charpentier, B., et al. (2002). RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucleic Acids Res. 30, 921-930. doi: 10.1093/nar/30.4.921
66. Tanner, M., and Cech, T. (1996). Activity and thermostability of the small self-splicing group I intron in the pre-tRNA(lle) of the purple bacterium Azoarcus. RNA 2, 74-83.
67. Thompson, L. D., and Daniels, C. J. (1990). Recognition of exon-intron boundaries by the Halobacterium volcanii tRNA intron endonuclease. J. Biol. Chem. 265, 18104-18111.
68. Tocchini-Valentini, G., Saks, M. E., and Abelson, J. (2000). tRNA leucine identity and recognition sets. J. Mol. Biol. 298, 779-793. doi: 10.1006/jmbi.2000.3694
69. Tocchini-Valentini, G. D., Fruscoloni, P., and Tocchini-Valentini, G. P. (2005a). Coevolution of tRNA intron motifs and tRNA endonuclease architecture in Archaea. Proc. Natl. Acad. Sci. U.S.A. 102, 15418-15422. doi: 10.1073/pnas.0506750102
70. Tocchini-Valentini, G. D., Fruscoloni, P., and Tocchini-Valentini, G. P. (2005b). Structure, function, and evolution of the tRNA endonucleases of Archaea: an example of subfunctionalization. Proc. Natl. Acad. Sci. U.S.A. 102, 8933-8938. doi: 10.1073/pnas.0502350102
71. Tocchini-Valentini, G. D., and Tocchini-Valentini, G. P. (2012). Avatar pre-tRNAs help elucidate the properties of tRNA-splicing endonucleases that produce tRNA from permuted genes. Proc. Natl. Acad. Sci. U.S.A. 109, 21325-21329. doi: 10.1073/pnas.1219336110
72. Trotta, C. R., Miao, F., Arn, E. A., Stevens, S. W., Ho, C. K., Rauhut, R., et al. (1997). The yeast tRNA splicing endonuclease: a tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases. Cell 89, 849-858. doi: 10.1016/S0092-8674(00)80270-6
73. Turk, R. M., Chumachenko, N. V., and Yarus, M. (2010). Multiple translational products from a five-nucleotide ribozyme. Proc. Natl. Acad. Sci. U.S.A. 107, 4585-4589. doi: 10.1073/pnas.0912895107
74. Vogel, J., and Hess, W. R. (2001). Complete 5' and 3' end maturation of group II intron-containing tRNA precursors. RNA 7, 285-292. doi: 10.1017/S1355838201001960
75. Weiner, A. M., and Maizels, N. (1999). The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication, and clues regarding the origin of protein synthesis. Biol. Bull. 196, 327. doi: 10.2307/1542962
76. Widmann, J., Giulio, M. D., Yarus, M., and Knight, R. (2005). tRNA creation by hairpin duplication. J. Mol. Evol. 61, 524-530. doi: 10.1007/s00239-004-0315-1
77. Williams, T. A., Foster, P. G., Cox, C. J., and Embley, T. M. (2013). An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231-236. doi: 10.1038/nature12779
78. Wolf, Y. I., Aravind, L., Grishin, N. V., and Koonin, E. V. (1999). Evolution of aminoacyl-tRNA synthetases-analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 9, 689-710. doi: 10.1101/gr.9.8.689
79. Wuchty, S., Fontana, W., Hofacker, I. L., and Schuster, P. (1999). Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers 49, 145-165. doi: 10.1002/(SICI)1097-0282(199902)49:2<145::AID-BIP4>3.0.CO;2-G
80. Yokobori, S.-I., Itoh, T., Yoshinari, S., Nomura, N., Sako, Y., Yamagishi, A., et al. (2009). Gain and loss of an intron in a protein-coding gene in Archaea: the case of an archaeal RNA pseudouridine synthase gene. BMC Evol. Biol. 9:198. doi: 10.1186/1471-2148-9-198
81. Yoshinari, S., Shiba, T., Inaoka, D.-K., Itoh, T., Kurisu, G., Harada, S., et al. (2009). Functional importance of Crenarchaea-specific extra-loop revealed by an X-ray structure of a heterotetrameric crenarchaeal splicing endonuclease. Nucleic Acids Res. 37, 4787-4798. doi: 10.1093/nar/gkp506