Large-scale tRNA intron transposition in the archaeal order Thermoproteales represents a novel mechanism of intron gain

Molecular Biology and Evolution

Volumn 27, Issue 10, 2010, Pages 2233-2243

  Fujishima, Kosuke ^a   Sugahara, Junichi ^a   Tomita, Masaru ^a   Kanai, Akio ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Archaea; Thermoproteales; transposition; tRNA intron

Indexed keywords

AMINO ACID; TRANSFER RNA;

ARTICLE; BACTERIAL GENE; CALDIVIRGA MAQUILINGENSIS; DNA TRANSPOSITION; INTRON; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PYROBACULUM AEROPHILUM; PYROBACULUM ARSENATICUM; PYROBACULUM CALIDIFONTIS; PYROBACULUM ISLANDICUM; RNA SEQUENCE; RNA STRUCTURE; THERMOPROTEALES; THERMOPROTEUS NEUTROPHLIUS; THERMOPROTEUS PENDENS;

BASE SEQUENCE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE REARRANGEMENT; INTRONS; PHYLOGENY; RNA, TRANSFER; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; THERMOPROTEALES;

ARCHAEA; EUKARYOTA; THERMOPROTEALES;

EID: 77957232919     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq111     Document Type: Article

References (35)

1. Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 37:D93-D97.
2. Clouet-d'Orval B, Gaspin C, Mougin A. 2005. Two different mechanisms for tRNA ribose methylation in Archaea: a short survey. Biochimie 87:889-895.
3. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
4. 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.
5. Di Giulio M. 2008. Transfer RNA genes in pieces are an ancestral character. EMBO Rep. 9:820; author reply. 820-821.
6. Diener JL, Moore PB. 1998. Solution structure of a substrate for the archaeal pre-tRNA splicing endonucleases: the bulge-helix-bulge motif. Mol Cell. 1:883-894.
7. Fujishima K, Sugahara J, Kikuta K, Hirano R, Sato A, Tomita M, Kanai A. 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\USA. 106:2683-2687.
8. Fujishima K, Sugahara J, Tomita M, 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.
9. Heinemann IU, Soll D, Randau L. 2009. Transfer RNA processing in archaea: unusual pathways and enzymes. FEBS Lett. 584: 303-309.
10. Hong X, Scofield DG, Lynch M. 2006. Intron size, abundance, and distribution within untranslated regions of genes. Mol Biol Evol. 23:2392-2404.
11. Kawach O, Voss C, Wolff J, Hadfi K, Maier UG, Zauner S. 2005. Unique tRNA introns of an enslaved algal cell. Mol Biol Evol. 22:1694-1701.
12. Krupovic M, Bamford DH. 2008. Archaeal proviruses TKV4 and MVV extend the PRD1-adenovirus lineage to the phylum Euryarchaeota. Virology 375:292-300.
13. Larkin MA, Blackshields G, Brown NP, et al. (13 co-authors). 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
14. Letunic I, Bork P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
15. Li H, Trotta CR, Abelson J. 1998. Crystal structure and evolution of a transfer RNA splicing enzyme. Science 280:279-284.
16. Marck C, Grosjean H. 2002. tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8:1189-1232.
17. Marck C, Grosjean H. 2003. Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: evolutionary implications. RNA 9:1516-1531.
18. Maruyama S, Sugahara J, Kanai A, Nozaki H. 2010. Permuted tRNA genes in the nuclear and nucleomorph genomes of photosyn-thetic eukaryotes. Mol Biol Evol. 27:1070-1076.
19. Ortmann AC, Wiedenheft B, Douglas T, Young M. 2006. Hot crenarchaeal viruses reveal deep evolutionary connections. Nat Rev Microbiol. 4:520-528.
20. Randau L, Munch R, Hohn MJ, Jahn D, Soll D. 2005. Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5'-and 3'-halves. Nature 433:537-541.
21. Randau L, Soll D. 2008. Transfer RNA genes in pieces. EMBO Rep. 9:623-628.
22. Reinhold-Hurek B, Shub DA. 1992. Self-splicing introns in tRNA genes of widely divergent bacteria. Nature 357:173-176.
23. Roy SW, Gilbert W. 2006. The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet. 7:211-221.
24. Schneider KL, Pollard KS, Baertsch R, Pohl A, Lowe TM. 2006. The UCSC Archaeal Genome Browser. Nucleic Acids Res. 34:D407-D410.
25. Singh SK, Gurha P, Tran EJ, Maxwell ES, Gupta R. 2004. Sequential 2'-O-methylation of archaeal pre-tRNATrp nucleotides is guided by the intron-encoded but trans-acting box C/D ribonucleo-protein of pre-tRNA. J Biol Chem. 279:47661-47671.
26. Soma A, Onodera A, Sugahara J, Kanai A, Yachie N, Tomita M, Kawamura F, Sekine Y. 2007. Permuted tRNA genes expressed via a circular RNA intermediate in Cyanidioschyzon merolae. Science 318:450-453.
27. Sugahara J, Fujishima K, Morita K, Tomita M, Kanai A. 2009. Disrupted tRNA gene diversity and possible evolutionary scenarios. J Mol Evol. 69:497-504.
28. Sugahara J, Kikuta K, Fujishima K, Yachie N, Tomita M, 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.
29. Sugahara J, Yachie N, Sekine Y, Soma A, Matsui M, Tomita M, Kanai A. 2006. SPLITS: a new program for predicting split and intron-containing tRNA genes at the genome level. In Silico Biol. 6:411-418.
30. Tang TH, Rozhdestvensky TS, d'Orval BC, Bortolin ML, Huber H, Charpentier B, Branlant C, Bachellerie JP, Brosius J, Huttenhofer A. 2002. RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucleic Acids Res. 30:921-930.
31. Tocchini-Valentini GD, Fruscoloni P, Tocchini-Valentini GP. 2005. Coevolution of tRNA intron motifs and tRNA endonuclease architecture in Archaea. Proc Natl Acad Sci\USA. 102:15418-15422.
32. Tocchini-Valentini GD, Fruscoloni P, Tocchini-Valentini GP. 2007. The dawn of dominance by the mature domain in tRNA splicing. Proc Natl Acad Sci\USA. 104:12300-12305.
33. Xue S, Calvin K, Li H. 2006. RNA recognition and cleavage by a splicing endonuclease. Science 312:906-910.
34. Yoshinari S, Itoh T, Hallam SJ, DeLong EF, Yokobori S, Yamagishi A, Oshima T, Kita K, Watanabe Y. 2006. Archaeal pre-mRNA splicing: a connection to hetero-oligomeric splicing endonucle-ase. Biochem Biophys Res Commun. 346:1024-1032.
35. Yoshinari S, Shiba T, Inaoka DK, Itoh T, Kurisu G, Harada S, Kita K, Watanabe Y. 2009. Functional importance of crenarchaea-specific extra-loop revealed by an X-ray structure of a hetero-tetrameric crenarchaeal splicing endonuclease. Nucleic Acids Res. 37:4787-4798.