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Disrupted tRNA Genes and tRNA Fragments: A Perspective on tRNA Gene Evolution.

Kanai A - Life (Basel) (2015)

Bottom Line: Even tRNA molecules themselves are fragmented post-transcriptionally in many species.These fragmented small RNAs are known as tRNA-derived fragments (tRFs).In this review, I summarize the progress of research into the disrupted tRNA genes and the tRFs, and propose a possible model for the molecular evolution of tRNAs based on the concept of the combination of fragmented tRNA halves.

View Article: PubMed Central - PubMed

Affiliation: Institute for Advanced Biosciences, Keio University, Tsuruoka 997-0017, Japan. akio@sfc.keio.ac.jp.

ABSTRACT
Transfer RNAs (tRNAs) are small non-coding RNAs with lengths of approximately 70-100 nt. They are directly involved in protein synthesis by carrying amino acids to the ribosome. In this sense, tRNAs are key molecules that connect the RNA world and the protein world. Thus, study of the evolution of tRNA molecules may reveal the processes that led to the establishment of the central dogma: genetic information flows from DNA to RNA to protein. Thanks to the development of DNA sequencers in this century, we have determined a huge number of nucleotide sequences from complete genomes as well as from transcriptomes in many species. Recent analyses of these large data sets have shown that particular tRNA genes, especially in Archaea, are disrupted in unique ways: some tRNA genes contain multiple introns and some are split genes. Even tRNA molecules themselves are fragmented post-transcriptionally in many species. These fragmented small RNAs are known as tRNA-derived fragments (tRFs). In this review, I summarize the progress of research into the disrupted tRNA genes and the tRFs, and propose a possible model for the molecular evolution of tRNAs based on the concept of the combination of fragmented tRNA halves.

No MeSH data available.


Split tRNAs. (A) Gene structure, primary transcripts, and precursors of split tRNAs. Exonic regions are colored in either black (5' half) or pink (3' half). Leader sequences are shown in grey. (B) Gene structures, primary transcripts, and precursors of tri-split tRNAs. Exonic regions are colored in either green (5' quarter), orange (anticodon loop), or pink (3' half). The secondary structures (BHB motifs) formed by the pairing of each leader sequence have been omitted from these cartoons for clarity.
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life-05-00321-f002: Split tRNAs. (A) Gene structure, primary transcripts, and precursors of split tRNAs. Exonic regions are colored in either black (5' half) or pink (3' half). Leader sequences are shown in grey. (B) Gene structures, primary transcripts, and precursors of tri-split tRNAs. Exonic regions are colored in either green (5' quarter), orange (anticodon loop), or pink (3' half). The secondary structures (BHB motifs) formed by the pairing of each leader sequence have been omitted from these cartoons for clarity.

Mentions: In 2005, Randau et al. reported that the hyperthermophilic archaeon Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5' and 3' halves (Figure 2A). This was the first report of “split tRNAs” [2], and a total of six tRNA genes (tRNAiMet[CAU], tRNAHis[GUG], tRNALys[CUU], tRNAGln[UUG], tRNAGlu[CUC], and tRNAGlu[UUC]) are generated by the combination of two tRNA halves [5]. It is noteworthy that two split tRNAs, tRNAGlu(CUC) and tRNAGlu(UUC), share the same 3' tRNA half-transcript. An RNA-seq study of the tRNA half-precursors in this organism supported the trans splicing of these tRNAs [18]. Because N. equitans is a parasite, with evidence of massive genomic reduction [19], it was unclear whether its tRNAs represented a form of tRNA that was unique to particular archaeal species or whether they were a later product of its genomic reduction. In 2009, we reported split tRNA genes [3] in a free-living organism, the hyperthermoacidophilic archaeon Caldivirga maquilingensis, which belongs to the deep-branching archaeal order Thermoproteales and was isolated from an acidic hot spring in the Philippines. In this case, four split tRNAs, tRNAGly(CCC), tRNAGlu(UUC), tRNAAla(CGC), and tRNAAla(UGC), are generated by the combination of tRNA halves. Interestingly, two tRNAs, tRNAAla(CGC) and tRNAAla(UGC), share the same 5' tRNA half-transcript. Recently, split tRNAs have also been found in several different species of the Desulfurococcales branch of the Crenarchaeota: tRNAAsp(GUC) in Aeropyrum pernix and Thermosphaera aggregans, and tRNALys(CUU) in Staphylothermus hellenicus and S. marinus [4]. These observations suggest that split tRNA genes have spread sporadically across a major branch of the Archaea [20]. It should be mentioned that split tRNAs and intron-containing tRNAs share a common BHB motif around their intron/leader-exon boundaries, which can be cleaved by the same tRNA splicing endonuclease [3,21]. We have also demonstrated that the intervening nucleotide sequences of split tRNAs display high identity to the tRNA intron sequences located at the same positions in intron-containing tRNAs in related archaeal species [3]. These observations suggest an evolutionary relationship between these disrupted tRNAs.


Disrupted tRNA Genes and tRNA Fragments: A Perspective on tRNA Gene Evolution.

Kanai A - Life (Basel) (2015)

Split tRNAs. (A) Gene structure, primary transcripts, and precursors of split tRNAs. Exonic regions are colored in either black (5' half) or pink (3' half). Leader sequences are shown in grey. (B) Gene structures, primary transcripts, and precursors of tri-split tRNAs. Exonic regions are colored in either green (5' quarter), orange (anticodon loop), or pink (3' half). The secondary structures (BHB motifs) formed by the pairing of each leader sequence have been omitted from these cartoons for clarity.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390854&req=5

life-05-00321-f002: Split tRNAs. (A) Gene structure, primary transcripts, and precursors of split tRNAs. Exonic regions are colored in either black (5' half) or pink (3' half). Leader sequences are shown in grey. (B) Gene structures, primary transcripts, and precursors of tri-split tRNAs. Exonic regions are colored in either green (5' quarter), orange (anticodon loop), or pink (3' half). The secondary structures (BHB motifs) formed by the pairing of each leader sequence have been omitted from these cartoons for clarity.
Mentions: In 2005, Randau et al. reported that the hyperthermophilic archaeon Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5' and 3' halves (Figure 2A). This was the first report of “split tRNAs” [2], and a total of six tRNA genes (tRNAiMet[CAU], tRNAHis[GUG], tRNALys[CUU], tRNAGln[UUG], tRNAGlu[CUC], and tRNAGlu[UUC]) are generated by the combination of two tRNA halves [5]. It is noteworthy that two split tRNAs, tRNAGlu(CUC) and tRNAGlu(UUC), share the same 3' tRNA half-transcript. An RNA-seq study of the tRNA half-precursors in this organism supported the trans splicing of these tRNAs [18]. Because N. equitans is a parasite, with evidence of massive genomic reduction [19], it was unclear whether its tRNAs represented a form of tRNA that was unique to particular archaeal species or whether they were a later product of its genomic reduction. In 2009, we reported split tRNA genes [3] in a free-living organism, the hyperthermoacidophilic archaeon Caldivirga maquilingensis, which belongs to the deep-branching archaeal order Thermoproteales and was isolated from an acidic hot spring in the Philippines. In this case, four split tRNAs, tRNAGly(CCC), tRNAGlu(UUC), tRNAAla(CGC), and tRNAAla(UGC), are generated by the combination of tRNA halves. Interestingly, two tRNAs, tRNAAla(CGC) and tRNAAla(UGC), share the same 5' tRNA half-transcript. Recently, split tRNAs have also been found in several different species of the Desulfurococcales branch of the Crenarchaeota: tRNAAsp(GUC) in Aeropyrum pernix and Thermosphaera aggregans, and tRNALys(CUU) in Staphylothermus hellenicus and S. marinus [4]. These observations suggest that split tRNA genes have spread sporadically across a major branch of the Archaea [20]. It should be mentioned that split tRNAs and intron-containing tRNAs share a common BHB motif around their intron/leader-exon boundaries, which can be cleaved by the same tRNA splicing endonuclease [3,21]. We have also demonstrated that the intervening nucleotide sequences of split tRNAs display high identity to the tRNA intron sequences located at the same positions in intron-containing tRNAs in related archaeal species [3]. These observations suggest an evolutionary relationship between these disrupted tRNAs.

Bottom Line: Even tRNA molecules themselves are fragmented post-transcriptionally in many species.These fragmented small RNAs are known as tRNA-derived fragments (tRFs).In this review, I summarize the progress of research into the disrupted tRNA genes and the tRFs, and propose a possible model for the molecular evolution of tRNAs based on the concept of the combination of fragmented tRNA halves.

View Article: PubMed Central - PubMed

Affiliation: Institute for Advanced Biosciences, Keio University, Tsuruoka 997-0017, Japan. akio@sfc.keio.ac.jp.

ABSTRACT
Transfer RNAs (tRNAs) are small non-coding RNAs with lengths of approximately 70-100 nt. They are directly involved in protein synthesis by carrying amino acids to the ribosome. In this sense, tRNAs are key molecules that connect the RNA world and the protein world. Thus, study of the evolution of tRNA molecules may reveal the processes that led to the establishment of the central dogma: genetic information flows from DNA to RNA to protein. Thanks to the development of DNA sequencers in this century, we have determined a huge number of nucleotide sequences from complete genomes as well as from transcriptomes in many species. Recent analyses of these large data sets have shown that particular tRNA genes, especially in Archaea, are disrupted in unique ways: some tRNA genes contain multiple introns and some are split genes. Even tRNA molecules themselves are fragmented post-transcriptionally in many species. These fragmented small RNAs are known as tRNA-derived fragments (tRFs). In this review, I summarize the progress of research into the disrupted tRNA genes and the tRFs, and propose a possible model for the molecular evolution of tRNAs based on the concept of the combination of fragmented tRNA halves.

No MeSH data available.