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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.


Related in: MedlinePlus

Intron-containing transfer RNAs (tRNAs). (A) Molecular structures of disrupted tRNAs. Exons are indicated in red and introns in grey. (a) Common tRNA. A description of each stem and loop is included; (b) tRNA containing a single intron at the canonical position, 37/38; (c) An example of a tRNA containing a single intron at a non-canonical position; (d) Example of a tRNA containing multiple introns (up to three introns) at various positions. The two arrowheads indicate the exon-intron boundaries cleaved by the splicing endonuclease. (B) The three domains of life and tRNAs containing a single intron. A phylogenetic tree representing the separation of the Bacteria, Eukaryotes, and Archaea. LUCA, last universal common ancestor. Most introns are located in the anticodon loop region of the tRNAs. Note that the secondary structures of the eukaryotic and archaeal tRNA introns are very similar and that the introns of both are processed by a specific enzyme, the tRNA splicing endonuclease. By contrast, the bacterial tRNA intron is a self-splicing-type intron.
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life-05-00321-f001: Intron-containing transfer RNAs (tRNAs). (A) Molecular structures of disrupted tRNAs. Exons are indicated in red and introns in grey. (a) Common tRNA. A description of each stem and loop is included; (b) tRNA containing a single intron at the canonical position, 37/38; (c) An example of a tRNA containing a single intron at a non-canonical position; (d) Example of a tRNA containing multiple introns (up to three introns) at various positions. The two arrowheads indicate the exon-intron boundaries cleaved by the splicing endonuclease. (B) The three domains of life and tRNAs containing a single intron. A phylogenetic tree representing the separation of the Bacteria, Eukaryotes, and Archaea. LUCA, last universal common ancestor. Most introns are located in the anticodon loop region of the tRNAs. Note that the secondary structures of the eukaryotic and archaeal tRNA introns are very similar and that the introns of both are processed by a specific enzyme, the tRNA splicing endonuclease. By contrast, the bacterial tRNA intron is a self-splicing-type intron.

Mentions: The secondary structure of tRNA can be represented as a cloverleaf with four stems (Figure 1A-a). In some cases, tRNA genes are interrupted by intronic sequence(s) like eukaryotic protein-encoding genes. However, the introns in precursor tRNAs (pre-tRNAs) do not precisely resemble those in precursor mRNAs (pre-mRNAs). The eukaryotic pre-mRNA intron is recognized by base pairing to short RNA molecules such as U1, U2, U4, U5, and U6, whereas the pre-tRNA intron is recognized by a specific enzyme (complex), the tRNA splicing endonuclease [9,10]. Many of the pre-tRNA introns are found at a position adjacent to the anticodon, between nucleotides 37 and 38 of the precursor tRNA (37/38), known as the “canonical” position (Figure 1A-b). The tRNA intron forms a specific RNA secondary structure, the bulge-helix-bulge (BHB), with parts of the exon sequences [11], and this structure is the target of the tRNA splicing endonuclease (shown by arrowheads in Figure 1A) [12]. Using a systematic computational approach we found that some pre-tRNAs possess a single intron located at an unconventional site (Figure 1A-c), or even three introns (Figure 1A-d) in the Archaea, especially in the phylum Crenarchaeota. For example, pre-tRNAGlu(UUC) in Pyrobaculum calidifontis and pre-tRNAPro(UGG) in P. islandicum both contain three introns [1]. However, the evolutionary view is that introns at non-canonical positions are rare, whereas introns at canonical positions (or in the anticodon loop region) are conserved in the three domains of life, Bacteria, Archaea, and Eukaryota (Figure 1B) [13].


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

Kanai A - Life (Basel) (2015)

Intron-containing transfer RNAs (tRNAs). (A) Molecular structures of disrupted tRNAs. Exons are indicated in red and introns in grey. (a) Common tRNA. A description of each stem and loop is included; (b) tRNA containing a single intron at the canonical position, 37/38; (c) An example of a tRNA containing a single intron at a non-canonical position; (d) Example of a tRNA containing multiple introns (up to three introns) at various positions. The two arrowheads indicate the exon-intron boundaries cleaved by the splicing endonuclease. (B) The three domains of life and tRNAs containing a single intron. A phylogenetic tree representing the separation of the Bacteria, Eukaryotes, and Archaea. LUCA, last universal common ancestor. Most introns are located in the anticodon loop region of the tRNAs. Note that the secondary structures of the eukaryotic and archaeal tRNA introns are very similar and that the introns of both are processed by a specific enzyme, the tRNA splicing endonuclease. By contrast, the bacterial tRNA intron is a self-splicing-type intron.
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Related In: Results  -  Collection

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

life-05-00321-f001: Intron-containing transfer RNAs (tRNAs). (A) Molecular structures of disrupted tRNAs. Exons are indicated in red and introns in grey. (a) Common tRNA. A description of each stem and loop is included; (b) tRNA containing a single intron at the canonical position, 37/38; (c) An example of a tRNA containing a single intron at a non-canonical position; (d) Example of a tRNA containing multiple introns (up to three introns) at various positions. The two arrowheads indicate the exon-intron boundaries cleaved by the splicing endonuclease. (B) The three domains of life and tRNAs containing a single intron. A phylogenetic tree representing the separation of the Bacteria, Eukaryotes, and Archaea. LUCA, last universal common ancestor. Most introns are located in the anticodon loop region of the tRNAs. Note that the secondary structures of the eukaryotic and archaeal tRNA introns are very similar and that the introns of both are processed by a specific enzyme, the tRNA splicing endonuclease. By contrast, the bacterial tRNA intron is a self-splicing-type intron.
Mentions: The secondary structure of tRNA can be represented as a cloverleaf with four stems (Figure 1A-a). In some cases, tRNA genes are interrupted by intronic sequence(s) like eukaryotic protein-encoding genes. However, the introns in precursor tRNAs (pre-tRNAs) do not precisely resemble those in precursor mRNAs (pre-mRNAs). The eukaryotic pre-mRNA intron is recognized by base pairing to short RNA molecules such as U1, U2, U4, U5, and U6, whereas the pre-tRNA intron is recognized by a specific enzyme (complex), the tRNA splicing endonuclease [9,10]. Many of the pre-tRNA introns are found at a position adjacent to the anticodon, between nucleotides 37 and 38 of the precursor tRNA (37/38), known as the “canonical” position (Figure 1A-b). The tRNA intron forms a specific RNA secondary structure, the bulge-helix-bulge (BHB), with parts of the exon sequences [11], and this structure is the target of the tRNA splicing endonuclease (shown by arrowheads in Figure 1A) [12]. Using a systematic computational approach we found that some pre-tRNAs possess a single intron located at an unconventional site (Figure 1A-c), or even three introns (Figure 1A-d) in the Archaea, especially in the phylum Crenarchaeota. For example, pre-tRNAGlu(UUC) in Pyrobaculum calidifontis and pre-tRNAPro(UGG) in P. islandicum both contain three introns [1]. However, the evolutionary view is that introns at non-canonical positions are rare, whereas introns at canonical positions (or in the anticodon loop region) are conserved in the three domains of life, Bacteria, Archaea, and Eukaryota (Figure 1B) [13].

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.


Related in: MedlinePlus