A eukaryote without tRNA introns

Abstract

One of the striking characteristics of eukaryotic genomes is the presence of three types of introns: spliceosomal introns, tRNA introns, and a unique intron in the XBP1 mRNA. Exceptional eukaryotic genomes that lack spliceosomal or XBP1 introns have been described. However, tRNA introns and the tRNA endonuclease that is required for their splicing are thought to be universal in eukaryotes. The introns in three tRNAs are widely conserved across Metazoa: Tyr-GUA, Ile-UAU and Leu-CAA. This study shows that some nematode species have lost the introns in Tyr-GUA and Ile-UAU tRNAs, and one species, Levipalatum texanum, completely lacks tRNA introns. The loss of the intron from Leu-CAA tRNA is accompanied by an unusual A-C mismatched basepair in the anticodon stem loop and a triplication of a tRNA deaminase that could potentially restore basepairing. These changes may be an adaptation to the loss of the intron. L. texanum also lacks the tRNA endonuclease, one of two enzymes required for tRNA splicing. The other key enzyme in tRNA splicing, tRNA ligase, is bifunctional and is also required for XBP1 mRNA splicing. L. texanum retains tRNA ligase and the XBP1 intron. This eukaryote without tRNA introns has the potential to be a valuable tool for disentangling the functions of tRNA splicing, XBP1 splicing and tRNA modification enzymes, and is the only animal known to have lost one of the three intron types. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=100 SRC="FIGDIR/small/660180v1_ufig1.gif" ALT="Figure 1"> View larger version (16K): org.highwire.dtl.DTLVardef@1a9b5fforg.highwire.dtl.DTLVardef@eb826eorg.highwire.dtl.DTLVardef@1c03a99org.highwire.dtl.DTLVardef@14718d5_HPS_FORMAT_FIGEXP M_FIG C_FIG SIGNIFICANCEtRNA introns are thought to be a universal feature of eukaryotic genomes, including all animal genomes. We identified a species of roundworm, Levipalatum texanum, that completely lacks tRNA introns. L. texanum also lacks the tRNA splicing endonuclease, one of two enzymes required for the removal of introns from tRNAs. The second enzyme involved in this process, tRNA ligase, has a second function: the splicing of a single mRNA. Interestingly, this mRNA splicing reaction is conserved. L. texanum has an usual leucine tRNA and a three copies of a tRNA modifying enzyme that may compensate for the absence of the intron. These findings highlight that although complex RNA processing is a hallmark of eukaryotes, individual reactions may be absent in specific eukaryotes.