Genome-Wide Analysis Reveals Origin of Transfer RNA Genes from tRNA Halves

Abstract

Transfer RNAs (tRNAs) play an important role linking mitochondrial RNA and amino acids during protein biogenesis. Four types of tRNA genes have been identified in living organisms. However, the evolutionary origin of tRNAs remains largely unknown. In this article, we conduct a deep sequence analysis of diverse genomes that cover all three domains of life to unveil the evolutionary history of tRNA genes from tRNA halves. tRNA half homologs were detected in diverse organisms, and some of them were expressed in mouse tissues. Continuous tRNA genes have a conserved pattern similar to indels, which is, more closely flanking regions have higher single nucleotide substitution rates, whereas tRNA half homologs do not have this pattern. In addition, tRNAs tend to break into tRNA halves when tissues are incubated in vitro, the tendency of tRNA to break into tRNA halves may be a "side-effect" of tRNA genes evolving from tRNA halves. These results suggest that modern tRNAs originated from tRNA halves through a repeat element-mediated mechanism. These findings provide insight into the evolutionary origin of tRNA genes.

A Dynamic Mobile DNA Family in the Yeast Mitochondrial Genome

“…The merger of palindromic sequences has been proposed as an important mechanism to create functional and structurally complex RNAs. For instance, nuclear tRNA halves can form hairpin structure and can be ligated into chimeric tRNA with cloverleaf structure during evolution ( Zuo et al 2013 ), that is, merger and shuffling of tRNA fragments created modern tRNAs. Modern tRNAs could have been inserted into the genome via retrotransposition ( Zuo et al 2013 ), which is likely also crucial for the mobility of GC clusters.…”

“…For instance, nuclear tRNA halves can form hairpin structure and can be ligated into chimeric tRNA with cloverleaf structure during evolution ( Zuo et al 2013 ), that is, merger and shuffling of tRNA fragments created modern tRNAs. Modern tRNAs could have been inserted into the genome via retrotransposition ( Zuo et al 2013 ), which is likely also crucial for the mobility of GC clusters. Many hairpin-structured RNAs have been previously shown to bear ribozyme activity, which catalyzes self-cleavage and ligation reactions ( Gwiazda et al 2012 ; Muller et al 2012 ).…”

Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications

“…Therefore, RNA-guided DNA methylation could be one possible mechanism that underlies transgenerational inheritance of acquired phenotypes. Intriguingly, sperm tsRNAs exhibit sequence matches at various gene promoters 9 , many of which are associated with transposable elements (TEs) 100 , suggesting that transcriptional regulation of these genes occurs through TEs. Indeed, injection of a single tsRNA (tsRNA Gly(GCC) ) into a mouse zygote can repress the genes associated with murine endogenous retrovirus with leucine tRNA (MERVL), a type of TE 11 .…”

Analyses of Genomic tRNA Reveal Presence of Novel tRNAs in Oryza sativa

“…Transfer RNAs (tRNA) are the most common ancestral short non-coding RNA present in the world and considered one of the single largest gene family in the genome of any species (Mallick et al, 2005; Michaud et al, 2011; Zuo et al, 2013). These molecules can be traced back to the RNA world before the separation of the three major domains of life (Eigen et al, 1989) demonstrating that, all tRNA genes are homologs and derived from an ancestral proto tRNA (Eigen and Winkler-Oswatitsch, 1981).…”