The Origin and Evolution of tRNA Inferred from Phylogenetic Analysis of Structure

Abstract

The evolutionary history of the two structural and functional domains of tRNA is controversial but harbors the secrets of early translation and the genetic code. To explore the origin and evolution of tRNA, we reconstructed phylogenetic trees directly from molecular structure. Forty-two structural characters describing the geometry of 571 tRNAs and three statistical parameters describing thermodynamic and mechanical features of molecules quantitatively were used to derive phylogenetic trees of molecules and molecular substructures. Trees of molecules failed to group tRNA according to amino acid specificity and did not reveal the tripartite nature of life, probably due to loss of phylogenetic signal or because tRNA diversification predated organismal diversification. Trees of substructures derived from both structural and statistical characters support the origin of tRNA in the acceptor arm and the hypothesis that the top half domain composed of acceptor and pseudouridine (TPsiC) arms is more ancient than the bottom half domain composed of dihydrouridine (DHU) and anticodon arms. This constitutes the cornerstone of the genomic tag hypothesis that postulates tRNAs were ancient telomeres in the RNA world. The trees of substructures suggest a model for the evolution of the major functional and structural components of tRNA. In this model, short RNA hairpins with stems homologous to the acceptor arm of present day tRNAs were extended with regions homologous to TPsiC and anticodon arms. The DHU arm was then incorporated into the resulting three-stemmed structure to form a proto-cloverleaf structure. The variable region was the last structural addition to the molecular repertoire of evolving tRNA substructures.

Phylogenetic signal at the Cytb-SertRNA-IG1-ND1 mitochondrial region in Anopheles (Kerteszia) neivai Howard, Dyar & Knab, 1913

“…The evolution of this molecule supports the hypothesis of accretion of its structural parts where acceptor arm and TΨC loop are known to be more ancient than the anticodon, the DHU and the variable loop (55). Because of its importance in cell protein biosynthesis, the tRNA secondary structure is highly conserved at DHU and TΨC loops (56).…”

Extensive tRNA Gene Changes in Synthetic Brassica napus

“…The failure of tRNA genes from the 199 tRNA loci to group in pedigrees in the phylogenetic tree in our study suggests that tRNA gene diversification is extremely rapid. This may support the idea that tRNA gene diversification preceded the divergence of species through all tRNA sequences analysis (Sun and Caetano-Anolles 2008b). tRNA and organisms did not co-evolve, and tRNA was created from a single hairpin duplication (Widmann et al 2005).…”

“…Modern tRNAs are derived from tRNA halves mediated by repeat elements (Zuo et al 2013). The bottom half is more recent than the top half, as deduced from specific codon recognition in mRNA (Sun and Caetano-Anolles 2008b;Sun and Caetano-Anolles 2008c). Furthermore, the tRNA cloverleaf structure can generally fold into the L-shaped 3D structure.…”

Origins and evolution of modern biochemistry: insights from genomes and molecular structure

“…Correlation between RNA folding and the occurrence of structural motifs in natural nucleic acids also supports tendencies towards order (86). Finally, tendencies towards order have been experimentally supported by phylogenetic congruence in the reconstruction of rooted trees generated from sequence, structure, and genomic rearrangements (see below) at different taxonomical levels (78,(87)(88)(89)(90)(91)(92)(93)(94). Note that order is seldom achieved in frustrated systems that are driven by the energetics of conformation and stability, such as RNA or proteins.…”

“…The value of this methodological approach is that it unifies phylogenetics with structural biology (133). We have recently extended the strategy by generating phylogenies of both molecules and substructures that can illuminate processes related to structural evolution (94). This allowed us not only to study phylogenetic relationships at the structural level but also to build timelines describing how substructural components of molecules were added to the evolving molecules.…”