Evolutionary Adjustment of tRNA Identity Rules in Bacillariophyta for Recognition by an Aminoacyl-tRNA Synthetase Adds a Facet to the Origin of Diatoms

Abstract

Error-free protein synthesis relies on the precise recognition by the aminoacyl-tRNA synthetases of their cognate tRNAs in order to attach the corresponding amino acid. A concept of universal tRNA identity elements requires the aminoacyl-tRNA synthetases provided by the genome of an organism to match the identity elements found in the cognate tRNAs in an evolution-independent manner. Identity elements tend to cluster in the tRNA anticodon and acceptor stem regions. However, in the arginine system, in addition to the anticodon, the importance of nucleotide A20 in the tRNA D-loop for cognate enzyme recognition has been a sustained feature for arginyl-tRNA synthetase in archaea, bacteria and in the nuclear-encoded cytosolic form in mammals and plants. However, nuclear-encoded mitochondrial arginyl-tRNA synthetase, which can be distinguished from its cytosolic form by the presence or absence of signature motifs, dispenses with the A20 requirement. An examination of several hundred non-metazoan organisms and their corresponding tRNAArg substrates has confirmed this general concept to a large extent and over numerous phyla. However, some Stramenopiles, and in particular, Diatoms (Bacillariophyta) present a notable exception. Unusually for non-fungal organisms, the nuclear genome encodes tRNAArg isoacceptors with C or U at position 20. In this case one of two nuclear-encoded cytosolic arginyl-tRNA synthetases has evolved to become insensitive to the nature of the D-loop identity element. The other, with a binding pocket that is compatible with tRNAArg-A20 recognition, is targeted to organelles that encode solely such tRNAs.

The tRNA identity landscape for aminoacylation and beyond

“…Further focused searches on several hundred non-metazoan organisms largely confirmed the importance of A 20 in the tRNA Arg identity, but revealed notable exceptions in Stramenopiles and Diatoms, where A 20 is replaced by C 20 or U 20 in most cytosolic tRNAs, whereas it is conserved in mitochondria and plastids ( 391 ).…”

Aminoacyl-tRNA Synthetase Evolution within the Dynamic Tripartite Translation System of Plant Cells

“…Such changes in targeting or tRNA substrates represent potentially radical perturbations in aaRS function, and we hypothesize that they could result in positive selection and accelerated evolution in aaRS sequence for at least three different reasons. First, aaRSs evolving to charge new tRNA substrates may require changes to key regions involved in recognition of tRNA “identity elements” ( Giegé et al 1998 ; Igloi 2021 , 2022 ). Second, mitochondria differ from the cytosol in numerous respects (e.g., osmotic conditions) that could potentially affect protein folding and tRNA interactions and, thus, create selection for changes in protein sequence.…”

Aminoacyl-tRNA synthetase evolution within the dynamic tripartite translation system of plant cells

“…Such changes in targeting or tRNA substrates represent potentially radical perturbations in aaRS function, and we hypothesize that they could result in positive selection and accelerated evolution in aaRS sequence for at least three different reasons. First, aaRSs evolving to charge new tRNA substrates may require changes to key regions involved in recognition of tRNA "identity elements" (Giegé, et al 1998;Igloi 2021Igloi , 2022. Second, mitochondria differ from the cytosol in numerous respects (e.g., osmotic conditions) that could potentially affect protein folding and tRNA interactions and, thus, create selection for changes in protein sequence.…”