From water to land: evolution of tRNA gene repertoires in photosynthetic organisms

Abstract

Abstract Photosynthetic eukaryotes have undergone evolutionary shifts from aquatic to terrestrial habitats, accompanied by changes in genome organization and gene regulation. Yet, the evolution of transfer RNA (tRNA) gene repertoires has received limited attention despite their central role in translation. Here, we review how tRNA gene content, structure, and genomic organization diversified across photosynthetic lineages, mainly Archaeplastida, and how changes relate to evolutionary transitions. We show that tRNA gene repertoires are shaped by ecological transitions, genome architecture, and translational demands. We highlight terrestrialization as a shift in tRNA evolution, marked by loss of selenocysteine and its dedicated tRNA, and changes in intron prevalence and structure. Copy number variation correlates with codon usage and amino acid composition, and in angiosperms, nuclear tRNA genes display reinforced cis-regulatory elements consistent with increased translational demands. We show that plant tRNA genes exhibit evenly dispersed arrangements, except in some algae enriched in clustered configurations. Together, these observations support a model in which tRNA gene repertoires are drivers of genome evolution, integrating translational demand, genomic organization, and ecological adaptation across photosynthetic lineages.