Multilevel genomic constraints shape the organization of nuclear tRNA genes in plants

Transfer RNAs (tRNAs) are key players in protein synthesis, and their abundance in cells directly influences the efficiency of translation. However, the rules governing their genomic organization in plants have remained poorly understood. In a study published in The Plant Journal, researchers from Institute of Molecular Plant Biology (IBMP, CNRS/Unistra) shed light on the mechanisms structuring this organization. By analyzing tRNA gene (tDNA) repertoires in 53 photosynthetic eukaryotes, covering the main plant lineages, as well as in seven non-photosynthetic eukaryotes, the researchers revealed that, despite considerable variation in the total number of tDNAs among species, the relative proportion of tRNA families for each amino acid remains strikingly conserved. This finding suggests the existence of strong evolutionary constraints on tRNA gene dosage, essential for maintaining optimal balance in the translational machinery.

Angiosperms stand out due to a coordinated enrichment of cis-regulatory elements associated with RNA polymerase III transcription, such as AT-rich upstream regions, precisely positioned CAA motifs, and longer poly(T) terminator sequences. These features, less pronounced in other lineages, may reflect an adaptation to the increased complexity of their genomes. At the chromosomal scale, tDNAs are primarily dispersed along chromosome arms, with homogeneous spacing that adjusts according to genome size, while avoiding centromeric regions. Occasionally, certain isotypes form localized clusters, such as those encoding proline, serine, or tyrosine, revealing an organization that is both conserved and lineage-specific.

To facilitate the exploration of these data, researchers developed Shiny tRNA, an interactive web application for analyzing and visualizing the genomic organization of tDNAs at the chromosomal scale. This tool, an extension of the PlantRNA database, offers a new perspective on how genomic, transcriptional, and chromosomal constraints collectively shape the evolution of tDNA repertoires in plants. This work paves the way for a better understanding of the mechanisms linking genome organization and translational efficiency, two key elements for plant adaptation to their environment.