Codon usage bias is presumably affected by tRNA selection effects in Actinidia polyploidization events

Polyploidization is one of the main mechanisms in speciation, yet its effects on the frequency and distribution of synonymous codons remain unclear, which may lead to distinct patterns of codon usage bias (CUB) in polyploid species. To detect whether the patterns of CUB change in Actinidia polyploidization events, we analyzed seven Actinidia species (two polyploid and five diploid species) and five phylogenetically related non-Actinidia species (one polyploid and four diploid species).

The GC and GC3 contents in the 12 plant genomes were below 50%, indicating a preference for A/T-rich nucleotides and A/T-ending codons in these species. The effective number of codons (ENC) and GC3s showed a left-skewed distribution pattern, suggesting that natural selection is the main factor in determining codon usage variation. The species tree inferred from relative synonymous codon usage (RSCU) of orthologs was associated with their phylogenetic relationship. No significant difference in CUB was detected among the subgenomes of A. deliciosa. Diploid A. chinensis and polyploid A. deliciosa shared some optimal codons, such as proline (CCG, CCA), glycine (GGC), and leucine (CTG). Diploid A. chinensis uniquely preferred the asparagine codons AAT and AAC, while polyploid A. deliciosa favored the optimal codons GGT (glycine), AAG (lysine), and GAT/GAC (aspartic acid). Significant correlations (S-values) of ENC and tRNA adaptation index (tAI) indicate tRNA selection effects on CUB, and the Actinidia species exhibited higher S-values (0.33-0.41) than the other non-Actinidia species (0.22-0.34).

Our findings highlight that CUB in Actinidia was not affected by polyploidization events but by natural selection, and the dominant force of shaping CUB is tRNA availability.