Base composition and translational selection are insufficient to explain codon usage bias in plant viruses

Viral codon usage bias may be the product of a number of synergistic or antagonistic factors, including genomic nucleotide composition, translational selection, genomic architecture, and mutational or repair biases. Most studies of viral codon bias evaluate only the relative importance of genomic base composition and translational selection, ignoring other possible factors. We analyzed the codon preferences of ssRNA (luteoviruses and potyviruses) and ssDNA (geminiviruses) plant viruses that infect translationally distinct monocot and dicot hosts. We found that neither genomic base composition nor translational selection satisfactorily explains their codon usage biases. Furthermore, we observed a strong relationship between the codon preferences of viruses in the same family or genus, regardless of host or genomic nucleotide content. Our results suggest that analyzing codon bias as either due to base composition or translational selection is a false dichotomy that obscures the role of other factors. Constraints such as genomic architecture and secondary structure can and do influence codon usage in plant viruses, and likely in viruses of other hosts.