IJMS, Vol. 19, Pages 3142: Differences in Codon Usage Bias between Photosynthesis-Related Genes and Genetic System-Related Genes of Chloroplast Genomes in Cultivated and Wild Solanum Species (International Journal of Molecular Sciences)

Solanum is one of the largest genera, including two important crops—potato (Solanum tuberosum) and tomato (Solanum lycopersicum). In this study we compared the chloroplast codon usage bias (CUB) among 12 Solanum species, between photosynthesis-related genes (Photo-genes) and genetic system-related genes (Genet-genes), and between cultivated species and wild relatives. The Photo-genes encode proteins for photosystems, the photosynthetic electron transport chain, and RuBisCO, while the Genet-genes encode proteins for ribosomal subunits, RNA polymerases, and maturases. The following findings about the Solanum chloroplast genome CUB were obtained: (1) the nucleotide composition, gene expression, and selective pressure are identified as the main factors affecting chloroplast CUB; (2) all these 12 chloroplast genomes prefer A/U over G/C and pyrimidines over purines at the third-base of codons; (3) Photo-genes have higher codon adaptation indexes than Genet-genes, indicative of a higher gene expression level and a stronger adaptation of Photo-genes; (4) gene function is the primary factor affecting CUB of Photo-genes but not Genet-genes; (5) Photo-genes prefer pyrimidine over purine, whereas Genet-genes favor purine over pyrimidine, at the third position of codons; (6) Photo-genes are mainly affected by the selective pressure, whereas Genet-genes are under the underlying mutational bias; (7) S. tuberosum is more similar with Solanum commersonii than with Solanum bulbocastanum; (8) S. lycopersicum is greatly different from the analyzed seven wild relatives; (9) the CUB in codons for valine, aspartic acid, and threonine are the same between the two crop species, S. tuberosum and S. lycopersicum. These findings suggest that the chloroplast CUB contributed to the differential requirement of gene expression activity and function between Photo-genes and Genet-genes and to the performance of cultivated potato and tomato.