Differences in Codon Usage Bias between Photosynthesis-Related Genes and Genetic System-Related Genes of Chloroplast Genomes in Cultivated and Wild Solanum Species

Abstract

<i>Solanum</i> is one of the largest genera, including two important crops-potato (<i>Solanum tuberosum</i>) and tomato (<i>Solanum lycopersicum</i>). In this study we compared the chloroplast codon usage bias (CUB) among 12 <i>Solanum</i> 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 <i>Solanum</i> 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) <i>S</i>. <i>tuberosum</i> is more similar with <i>Solanum commersonii</i> than with <i>Solanum bulbocastanum</i>; (8) <i>S</i>. <i>lycopersicum</i> 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, <i>S. tuberosum</i> and <i>S. lycopersicum.</i> 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.