Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America.
Laboratory of Genetics, Genome Center of Wisconsin, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Wisconsin, United States of America.
PLoS Genet. 2019 Jul 31;15(7):e1008304. doi: 10.1371/journal.pgen.1008304. eCollection 2019 Jul.
Variation in synonymous codon usage is abundant across multiple levels of organization: between codons of an amino acid, between genes in a genome, and between genomes of different species. It is now well understood that variation in synonymous codon usage is influenced by mutational bias coupled with both natural selection for translational efficiency and genetic drift, but how these processes shape patterns of codon usage bias across entire lineages remains unexplored. To address this question, we used a rich genomic data set of 327 species that covers nearly one third of the known biodiversity of the budding yeast subphylum Saccharomycotina. We found that, while genome-wide relative synonymous codon usage (RSCU) for all codons was highly correlated with the GC content of the third codon position (GC3), the usage of codons for the amino acids proline, arginine, and glycine was inconsistent with the neutral expectation where mutational bias coupled with genetic drift drive codon usage. Examination between genes' effective numbers of codons and their GC3 contents in individual genomes revealed that nearly a quarter of genes (381,174/1,683,203; 23%), as well as most genomes (308/327; 94%), significantly deviate from the neutral expectation. Finally, by evaluating the imprint of translational selection on codon usage, measured as the degree to which genes' adaptiveness to the tRNA pool were correlated with selective pressure, we show that translational selection is widespread in budding yeast genomes (264/327; 81%). These results suggest that the contribution of translational selection and drift to patterns of synonymous codon usage across budding yeasts varies across codons, genes, and genomes; whereas drift is the primary driver of global codon usage across the subphylum, the codon bias of large numbers of genes in the majority of genomes is influenced by translational selection.
在一个氨基酸的密码子之间、一个基因组中的基因之间以及不同物种的基因组之间。现在人们已经很好地理解了同义密码子使用的变化受到突变偏向性的影响，同时还受到翻译效率的自然选择和遗传漂变的影响，但这些过程如何塑造整个谱系中密码子使用偏向性的模式仍未被探索。为了解决这个问题，我们使用了一个包含 327 个物种的丰富基因组数据集，这些物种几乎涵盖了芽殖酵母亚门 Saccharomycotina 已知生物多样性的三分之一。我们发现，虽然所有密码子的全基因组相对同义密码子使用（RSCU）与第三个密码子位置的 GC 含量（GC3）高度相关，但脯氨酸、精氨酸和甘氨酸的密码子使用与突变偏向性与遗传漂变共同驱动密码子使用的中性预期不一致。在单个基因组中检查基因的有效密码子数量与其 GC3 含量之间的关系表明，近四分之一的基因（381,174/1,683,203；23%）以及大多数基因组（308/327；94%）显著偏离中性预期。最后，通过评估翻译选择对密码子使用的影响，即基因对 tRNA 池的适应性与选择压力之间的相关性程度，我们表明翻译选择在芽殖酵母基因组中广泛存在（264/327；81%）。这些结果表明，翻译选择和漂变对芽殖酵母谱系中同义密码子使用模式的贡献在密码子、基因和基因组之间是不同的；虽然漂变是整个亚门全局密码子使用的主要驱动因素，但大多数基因组中大量基因的密码子偏向性受到翻译选择的影响。
