Dinucleotide preferences underlie apparent codon preference reversals in the Drosophila melanogaster lineage

• 成果类型: Article
• 署名作者: Yamashita, Haruka; Matsumoto, Tomotaka; Kawashima, Kent; Daanaa, Hassan Sibroe Abdulla; Yang, Ziheng; Akashi, Hiroshi
• 署名单位: Research Organization of Information & Systems (ROIS); National Institute of Genetics (NIG) - Japan; Graduate University for Advanced Studies - Japan; University of London; University College London; Graduate University for Advanced Studies - Japan
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-12694
• DOI: 10.1073/pnas.2419696122
• 发表日期: 2025-05-27
• 关键词: biased gene conversion; coli transfer-rnas; escherichia-coli; molecular evolution; respective codons; translational selection; natural-selection; expression level; transfer-rnahis; protein genes

摘要

We employ fine-scale population genetic analyses to reveal dynamics among interacting forces that act at synonymous sites and introns among closely related Drosophila cies. Synonymous codon usage bias has proven to be well suited for population genetic inference. Under major codon preference (MCP), translationally superior major codons confer fitness benefits relative to their less efficiently and/or accurately decoded synonymous counterparts. Our codon family and lineage-specific analyses expand previous findings in the Drosophila simulans lineage; patterns in naturally occurring polymorphism demonstrate fixation biases toward GC-ending codons that are sistent in direction, but heterogeneous in magnitude, among synonymous families. These forces are generally stronger than fixation biases in intron sequences. In contrast, population genetic analyses reveal unexpected evidence of codon preference reversals in the Drosophila melanogaster lineage. Codon family-specific polymorphism patterns support reduced efficacy of natural selection in most synonymous families but indicate reversals of favored states in the four codon families encoded by NAY. Accelerated onymous fixations in favor of NAT and greater differences for both allele frequencies and fixation rates among X-linked, relative to autosomal, loci bolster support for fitness effect reversals. The specificity of preference reversals to codons whose cognate tRNAs undergo wobble position queuosine modification is intriguing. However, our analyses reveal prevalent dinucleotide preferences for ApT over ApC that act in opposition GC-favoring forces in both coding and intron regions. We present evidence that changes in the relative efficacy of translational selection and dinucleotide preference underlie apparent codon preference reversals.