Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species

Qian Yang; Cheng Xin; Qing-Song Xiao; Ya-Ting Lin; Li Li; Jian-Li Zhao

doi:10.3389/fpls.2023.1304264

Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species

Front Plant Sci. 2023 Dec 15:14:1304264. doi: 10.3389/fpls.2023.1304264. eCollection 2023.

Authors

Qian Yang¹, Cheng Xin², Qing-Song Xiao¹, Ya-Ting Lin¹, Li Li¹, Jian-Li Zhao¹

Affiliations

¹ Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming, Yunnan, China.
² School of Life Sciences, Zhengzhou University, Zhengzhou, China.

Abstract

Codon usage bias (CUB) refers to different codons exhibiting varying frequencies of usage in the genome. Studying CUB is crucial for understanding genome structure, function, and evolutionary processes. Herein, we investigated the codon usage patterns and influencing factors of protein-coding genes in the chloroplast genomes of four sister genera (monophyletic Roscoea and Cautleya, and monophyletic Pommereschea and Rhynchanthus) from the Zingiberaceae family with contrasting habitats in southwestern China. These genera exhibit distinct habitats, providing a unique opportunity to explore the adaptive evolution of codon usage. We conducted a comprehensive analysis of nucleotide composition and codon usage on protein-coding genes in the chloroplast genomes. The study focused on understanding the relationship between codon usage and environmental adaptation, with a particular emphasis on genes associated with photosynthesis. Nucleotide composition analysis revealed that the overall G/C content of the coding genes was ˂ 48%, indicating an enrichment of A/T bases. Additionally, synonymous and optimal codons were biased toward ending with A/U bases. Natural selection is the primary factor influencing CUB characteristics, particularly photosynthesis-associated genes. We observed differential gene expressions related to light adaptation among sister genera inhabiting different environments. Certain codons were favored under specific conditions, possibly contributing to gene expression regulation in particular environments. This study provides insights into the adaptive evolution of these sister genera by analyzing CUB and offers theoretical assistance for understanding gene expression and regulation. In addition, the data support the relationship between RNA editing and CUB, and the findings shed light on potential research directions for investigating adaptive evolution.

Keywords: adaptive evolution; chloroplast genomes; codon usage bias; mutation pressure; natural selection.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by National Natural Science Foundation of China (grant number 42171057) and the Yunnan Revitalization Talent Support Program “Young Talent Project” (YNWR-QNBJ-2019-214).