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

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...

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Main Authors: Qian Yang, Cheng Xin, Qing-Song Xiao, Ya-Ting Lin, Li Li, Jian-Li Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1304264/full
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author Qian Yang
Cheng Xin
Qing-Song Xiao
Ya-Ting Lin
Li Li
Jian-Li Zhao
author_facet Qian Yang
Cheng Xin
Qing-Song Xiao
Ya-Ting Lin
Li Li
Jian-Li Zhao
author_sort Qian Yang
collection DOAJ
description 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.
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spelling doaj.art-1bd28d45c06140ec9b7aefceec7973952023-12-15T09:43:02ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-12-011410.3389/fpls.2023.13042641304264Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger speciesQian Yang0Cheng Xin1Qing-Song Xiao2Ya-Ting Lin3Li Li4Jian-Li Zhao5Ministry 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, ChinaSchool of Life Sciences, Zhengzhou University, Zhengzhou, ChinaMinistry 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, ChinaMinistry 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, ChinaMinistry 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, ChinaMinistry 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, ChinaCodon 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.https://www.frontiersin.org/articles/10.3389/fpls.2023.1304264/fullcodon usage biaschloroplast genomesadaptive evolutionnatural selectionmutation pressure
spellingShingle Qian Yang
Cheng Xin
Qing-Song Xiao
Ya-Ting Lin
Li Li
Jian-Li Zhao
Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
Frontiers in Plant Science
codon usage bias
chloroplast genomes
adaptive evolution
natural selection
mutation pressure
title Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
title_full Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
title_fullStr Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
title_full_unstemmed Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
title_short Codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
title_sort codon usage bias in chloroplast genes implicate adaptive evolution of four ginger species
topic codon usage bias
chloroplast genomes
adaptive evolution
natural selection
mutation pressure
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1304264/full
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