Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions

Tomato spotted wilt virus (TSWV), belonging to the genus <i>Orthotospovirus</i>, is a significant pathogen through its infection of economically vital crops including tomato, tobacco, pepper, and other species worldwide. Given its substantial influence on the agricultural industry, in-de...

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Main Authors: Haiting Zhao, Lang Qin, Xiaolong Deng, Stuart Reitz, Shengyong Wu, Zhen He
Format: Article
Language:English
Published: MDPI AG 2025-06-01
Series:Horticulturae
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Online Access:https://www.mdpi.com/2311-7524/11/7/721
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author Haiting Zhao
Lang Qin
Xiaolong Deng
Stuart Reitz
Shengyong Wu
Zhen He
author_facet Haiting Zhao
Lang Qin
Xiaolong Deng
Stuart Reitz
Shengyong Wu
Zhen He
author_sort Haiting Zhao
collection DOAJ
description Tomato spotted wilt virus (TSWV), belonging to the genus <i>Orthotospovirus</i>, is a significant pathogen through its infection of economically vital crops including tomato, tobacco, pepper, and other species worldwide. Given its substantial influence on the agricultural industry, in-depth research on TSWV is of great necessity. Several studies have been conducted on the dinucleotide preference of TSWV previously; however, the information regarding codon usage bias (CUB) and the virus’s adaptive evolution remains inconclusive. Here, a thorough analysis of TSWV was performed by utilizing five protein-coding sequences in order to investigate the characteristics of CUB. It has been observed that the TSWV protein-coding sequences are AU-rich, and codons ending with A or U are also preferred in these sequences. A consistently stable and preserved genomic composition characterized by a lower codon usage preference was also observed. Principal Component Analysis (PCA), neutrality analysis, and ENC-plot indicated that, in comparison to mutational pressure, natural selection has a more dominant influence on the CUB of TSWV. The codon adaptation index (CAI) demonstrated a more significant correlation between TSWV and <i>Nicotiana tabacum</i>. Meanwhile, the relative codon deoptimization index (RCDI) indicated a stronger correlation between TSWV and <i>Solanum lycopersicum</i>. This study is the first to systematically characterize the CUB of TSWV based on its protein-coding sequences, providing critical insights into viral genetic diversity, evolution mechanisms, and host adaptation. The findings advance understanding of plant-virus coevolution and inform virus-resistant crop breeding and antiviral strategies.
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spelling doaj-art-d3c9f34d4f3545eb89869cedb7874cb42025-07-25T13:24:20ZengMDPI AGHorticulturae2311-75242025-06-0111772110.3390/horticulturae11070721Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host InteractionsHaiting Zhao0Lang Qin1Xiaolong Deng2Stuart Reitz3Shengyong Wu4Zhen He5School of Plant Protection, Yangzhou University, Yangzhou 225009, ChinaSchool of Plant Protection, Yangzhou University, Yangzhou 225009, ChinaSchool of Plant Protection, Yangzhou University, Yangzhou 225009, ChinaMalheur Experiment Station, Oregon State University, Ontario, OR 97914, USAState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaSchool of Plant Protection, Yangzhou University, Yangzhou 225009, ChinaTomato spotted wilt virus (TSWV), belonging to the genus <i>Orthotospovirus</i>, is a significant pathogen through its infection of economically vital crops including tomato, tobacco, pepper, and other species worldwide. Given its substantial influence on the agricultural industry, in-depth research on TSWV is of great necessity. Several studies have been conducted on the dinucleotide preference of TSWV previously; however, the information regarding codon usage bias (CUB) and the virus’s adaptive evolution remains inconclusive. Here, a thorough analysis of TSWV was performed by utilizing five protein-coding sequences in order to investigate the characteristics of CUB. It has been observed that the TSWV protein-coding sequences are AU-rich, and codons ending with A or U are also preferred in these sequences. A consistently stable and preserved genomic composition characterized by a lower codon usage preference was also observed. Principal Component Analysis (PCA), neutrality analysis, and ENC-plot indicated that, in comparison to mutational pressure, natural selection has a more dominant influence on the CUB of TSWV. The codon adaptation index (CAI) demonstrated a more significant correlation between TSWV and <i>Nicotiana tabacum</i>. Meanwhile, the relative codon deoptimization index (RCDI) indicated a stronger correlation between TSWV and <i>Solanum lycopersicum</i>. This study is the first to systematically characterize the CUB of TSWV based on its protein-coding sequences, providing critical insights into viral genetic diversity, evolution mechanisms, and host adaptation. The findings advance understanding of plant-virus coevolution and inform virus-resistant crop breeding and antiviral strategies.https://www.mdpi.com/2311-7524/11/7/721tomato spotted wilt virusnatural selectionmutational pressurecodon usage patternhost adaptation
spellingShingle Haiting Zhao
Lang Qin
Xiaolong Deng
Stuart Reitz
Shengyong Wu
Zhen He
Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions
Horticulturae
tomato spotted wilt virus
natural selection
mutational pressure
codon usage pattern
host adaptation
title Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions
title_full Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions
title_fullStr Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions
title_full_unstemmed Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions
title_short Evolutionary Dynamics of Codon Usage Bias in Tomato Spotted Wilt Virus: Insights into Viral Adaptation and Host Interactions
title_sort evolutionary dynamics of codon usage bias in tomato spotted wilt virus insights into viral adaptation and host interactions
topic tomato spotted wilt virus
natural selection
mutational pressure
codon usage pattern
host adaptation
url https://www.mdpi.com/2311-7524/11/7/721
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