In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae

Verticillium dahliae is highly prone to pathogenic differentiation and influenced by host cotton's resistance. To better understand the mechanisms of this phenomenon, we applied the host selective pressures of resistant and susceptible cotton varieties on V. dahliae strain Vd076 within an artif...

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Main Authors: Yalin Zhang, Lifang Cui, Ruibing Liu, Zili Feng, Hongjie Feng, Jinglong Zhou, Lihong Zhao, Feng Wei, Heqin Zhu
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325000661
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author Yalin Zhang
Lifang Cui
Ruibing Liu
Zili Feng
Hongjie Feng
Jinglong Zhou
Lihong Zhao
Feng Wei
Heqin Zhu
author_facet Yalin Zhang
Lifang Cui
Ruibing Liu
Zili Feng
Hongjie Feng
Jinglong Zhou
Lihong Zhao
Feng Wei
Heqin Zhu
author_sort Yalin Zhang
collection DOAJ
description Verticillium dahliae is highly prone to pathogenic differentiation and influenced by host cotton's resistance. To better understand the mechanisms of this phenomenon, we applied the host selective pressures of resistant and susceptible cotton varieties on V. dahliae strain Vd076 within an artificial cotton Verticillium wilt nursery and greenhouse. Consequently, among the offspring strains, high virulence strains exhibited higher levels of physiological characteristics and genetic diversity compared to moderate and low virulence strains. Moreover, whole genome resequencing revealed that the Ka/Ks ratio of single nucleotide polymorphism (SNPs) in the majority of the offspring strains was about 0.6, indicating an adverse selection impact in the offspring strains. Pathogenicity assays demonstrated that the virulence of the offspring strains triggered by continuous induction of disease-resistant cotton cultivar increased from the 4th generation and reached its peak by the 6th generation. Additionally, the transcriptome analysis revealed that the 4th and 6th generations of strains differentially expressed genes (DEGs) accumulated a significant number of response genes associated with pathogen pathogenicity differentiation, including the mitogen-activated protein kinase (MAPK) signaling pathway, amino and antibiotic biosynthesis, phenylpropanoid metabolism. Furthermore, VDAG_04757, VDAG_06462, VDAG_03218, and VDAG_08487 genes exhibited significant correlation with the pathogenicity of V. dahliae. Collectively, this study has significant implications for elucidating the evolution of virulence in V. dahliae induced by the host, as well as for advancing holistic strategies for preventing and managing Verticillium wilt disease.
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spelling doaj-art-4dfc16dd5ea84530bbce3f89ee334ecc2025-02-12T05:30:07ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01290117730In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliaeYalin Zhang0Lifang Cui1Ruibing Liu2Zili Feng3Hongjie Feng4Jinglong Zhou5Lihong Zhao6Feng Wei7Heqin Zhu8State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, China; Western Agricultural Research Center of Chinese Academy of Agricultural Sciences, Changji 831100, China; Hebei Agricultural University, Hebei Research Base of State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, State Key Laboratory of North China Crop Improvement and Regulation, Baoding 071000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, China; Western Agricultural Research Center of Chinese Academy of Agricultural Sciences, Changji 831100, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, China; Corresponding author.State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, China; Western Agricultural Research Center of Chinese Academy of Agricultural Sciences, Changji 831100, China; Corresponding author at: State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, China.Verticillium dahliae is highly prone to pathogenic differentiation and influenced by host cotton's resistance. To better understand the mechanisms of this phenomenon, we applied the host selective pressures of resistant and susceptible cotton varieties on V. dahliae strain Vd076 within an artificial cotton Verticillium wilt nursery and greenhouse. Consequently, among the offspring strains, high virulence strains exhibited higher levels of physiological characteristics and genetic diversity compared to moderate and low virulence strains. Moreover, whole genome resequencing revealed that the Ka/Ks ratio of single nucleotide polymorphism (SNPs) in the majority of the offspring strains was about 0.6, indicating an adverse selection impact in the offspring strains. Pathogenicity assays demonstrated that the virulence of the offspring strains triggered by continuous induction of disease-resistant cotton cultivar increased from the 4th generation and reached its peak by the 6th generation. Additionally, the transcriptome analysis revealed that the 4th and 6th generations of strains differentially expressed genes (DEGs) accumulated a significant number of response genes associated with pathogen pathogenicity differentiation, including the mitogen-activated protein kinase (MAPK) signaling pathway, amino and antibiotic biosynthesis, phenylpropanoid metabolism. Furthermore, VDAG_04757, VDAG_06462, VDAG_03218, and VDAG_08487 genes exhibited significant correlation with the pathogenicity of V. dahliae. Collectively, this study has significant implications for elucidating the evolution of virulence in V. dahliae induced by the host, as well as for advancing holistic strategies for preventing and managing Verticillium wilt disease.http://www.sciencedirect.com/science/article/pii/S0147651325000661CottonHost-pathogen interactionPathogenicity geneVerticillium dahliaeVirulence variation
spellingShingle Yalin Zhang
Lifang Cui
Ruibing Liu
Zili Feng
Hongjie Feng
Jinglong Zhou
Lihong Zhao
Feng Wei
Heqin Zhu
In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae
Ecotoxicology and Environmental Safety
Cotton
Host-pathogen interaction
Pathogenicity gene
Verticillium dahliae
Virulence variation
title In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae
title_full In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae
title_fullStr In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae
title_full_unstemmed In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae
title_short In the coevolution of cotton and pathogenic fungi, resistant cotton varieties lead to an escalation in the virulence of Verticillium dahliae
title_sort in the coevolution of cotton and pathogenic fungi resistant cotton varieties lead to an escalation in the virulence of verticillium dahliae
topic Cotton
Host-pathogen interaction
Pathogenicity gene
Verticillium dahliae
Virulence variation
url http://www.sciencedirect.com/science/article/pii/S0147651325000661
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