Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.

Reactive oxygen species (ROS) production is one of the earliest responses when plants percept pathogens and acts as antimicrobials to block pathogen entry. However, whether and how pathogens tolerate ROS stress remains elusive. Here, we report the chromatin remodeling in Verticillium dahliae, a soil...

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Main Authors: Sheng Wang, Xue-Ming Wu, Chuan-Hui Liu, Jing-Yun Shang, Feng Gao, Hui-Shan Guo
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-04-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1008481
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author Sheng Wang
Xue-Ming Wu
Chuan-Hui Liu
Jing-Yun Shang
Feng Gao
Hui-Shan Guo
author_facet Sheng Wang
Xue-Ming Wu
Chuan-Hui Liu
Jing-Yun Shang
Feng Gao
Hui-Shan Guo
author_sort Sheng Wang
collection DOAJ
description Reactive oxygen species (ROS) production is one of the earliest responses when plants percept pathogens and acts as antimicrobials to block pathogen entry. However, whether and how pathogens tolerate ROS stress remains elusive. Here, we report the chromatin remodeling in Verticillium dahliae, a soil-borne pathogenic fungus that causes vascular wilts of a wide range of plants, facilitates the DNA damage repair in response to plant ROS stress. We identified VdDpb4, encoding a histone-fold protein of the ISW2 chromatin remodeling complex in V. dahliae, is a virulence gene. The reduced virulence in wild type Arabidopsis plants arising from VdDpb4 deletion was impaired in the rbohd mutant plants that did not produce ROS. Further characterization of VdDpb4 and its interacting protein, VdIsw2, an ATP-dependent chromatin-remodeling factor, we show that while the depletion of VdIsw2 led to the decondensing of chromatin, the depletion of VdDpb4 resulted in a more compact chromatin structure and affected the VdIsw2-dependent transcriptional effect on gene expression, including genes involved in DNA damage repair. A knockout mutant of either VdDpb4 or VdIsw2 reduced the efficiency of DNA repair in the presence of DNA-damaging agents and virulence during plant infection. Together, our data demonstrate that VdDpb4 and VdIsw2 play roles in maintaining chromatin structure for positioning nucleosomes and transcription regulation, including genes involved in DNA repair in response to ROS stress during development and plant infection.
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spelling doaj.art-f1302b1a16a2407ebe4220f2f77543bf2022-12-21T22:38:56ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742020-04-01164e100848110.1371/journal.ppat.1008481Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.Sheng WangXue-Ming WuChuan-Hui LiuJing-Yun ShangFeng GaoHui-Shan GuoReactive oxygen species (ROS) production is one of the earliest responses when plants percept pathogens and acts as antimicrobials to block pathogen entry. However, whether and how pathogens tolerate ROS stress remains elusive. Here, we report the chromatin remodeling in Verticillium dahliae, a soil-borne pathogenic fungus that causes vascular wilts of a wide range of plants, facilitates the DNA damage repair in response to plant ROS stress. We identified VdDpb4, encoding a histone-fold protein of the ISW2 chromatin remodeling complex in V. dahliae, is a virulence gene. The reduced virulence in wild type Arabidopsis plants arising from VdDpb4 deletion was impaired in the rbohd mutant plants that did not produce ROS. Further characterization of VdDpb4 and its interacting protein, VdIsw2, an ATP-dependent chromatin-remodeling factor, we show that while the depletion of VdIsw2 led to the decondensing of chromatin, the depletion of VdDpb4 resulted in a more compact chromatin structure and affected the VdIsw2-dependent transcriptional effect on gene expression, including genes involved in DNA damage repair. A knockout mutant of either VdDpb4 or VdIsw2 reduced the efficiency of DNA repair in the presence of DNA-damaging agents and virulence during plant infection. Together, our data demonstrate that VdDpb4 and VdIsw2 play roles in maintaining chromatin structure for positioning nucleosomes and transcription regulation, including genes involved in DNA repair in response to ROS stress during development and plant infection.https://doi.org/10.1371/journal.ppat.1008481
spellingShingle Sheng Wang
Xue-Ming Wu
Chuan-Hui Liu
Jing-Yun Shang
Feng Gao
Hui-Shan Guo
Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.
PLoS Pathogens
title Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.
title_full Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.
title_fullStr Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.
title_full_unstemmed Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.
title_short Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress.
title_sort verticillium dahliae chromatin remodeling facilitates the dna damage repair in response to plant ros stress
url https://doi.org/10.1371/journal.ppat.1008481
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