A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae

The production of reactive oxygen species (ROS) is a ubiquitous defense response in plants. Adapted pathogens evolved mechanisms to counteract the deleterious effects of host-derived ROS and promote infection. How plant pathogens regulate this elaborate response against ROS burst remains unclear. Us...

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Main Authors: Xinyu Liu, Qikun Zhou, Ziqian Guo, Peng Liu, Lingbo Shen, Ning Chai, Bin Qian, Yongchao Cai, Wenya Wang, Ziyi Yin, Haifeng Zhang, Xiaobo Zheng, Zhengguang Zhang
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/61605
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record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Xinyu Liu
Qikun Zhou
Ziqian Guo
Peng Liu
Lingbo Shen
Ning Chai
Bin Qian
Yongchao Cai
Wenya Wang
Ziyi Yin
Haifeng Zhang
Xiaobo Zheng
Zhengguang Zhang
spellingShingle Xinyu Liu
Qikun Zhou
Ziqian Guo
Peng Liu
Lingbo Shen
Ning Chai
Bin Qian
Yongchao Cai
Wenya Wang
Ziyi Yin
Haifeng Zhang
Xiaobo Zheng
Zhengguang Zhang
A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae
eLife
transcription factor
M. oryzae
pathogenicity
phosphorylation
reactive oxygen species
author_facet Xinyu Liu
Qikun Zhou
Ziqian Guo
Peng Liu
Lingbo Shen
Ning Chai
Bin Qian
Yongchao Cai
Wenya Wang
Ziyi Yin
Haifeng Zhang
Xiaobo Zheng
Zhengguang Zhang
author_sort Xinyu Liu
title A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae
title_short A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae
title_full A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae
title_fullStr A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae
title_full_unstemmed A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae
title_sort self-balancing circuit centered on moosm1 kinase governs adaptive responses to host-derived ros in magnaporthe oryzae
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-12-01
description The production of reactive oxygen species (ROS) is a ubiquitous defense response in plants. Adapted pathogens evolved mechanisms to counteract the deleterious effects of host-derived ROS and promote infection. How plant pathogens regulate this elaborate response against ROS burst remains unclear. Using the rice blast fungus Magnaporthe oryzae, we uncovered a self-balancing circuit controlling response to ROS in planta and virulence. During infection, ROS induces phosphorylation of the high osmolarity glycerol pathway kinase MoOsm1 and its nuclear translocation. There, MoOsm1 phosphorylates transcription factor MoAtf1 and dissociates MoAtf1-MoTup1 complex. This releases MoTup1-mediated transcriptional repression on oxidoreduction-pathway genes and activates the transcription of MoPtp1/2 protein phosphatases. In turn, MoPtp1/2 dephosphorylate MoOsm1, restoring the circuit to its initial state. Balanced interactions among proteins centered on MoOsm1 provide a means to counter host-derived ROS. Our findings thereby reveal new insights into how M. oryzae utilizes a phosphor-regulatory circuitry to face plant immunity during infection.
topic transcription factor
M. oryzae
pathogenicity
phosphorylation
reactive oxygen species
url https://elifesciences.org/articles/61605
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spelling doaj-7793729c36b943bfb8a2bd03e07d6eee2021-05-05T21:47:35ZengeLife Sciences Publications LtdeLife2050-084X2020-12-01910.7554/eLife.61605A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzaeXinyu Liu0Qikun Zhou1Ziqian Guo2Peng Liu3Lingbo Shen4Ning Chai5Bin Qian6Yongchao Cai7Wenya Wang8Ziyi Yin9Haifeng Zhang10Xiaobo Zheng11Zhengguang Zhang12https://orcid.org/0000-0001-8253-4505Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China; The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China; The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, ChinaDepartment of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China; The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, ChinaThe production of reactive oxygen species (ROS) is a ubiquitous defense response in plants. Adapted pathogens evolved mechanisms to counteract the deleterious effects of host-derived ROS and promote infection. How plant pathogens regulate this elaborate response against ROS burst remains unclear. Using the rice blast fungus Magnaporthe oryzae, we uncovered a self-balancing circuit controlling response to ROS in planta and virulence. During infection, ROS induces phosphorylation of the high osmolarity glycerol pathway kinase MoOsm1 and its nuclear translocation. There, MoOsm1 phosphorylates transcription factor MoAtf1 and dissociates MoAtf1-MoTup1 complex. This releases MoTup1-mediated transcriptional repression on oxidoreduction-pathway genes and activates the transcription of MoPtp1/2 protein phosphatases. In turn, MoPtp1/2 dephosphorylate MoOsm1, restoring the circuit to its initial state. Balanced interactions among proteins centered on MoOsm1 provide a means to counter host-derived ROS. Our findings thereby reveal new insights into how M. oryzae utilizes a phosphor-regulatory circuitry to face plant immunity during infection.https://elifesciences.org/articles/61605transcription factorM. oryzaepathogenicityphosphorylationreactive oxygen species