URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus

Ubiquitin is a small modifier protein which is usually conjugated to substrate proteins for degradation. In recent years, a number of ubiquitin-like proteins have been identified; however, their roles in eukaryotes are largely unknown. Here, we describe a ubiquitin-like protein URM1, and found it pl...

Full description

Bibliographic Details
Main Authors: Luyang Wang, Xuan Cai, Junjie Xing, Caiyun Liu, Ahmed Hendy, Xiao-Lin Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02039/full
id doaj-d5995c73df13430a8cf7a33e58e9a25c
record_format Article
spelling doaj-d5995c73df13430a8cf7a33e58e9a25c2020-11-25T02:11:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-09-011010.3389/fmicb.2019.02039481079URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast FungusLuyang Wang0Xuan Cai1Junjie Xing2Caiyun Liu3Ahmed Hendy4Ahmed Hendy5Xiao-Lin Chen6Xiao-Lin Chen7The Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, ChinaThe Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaThe Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, ChinaThe Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, ChinaDepartment of Agricultural Botany, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria, EgyptThe Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaUbiquitin is a small modifier protein which is usually conjugated to substrate proteins for degradation. In recent years, a number of ubiquitin-like proteins have been identified; however, their roles in eukaryotes are largely unknown. Here, we describe a ubiquitin-like protein URM1, and found it plays important roles in the development and infection process of the rice blast fungus, Magnaporthe oryzae. Targeted deletion of URM1 in M. oryzae resulted in slight reduction in vegetative growth and significant decrease in conidiation. More importantly, the Δurm1 mutant also showed evident reduction in virulence to host plants. Infection process observation demonstrated that the mutant was arrested in invasive growth and resulted in accumulation of massive host reactive oxygen species (ROS). Further, we found the Δurm1 mutant was sensitive to the cell wall disturbing reagents, thiol oxidizing agent diamide and rapamycin. We also showed that URM1-mediated modification was responsive to oxidative stresses, and the thioredoxin peroxidase Ahp1 was one of the important urmylation targets. These results suggested that URM1-mediated urmylation plays important roles in detoxification of host oxidative stress to facilitate invasive growth in M. oryzae.https://www.frontiersin.org/article/10.3389/fmicb.2019.02039/fullubiquitin-like modificationurmylationinfection processoxidative stressMagnaporthe oryzae
collection DOAJ
language English
format Article
sources DOAJ
author Luyang Wang
Xuan Cai
Junjie Xing
Caiyun Liu
Ahmed Hendy
Ahmed Hendy
Xiao-Lin Chen
Xiao-Lin Chen
spellingShingle Luyang Wang
Xuan Cai
Junjie Xing
Caiyun Liu
Ahmed Hendy
Ahmed Hendy
Xiao-Lin Chen
Xiao-Lin Chen
URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus
Frontiers in Microbiology
ubiquitin-like modification
urmylation
infection process
oxidative stress
Magnaporthe oryzae
author_facet Luyang Wang
Xuan Cai
Junjie Xing
Caiyun Liu
Ahmed Hendy
Ahmed Hendy
Xiao-Lin Chen
Xiao-Lin Chen
author_sort Luyang Wang
title URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus
title_short URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus
title_full URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus
title_fullStr URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus
title_full_unstemmed URM1-Mediated Ubiquitin-Like Modification Is Required for Oxidative Stress Adaptation During Infection of the Rice Blast Fungus
title_sort urm1-mediated ubiquitin-like modification is required for oxidative stress adaptation during infection of the rice blast fungus
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-09-01
description Ubiquitin is a small modifier protein which is usually conjugated to substrate proteins for degradation. In recent years, a number of ubiquitin-like proteins have been identified; however, their roles in eukaryotes are largely unknown. Here, we describe a ubiquitin-like protein URM1, and found it plays important roles in the development and infection process of the rice blast fungus, Magnaporthe oryzae. Targeted deletion of URM1 in M. oryzae resulted in slight reduction in vegetative growth and significant decrease in conidiation. More importantly, the Δurm1 mutant also showed evident reduction in virulence to host plants. Infection process observation demonstrated that the mutant was arrested in invasive growth and resulted in accumulation of massive host reactive oxygen species (ROS). Further, we found the Δurm1 mutant was sensitive to the cell wall disturbing reagents, thiol oxidizing agent diamide and rapamycin. We also showed that URM1-mediated modification was responsive to oxidative stresses, and the thioredoxin peroxidase Ahp1 was one of the important urmylation targets. These results suggested that URM1-mediated urmylation plays important roles in detoxification of host oxidative stress to facilitate invasive growth in M. oryzae.
topic ubiquitin-like modification
urmylation
infection process
oxidative stress
Magnaporthe oryzae
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02039/full
work_keys_str_mv AT luyangwang urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT xuancai urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT junjiexing urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT caiyunliu urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT ahmedhendy urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT ahmedhendy urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT xiaolinchen urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
AT xiaolinchen urm1mediatedubiquitinlikemodificationisrequiredforoxidativestressadaptationduringinfectionofthericeblastfungus
_version_ 1724915180150718464