Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum

All organisms must secure essential trace elements (e.g., Cu) for survival and reproduction. However, excess trace element accumulation in cells is highly toxic. The maintenance of copper (Cu) homeostasis has been extensively studied in mammals, bacteria, and yeast but not in plant pathogens. In thi...

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Main Authors: Xin Liu, Yichen Jiang, Dan He, Xin Fang, Jianhong Xu, Yin-Won Lee, Nancy P. Keller, Jianrong Shi
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.01392/full
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author Xin Liu
Xin Liu
Xin Liu
Yichen Jiang
Yichen Jiang
Dan He
Xin Fang
Xin Fang
Jianhong Xu
Jianhong Xu
Yin-Won Lee
Yin-Won Lee
Nancy P. Keller
Nancy P. Keller
Jianrong Shi
Jianrong Shi
author_facet Xin Liu
Xin Liu
Xin Liu
Yichen Jiang
Yichen Jiang
Dan He
Xin Fang
Xin Fang
Jianhong Xu
Jianhong Xu
Yin-Won Lee
Yin-Won Lee
Nancy P. Keller
Nancy P. Keller
Jianrong Shi
Jianrong Shi
author_sort Xin Liu
collection DOAJ
description All organisms must secure essential trace elements (e.g., Cu) for survival and reproduction. However, excess trace element accumulation in cells is highly toxic. The maintenance of copper (Cu) homeostasis has been extensively studied in mammals, bacteria, and yeast but not in plant pathogens. In this study, we investigated the molecular mechanisms of copper tolerance in Fusarium graminearum, the important wheat head scab fungus. RNA-seq revealed induced expression of the P-type ATPase transporter FgCrpA and metallothionein (MT) FgCrdA after excess Cu treatment. Deletion of FgCrpA but not FgCrdA resulted in reduced tolerance to Cu toxicity. The “Cu fist” transcription factor FgAceA was involved in Cu detoxification through activation of FgCrpA. △FgAceA was more sensitive to copper toxicity than △FgCrpA and overexpression of FgCrpA restored copper tolerance in △FgAceA. FgAceA negatively regulated aurofusarin production and its biosynthetic gene expression. △FgCrpA and △FgAceA were reduced in virulence in flowering wheat heads and synthesized decreased amounts of the mycotoxin deoxynivalenol when challenged with excess Cu. Taken together, these results suggest that mediation of Cu tolerance in F. graminearum mainly relies on the Cu efflux pump and that FgAceA governs Cu detoxification through activation of FgCrpA.
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spelling doaj.art-d324806b2e9e4acc8b28b3c68aa0e04d2022-12-22T01:05:11ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-06-011110.3389/fmicb.2020.01392548639Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearumXin Liu0Xin Liu1Xin Liu2Yichen Jiang3Yichen Jiang4Dan He5Xin Fang6Xin Fang7Jianhong Xu8Jianhong Xu9Yin-Won Lee10Yin-Won Lee11Nancy P. Keller12Nancy P. Keller13Jianrong Shi14Jianrong Shi15Jiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaDepartment of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI, United StatesSchool of Food and Biological Engineering, Jiangsu University, Zhenjiang, ChinaJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaCollege of Food Science, Tibet Agriculture and Animal Husbandry University, Nyingchi, ChinaJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaSchool of Food and Biological Engineering, Jiangsu University, Zhenjiang, ChinaJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaSchool of Food and Biological Engineering, Jiangsu University, Zhenjiang, ChinaJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaSchool of Agricultural Biotechnology, Seoul National University, Seoul, South KoreaDepartment of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Bacteriology, University of Wisconsin-Madison, Madison, WI, United StatesJiangsu Key Laboratory for Food Quality and Safety-State Key Laboratory Cultivation Base, Ministry of Science and Technology/Key Laboratory for Control Technology and Standard for Agro-product Safety and Quality, Ministry of Agriculture and Rural Affairs/Key Laboratory for Agro-product Safety Risk Evaluation (Nanjing), Ministry of Agriculture and Rural Affairs/Collaborative Innovation Center for Modern Grain Circulation and Safety/Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, ChinaSchool of Food and Biological Engineering, Jiangsu University, Zhenjiang, ChinaAll organisms must secure essential trace elements (e.g., Cu) for survival and reproduction. However, excess trace element accumulation in cells is highly toxic. The maintenance of copper (Cu) homeostasis has been extensively studied in mammals, bacteria, and yeast but not in plant pathogens. In this study, we investigated the molecular mechanisms of copper tolerance in Fusarium graminearum, the important wheat head scab fungus. RNA-seq revealed induced expression of the P-type ATPase transporter FgCrpA and metallothionein (MT) FgCrdA after excess Cu treatment. Deletion of FgCrpA but not FgCrdA resulted in reduced tolerance to Cu toxicity. The “Cu fist” transcription factor FgAceA was involved in Cu detoxification through activation of FgCrpA. △FgAceA was more sensitive to copper toxicity than △FgCrpA and overexpression of FgCrpA restored copper tolerance in △FgAceA. FgAceA negatively regulated aurofusarin production and its biosynthetic gene expression. △FgCrpA and △FgAceA were reduced in virulence in flowering wheat heads and synthesized decreased amounts of the mycotoxin deoxynivalenol when challenged with excess Cu. Taken together, these results suggest that mediation of Cu tolerance in F. graminearum mainly relies on the Cu efflux pump and that FgAceA governs Cu detoxification through activation of FgCrpA.https://www.frontiersin.org/article/10.3389/fmicb.2020.01392/fullFusarium graminearumcopper toleranceFgAceAcopper transportersmetallothioneinvirulence
spellingShingle Xin Liu
Xin Liu
Xin Liu
Yichen Jiang
Yichen Jiang
Dan He
Xin Fang
Xin Fang
Jianhong Xu
Jianhong Xu
Yin-Won Lee
Yin-Won Lee
Nancy P. Keller
Nancy P. Keller
Jianrong Shi
Jianrong Shi
Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum
Frontiers in Microbiology
Fusarium graminearum
copper tolerance
FgAceA
copper transporters
metallothionein
virulence
title Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum
title_full Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum
title_fullStr Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum
title_full_unstemmed Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum
title_short Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum
title_sort copper tolerance mediated by fgacea and fgcrpa in fusarium graminearum
topic Fusarium graminearum
copper tolerance
FgAceA
copper transporters
metallothionein
virulence
url https://www.frontiersin.org/article/10.3389/fmicb.2020.01392/full
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