Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum

Xin Liu; Yichen Jiang; Dan He; Xin Fang; Jianhong Xu; Yin-Won Lee; Nancy P Keller; Jianrong Shi

doi:10.3389/fmicb.2020.01392

Copper Tolerance Mediated by FgAceA and FgCrpA in Fusarium graminearum

Front Microbiol. 2020 Jun 26:11:1392. doi: 10.3389/fmicb.2020.01392. eCollection 2020.

Authors

Xin Liu^{1

2

3}, Yichen Jiang^{1

4}, Dan He¹, Xin Fang^{1

3}, Jianhong Xu^{1

3}, Yin-Won Lee^{1

5}, Nancy P Keller^{2

6}, Jianrong Shi^{1

3}

Affiliations

¹ Jiangsu 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, China.
² Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI, United States.
³ School of Food and Biological Engineering, Jiangsu University, Zhenjiang, China.
⁴ College of Food Science, Tibet Agriculture and Animal Husbandry University, Nyingchi, China.
⁵ School of Agricultural Biotechnology, Seoul National University, Seoul, South Korea.
⁶ Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, United States.

Abstract

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.

Keywords: FgAceA; Fusarium graminearum; copper tolerance; copper transporters; metallothionein; virulence.