The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel

Xuetao Shi; Yu Long; Feng He; Chongyang Zhang; Ruyi Wang; Ting Zhang; Wei Wu; Zeyun Hao; Yi Wang; Guo-Liang Wang; Yuese Ning

doi:10.1371/journal.ppat.1006878

The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel

PLoS Pathog. 2018 Jan 31;14(1):e1006878. doi: 10.1371/journal.ppat.1006878. eCollection 2018 Jan.

Authors

Xuetao Shi¹, Yu Long², Feng He¹, Chongyang Zhang¹, Ruyi Wang¹, Ting Zhang¹, Wei Wu², Zeyun Hao¹, Yi Wang², Guo-Liang Wang^{1

3}, Yuese Ning¹

Affiliations

¹ State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
² State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, China.
³ Department of Plant Pathology, Ohio State University, Columbus, Ohio, United States of America.

Abstract

Potassium (K+) is required by plants for growth and development, and also contributes to immunity against pathogens. However, it has not been established whether pathogens modulate host K+ signaling pathways to enhance virulence and subvert host immunity. Here, we show that the effector protein AvrPiz-t from the rice blast pathogen Magnaporthe oryzae targets a K+ channel to subvert plant immunity. AvrPiz-t interacts with the rice plasma-membrane-localized K+ channel protein OsAKT1 and specifically suppresses the OsAKT1-mediated K+ currents. Genetic and phenotypic analyses show that loss of OsAKT1 leads to decreased K+ content and reduced resistance against M. oryzae. Strikingly, AvrPiz-t interferes with the association of OsAKT1 with its upstream regulator, the cytoplasmic kinase OsCIPK23, which also plays a positive role in K+ absorption and resistance to M. oryzae. Furthermore, we show a direct correlation between blast disease resistance and external K+ status in rice plants. Together, our data present a novel mechanism by which a pathogen suppresses plant host immunity by modulating a host K+ channel.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Host-Pathogen Interactions / genetics
Host-Pathogen Interactions / immunology
Immune Evasion* / genetics
Immunity, Innate / genetics
Magnaporthe / pathogenicity
Magnaporthe / physiology*
Organisms, Genetically Modified
Oryza / genetics
Oryza / immunology
Oryza / microbiology*
Plant Diseases / genetics
Plant Diseases / immunology
Plant Diseases / microbiology
Plants, Genetically Modified
Potassium Channels / genetics*
Potassium Channels / metabolism
Virulence / genetics

Substances

Potassium Channels

Grants and funding

This project was supported by grants from the National Key Research and Development Program of China (http://program.most.gov.cn/) (2016YFD0100600 to YN), the National Natural Science Foundation of China (http://www.nsfc.gov.cn/) (31571944 to YN and 31622008 to YW), the Young Elite Scientist Sponsorship of China Association for Science and Technology (http://www.cast.org.cn/) (2015QNRC001 to YN), and the US National Science Foundation (IOS#1120949 to GLW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.