NLRs guard metabolism to coordinate pattern- and effector-triggered immunity

Keran Zhai; Di Liang; Helin Li; Fangyuan Jiao; Bingxiao Yan; Jing Liu; Ziyao Lei; Li Huang; Xiangyu Gong; Xin Wang; Jiashun Miao; Yichuan Wang; Ji-Yun Liu; Lin Zhang; Ertao Wang; Yiwen Deng; Chi-Kuang Wen; Hongwei Guo; Bin Han; Zuhua He

doi:10.1038/s41586-021-04219-2

NLRs guard metabolism to coordinate pattern- and effector-triggered immunity

Nature. 2022 Jan;601(7892):245-251. doi: 10.1038/s41586-021-04219-2. Epub 2021 Dec 15.

Authors

Keran Zhai^#¹, Di Liang^#^{1

2}, Helin Li^{1

3}, Fangyuan Jiao^{1

4}, Bingxiao Yan^{1

2}, Jing Liu^{1

2}, Ziyao Lei^{1

2}, Li Huang^{1

2}, Xiangyu Gong^{1

2}, Xin Wang¹, Jiashun Miao¹, Yichuan Wang⁵, Ji-Yun Liu¹, Lin Zhang⁶, Ertao Wang¹, Yiwen Deng¹, Chi-Kuang Wen¹, Hongwei Guo⁵, Bin Han¹, Zuhua He^{7

8}

Affiliations

¹ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.
² University of the Chinese Academy of Sciences, Beijing, China.
³ School of Life Sciences, Henan University, Kaifeng, China.
⁴ School of Life Science and Technology, Shanghai Tech University, Shanghai, China.
⁵ Department of Biology, Institute of Plant and Food Science, Southern University of Science and Technology, Shenzhen, China.
⁶ Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding, Yangzhou University, Yangzhou, China.
⁷ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China. zhhe@cemps.ac.cn.
⁸ School of Life Science and Technology, Shanghai Tech University, Shanghai, China. zhhe@cemps.ac.cn.

^# Contributed equally.

PMID: 34912119
DOI: 10.1038/s41586-021-04219-2

Abstract

Pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) in plants enable them to respond to pathogens by activating the production of defence metabolites that orchestrate immune responses^1-4. How the production of defence metabolites is promoted by immune receptors and coordinated with broad-spectrum resistance remains elusive. Here we identify the deubiquitinase PICI1 as an immunity hub for PTI and ETI in rice (Oryza sativa). PICI1 deubiquitinates and stabilizes methionine synthetases to activate methionine-mediated immunity principally through biosynthesis of the phytohormone ethylene. PICI1 is targeted for degradation by blast fungal effectors, including AvrPi9, to dampen PTI. Nucleotide-binding domain, leucine-rich-repeat-containing receptors (NLRs) in the plant immune system, such as PigmR, protect PICI1 from effector-mediated degradation to reboot the methionine-ethylene cascade. Natural variation in the PICI1 gene contributes to divergence in basal blast resistance between the rice subspecies indica and japonica. Thus, NLRs govern an arms race with effectors, using a competitive mode that hinges on a critical defence metabolic pathway to synchronize PTI with ETI and ensure broad-spectrum resistance.

MeSH terms

Methionine
Oryza* / genetics
Oryza* / microbiology
Plant Diseases* / microbiology
Plant Immunity / genetics
Plants
Signal Transduction / genetics

Substances

Methionine