Pattern-recognition receptors are required for NLR-mediated plant immunity

The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI...

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Published inNature (London) Vol. 592; no. 7852; pp. 105 - 109
Main Authors Yuan, Minhang, Jiang, Zeyu, Bi, Guozhi, Nomura, Kinya, Liu, Menghui, Wang, Yiping, Cai, Boying, Zhou, Jian-Min, He, Sheng Yang, Xin, Xiu-Fang
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.04.2021
Nature Publishing Group
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Summary:The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is triggered by microbial patterns via cell surface-localized pattern-recognition receptors (PRRs), whereas ETI is activated by pathogen effector proteins via predominantly intracellularly localized receptors called nucleotide-binding, leucine-rich repeat receptors (NLRs) 1 – 4 . PTI and ETI are initiated by distinct activation mechanisms and involve different early signalling cascades 5 , 6 . Here we show that Arabidopsis PRR and PRR co-receptor mutants— fls2 efr cerk1 and bak1 bkk1 cerk1 triple mutants—are markedly impaired in ETI responses when challenged with incompatible Pseudomonas syrinage bacteria. We further show that the production of reactive oxygen species by the NADPH oxidase RBOHD is a critical early signalling event connecting PRR- and NLR-mediated immunity, and that the receptor-like cytoplasmic kinase BIK1 is necessary for full activation of RBOHD, gene expression and bacterial resistance during ETI. Moreover, NLR signalling rapidly augments the transcript and/or protein levels of key PTI components. Our study supports a revised model in which potentiation of PTI is an indispensable component of ETI during bacterial infection. This revised model conceptually unites two major immune signalling cascades in plants and mechanistically explains some of the long-observed similarities in downstream defence outputs between PTI and ETI. Bacteria elicit two distinct immune responses in Arabidopsis thaliana , mediated by diverse signalling receptors but working in a synergistic manner.
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With initial observation of PRR dependency for ETI resistance made by X-F. X. while at Michigan State University, supported by the US National Institute of General Medical Sciences (GM109928), M. Y. and X-F. X. conceptualized and designed subsequent experiments at CAS Center for Excellence in Molecular Plant Sciences/Institute of Plant Physiology and Ecology. M. Y. performed most experiments including ROS detection, disease/HR assays, RNAseq, transcript and protein analysis. Z. J. and M. L. performed RIN4 cleavage, MAPK phosphorylation and gene expression experiments. G. B., Y. W., M. Y. and B. C. performed protoplast experiments for detecting RBOHD phosphorylation. K. N. performed the disease assay and gene expression analysis in bik1 and rbohd mutants. S. Y. H, and J-M. Z supervised K. N. and G. B., respectively. M. Y. and X-F. X. wrote the paper and S. Y. H. and J-M. Z. edited the paper.
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ISSN:0028-0836
1476-4687
DOI:10.1038/s41586-021-03316-6