A receptor for dual ligands governs plant immunity and hormone response and is targeted by a nematode effector

Authors

• Li Huang, University of Idaho
• Yulin Yuan, University of Idaho
• Chloe Ramirez, University of Idaho
• Zhe Zhao, South China Agricultural University, Guangzhou
• Letien Chen, South China Agricultural University, Guangzhou
• Thomas Griebl, Freie Universität Berlin
• Joanna Kud, University of Arkansas, Fayetteville
• Joseph C. Kuhl, University of Idaho
• Allan Caplan, University of Idaho
• Louise-Marie Dandurand, University of Idaho
• Fangming Xiao, University of Idaho

Document Type

Article

Publication Date

10-10-2024

Keywords

dual receptor, StNILR1, Ascr18, BR, RHA1B

Abstract

Significance

This study reveals a previously undescribed mechanism in plant defense, wherein a single pattern recognition receptor (StNILR1) recognizes a nematode-associated molecular pattern (NAMP) ascaroside #18 (Ascr18) as well as the phytohormone brassinosteroid (BR) to trigger distinct physiological responses. Furthermore, we identify a nematode effector (RHA1B) that disrupts this dual signaling by targeting StNILR1 for degradation. These findings shed light on the intricate interplay between plant immunity, hormonal regulation, and nematode parasitism.

Abstract

In this study, we show that the potato (Solanum tuberosum) pattern recognition receptor (PRR) NEMATODE-INDUCED LEUCINE-RICH REPEAT (LRR)-RLK1 (StNILR1) functions as a dual receptor, recognizing both nematode-associated molecular pattern ascaroside #18 (Ascr18) and plant hormone brassinosteroid (BR) to activate two different physiological outputs: pattern-triggered immunity (PTI) and BR response. Ascr18/BR-StNILR1 signaling requires the coreceptor potato BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED RECEPTOR KINASE 1 (StBAK1) and perception of either ligand strengthens StNILR1 interaction with StBAK1 in plant cells. Significantly, the parasitically successful potato cyst nematode (Globodera pallida) utilizes the effector RHA1B, which is a functional ubiquitin ligase, to target StNILR1 for ubiquitination-mediated proteasome-dependent degradation, thereby countering Ascr18/BR-StNILR1-mediated PTI in potato and facilitating nematode parasitism. These findings broaden our understanding of PRR specificity and reveal a nematode parasitic mechanism that targets a PTI signaling pathway.

Citation

L. Huang, Y. Yuan, C. Ramirez, Z. Zhao, L. Chen, T. Griebel, J. Kud, J.C. Kuhl, A. Caplan, L. Dandurand, & F. Xiao, A receptor for dual ligands governs plant immunity and hormone response and is targeted by a nematode effector, Proc. Natl. Acad. Sci. U.S.A. 121 (42) e2412016121, https://doi.org/10.1073/pnas.2412016121 (2024).