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A receptor for dual ligands governs plant immunity and hormone response and is targeted by a nematode effector
Friday, 2024/10/18 | 08:10:35

Li HuangYulin YuanChloe RamirezZhe ZhaoLetian ChenThomas GriebelJoanna Kud

Joseph C. KuhlAllan CaplanLouise-Marie Dandurand, and Fangming Xiao

 

PNAS; October 10, 2024; 121 (42) e2412016121; https://doi.org/10.1073/pnas.2412016121

 

Figure: Potato cyst nematode (Globodera pallida)  

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.

 

See https://www.pnas.org/doi/10.1073/pnas.2412016121

 

Figure 1: StNILR1 recognizes Ascr18, mediating PTI responses. (A) ITC assay indicates the StNILR1 ectodomain (Ecto-StNILR1) binds to Ascr18. 100 μM Ascr18 was injected into Ecto-StNILR1 solution in the ITC cell. The area of each single injection peak corresponds to the total heat released from that injection. The integrated heat is plotted against the molar ratio of Ascr18 titrated into the cell containing Ecto-StNILR1. The binding constant (Kd) and the calculated stoichiometry (N) (± fitting error) are indicated. (B) The C-terminal five LRRs of Ecto-StNILR1 are dispensable for StNILR1 binding to Ascr18 in the ITC assay. (C–F) StNILR1 plays an important role in basal-level resistance to G. pallida, as manifested by that, in comparison to the WT potato plants, StNILR1-OX lines displayed resistance to G. pallida (C) and (D), whereas StNILR1-KD lines were more susceptible (E) and (F). Four-week-old vegetatively propagated WT or transgenic potato plants were inoculated with G. pallida. Nematodes (male and female) were counted 6 wk after the inoculation using acid fuchsin staining. Data are presented as mean ± SD (n = 10). (G) StNILR1 mediates Ascr18-triggered PTI signaling. Leaves of 2-wk-old vegetatively propagated WT or StNILR1-KD transgenic potato seedlings were soaked in 0.2 μM Ascr18 or the Mock solution containing 0.01% Tween 80 for 5 s and the roots were analyzed by RT-PCR at 72 h after treatment. Ascr18-induced expression of StPR1 and StPDF1.2 was compromised in the StNILR1 knockdown transgenic potato roots. StACT41 served as an internal reference for normalization. Data are presented as mean ± SD (n = 3). (H) and (I) StNILR1 is required for Ascr18-triggered immunity against potato cyst nematode G. pallida. Four-week-old vegetatively propagated WT or transgenic potato plants were inoculated with G. pallida cysts and leaf-sprayed with 0.2 μM Ascr18 or Mock solution every other day for 6 wk. Nematodes (male and female) were counted 6 wk after inoculation using acid fuchsin assay. Data are presented as mean ± SD (n = 10). Experiments were repeated two times with similar results. Data were analyzed by two-sided Student’s t test (D, F, and I), one-way ANOVA (G), or two-way ANOVA (C, E, and H) followed by Tukey’s test. Statistical analysis was performed within the same genotype (D, F, and I). n = biologically independent samples.

 

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