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Loss of the common immune coreceptor BAK1 leads to NLR-dependent cell death
Wednesday, 2020/10/28 | 10:38:48

Yujun Wu, Yang Gao, Yanyan Zhan, Hong Kui, Hongyan Liu, Li Yan,  Birgit Kemmerling,  Jian-Min Zhou,  Kai He, and Jia Li.

PNAS October 27, 2020 117 (43) 27044-27053


BAK1 plays a key role in multiple PRR-triggered immune signaling pathways. Double mutants generated by BAK1 and its paralog BKK1 show spontaneous cell death, which is not seen in any known PRR mutants. We discovered that the ADR1 class of helper nucleotide-binding leucine-rich repeat proteins (NLRs) is required for the autoimmune responses of bak1 bkk1. Knocking out three ADR1s can significantly suppress the cell death of bak1-3 bkk1-1, suggesting the autoimmune responses of bak1 bkk1 are caused by NLR activation. Furthermore, expression of HopB1, an effector derived from Pseudomonas syringae that cleaves activated BAK1 and its paralogs, leads to cell death similar to bak1 bkk1, which requires ADR1s. Our results indicate BAK1 and its paralogs serve as guardees for NLRs.


Plants utilize a two-tiered immune system consisting of pattern recognition receptor (PRR)-triggered immunity (PTI) and effector-triggered immunity (ETI) to defend themselves against pathogenic microbes. The receptor protein kinase BAK1 plays a central role in multiple PTI signaling pathways in Arabidopsis. However, double mutants made by BAK1 and its closest paralog BKK1 exhibit autoimmune phenotypes, including cell death resembling a typical nucleotide-binding leucine-rich repeat protein (NLR)-mediated ETI response. The molecular mechanisms of the cell death caused by the depletion of BAK1 and BKK1 are poorly understood. Here, we show that the cell-death phenotype of bak1 bkk1 is suppressed when a group of NLRs, ADR1s, are mutated, indicating the cell-death of bak1 bkk1 is the consequence of NLR activation. Furthermore, introduction of a Pseudomonas syringae effector HopB1, which proteolytically cleaves activated BAK1 and its paralogs via either gene transformation or bacterium-delivery, results in a cell-death phenotype in an ADR1s-dependent manner. Our study thus pinpoints that BAK1 and its paralogs are likely guarded by NLRs.


See: https://www.pnas.org/content/117/43/27044

Figure 1:

ADR1s are up-regulated in bak1 bkk1 double mutants. (A and B) qRT-PCR assays indicate the expression levels of ADR1ADR1-L1, and ADR1-L2 are significantly increased in bak1-4 bkk1-1 (A) and bak1-3 bkk1-1 (B). qRT-PCR was performed by using the total RNA from 8-d-old bak1-4 bkk1-1 seedlings grown on 1/2 MS media or 2-wk-old bak1-3 bkk1-1 plants grown in soil. (C) Overexpression of ADR1s in Col-0 results in autoimmune phenotypes similar to bak1-3 bkk1-1. Three-week-old plants grown in soil are presented. (Scale bars, 1 cm.) (D and E) Trypan blue staining (D) and DAB staining (E) assays indicate overexpression of ADR1s in Col-0 causes cell-death symptoms (D) and H2O2 accumulation (E) similar to bak1-3 bkk1-1. (Scale bars, 100 μm.) (F and GPR1 (F) and FMO1 (G) are expressed in higher levels in ADR1 overexpression lines and bak1-3 bkk1-1. qRT-PCR was performed by using the total RNA from 3-wk-old plants grown in soil. ACT7 was used to normalize the transcript levels. Arbitrary units were used to show the relative abundance of transcript levels of ADR1s, PR1, and FMO1 as compared to Col-0. Bars represent mean ± SD (n = 3). Different letters indicate a significant difference following one-way ANOVA with Tukey's multiple comparison test (P < 0.05).

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