The immune receptor SNC1 monitors helper NLRs targeted by a bacterial effector

Abstract

Plants deploy intracellular receptors to counteract pathogen effectors that suppress cell-surface receptor-mediated immunity. To what extent pathogens manipulate also immunity mediated by intracellular receptors, and how plants tackle such manipulation, remains unknown. Arabidopsis thaliana encodes three very similar ADR1 class helper NLRs (ADR1, ADR1-L1 and ADR1-L2), which play key roles in plant immunity initiated by intracellular receptors. Here, we report that Pseudomonas syringae AvrPtoB, an effector with E3 ligase activity, can suppress ADR1-L1- and ADR1-L2-mediated cell death. ADR1, however, evades such suppression by diversification of two ubiquitination sites targeted by AvrPtoB. The intracellular sensor NLR SNC1 interacts with and guards the CCR domains of ADR1-L1 and ADR-L2. Removal of ADR1-L1 and ADR1-L2 or delivery of AvrPtoB activates SNC1, which then signals through ADR1 to trigger immunity. Our work not only uncovers the long sought-after physiological function of SNC1 in pathogen defense,but also that reveals how plants can use dual strategies, sequence diversification and a multiple layered guard-guardee system, to counteract pathogen attack on core immunity functions.

NLR receptors in plant immunity: making sense of the alphabet soup

“…This would be analogous to the TIR-NLR SNC1, which recognizes the effector AvrPtoB. By guarding ADR1-L1/L2 helpers targeted for suppression by AvrPtoB, SNC1 activates immune signaling via ADR1, a helper that is insensitive to AvrPtoB (preprint: Wang et al, 2023a;Fig 4D). Therefore, NLR suppressing effectors can be recognized and in addition, just like other important immune nodes, helper NLRs can be guarded by particular NLRs in order to prevent pathogen interference.…”

“…This effector‐mediated suppression of NLR signaling can be achieved by various mechanisms. Some effectors act indirectly by interfering with host proteins that contribute to NLR signaling pathways, while others act directly by physically interacting with NLRs to perturb their function (Lopez et al , 2019 ; Derevnina et al , 2021 ; Karki et al , 2021 ; preprint: Wang et al , 2023a ; Fig 4A and B ).…”

“…indicates that the exact mechanism by which these proteins (AVRcap1b and TOL9a) modulate the other proteins in the figure (NRC2/3, specifically), is not known. (D) The bacterial effector AvrPtoB can suppress ADR1‐L1 and ADR1‐L2 by acting as an E3 ligase, targeting these helper NLRs for degradation (preprint: Wang et al , 2023a ). AVRPtoB cannot suppress ADR1, another helper NLR.…”

“…A recent study on the bacterial effector AvrPtoB revealed that it can target helper NLRs in the NRG1/ADR1 network for degradation. AvrPtoB has E3 ligase activity and can ubiquitinate and promote degradation of ADR1‐L1, while having similar but milder effects on ADR1‐L2 (preprint: Wang et al , 2023a ). This activity suppresses ADR1‐L1 and ADR1‐L2‐mediated cell death (Fig 4D ).…”

Taking the lead: NLR immune receptor N‐terminal domains execute plant immune responses

“…As an example, emerging research demonstrates that the bacterial phytopathogen Pseudomonas syringae utilizes virulence effectors that disrupt TIR‐type (hopAM1, hopBY1) and RPW8‐type (AvrPtoB) NLR immune receptors (Eastman et al ., 2022 ; Hulin et al ., 2023 ; M.‐Y. Wang et al ., 2023 ). We therefore propose that an extended set of model hosts and pathogens is needed to fully leverage the evolutionary diversity of NLR‐mediated immune responses in plants.…”