Parasite effectors target helper NLRs in plants to suppress immunity-related cell death

Abstract

Parasites target the plant immune system for successful colonization. A new study in PLOS Biology reveals that unrelated parasites have evolved effectors that specifically suppress the function of helper nucleotide-binding leucine-rich repeats (NLRs), explaining the complex plant-parasite coevolutionary dynamics.Plants have evolved a robust innate immune system to defend against a large number of parasites present in their ecological niche [1]. The plant's first layer of defense involves detection of conserved pathogen/microbe-associated molecular patterns (PAMPs/MAMPs) leading to pattern-triggered immunity (PTI). Parasites have evolved to sense and suppress PTI by secreting virulence factors called effectors into plant cells. Plants have evolved to recognize parasiteencoded effectors via the nucleotide-binding leucine-rich repeat (NLR) class of immune receptors and activate more robust effector-triggered immunity (ETI), which ultimately leads to cell death at the site of infection called the hypersensitive response (HR) [1] (Fig 1). This serves to starve out parasites and prevent further colonization. The plant genome encodes a large number of NLRs [2,3]. The NLRs that are involved in the recognition of parasite effectors either directly or indirectly are classified as sensor NLRs [2,4,5] (Fig 1). Accumulating evidence indicates that some sensor NLRs require the function of other NLRs, referred to as helper NLRs, to activate downstream immune signaling and cell death induction [4,5] (Fig 1). To date, there are 3 described helper NLR families: the Activated Disease Resistance 1 (ADR1) family, the N Requirement Gene 1 (NRG1) family, and NB-LRR protein required for HR-associated cell death (NRC) family [6].The Solanaceae-specific NRC family is required for the function of a large number of CCtype sensor NLRs that confer resistance to a diverse array of parasites [4,5]. An emerging model shows that NRCs and their sensor NLR partners form a complex genetic network, in which NRCs form redundant central nodes and also exhibit some specificity toward their sensor NLR partners. For example, the sensor NLR Prf requires NRC2 and NRC3 to confer resistance to Pseudomonas syringae bacteria, AU : Anabbreviationlisthasbeencompiledforthoseusedthrougho but NLR Rpi-blb2 only requires NRC4 to confer resistance to potato blight caused by the oomycete pathogen Phytophthora infestans [4,5]. Furthermore, Rx requires NRC2, NRC3, and NRC4 in a genetically redundant manner to confer resistance to Potato virus X (PVX). Given that some helper NLRs are points of convergence in downstream signaling of multiple upstream sensor NLRs, they would be ideal targets for parasite effectors to overcome NLR-mediated ETI.

Nucleotide‐binding leucine‐rich repeat network underlies nonhost resistance of pepper against the Irish potato famine pathogen Phytophthora infestans

“…A number of NLRs have been identified and the majority depend on helper NLRs such as NRCs, NRG1, and ADR1 for their function (Kamoun et al ., 2018 ; Ngou et al ., 2022 ). Thus, helper NLRs could be ideal targets for pathogens to efficiently overcome multiple NLR‐mediated immune responses of plants (Li et al ., 2021 ). Divergent pathogens possess multiple effectors that function as suppressors of helper NLRs, such as Avrcab1b of P. infestans and SS17 of nematodes that suppresses NbNRC2/3 (Derevnina et al ., 2021 ).…”

An Overview of PRR- and NLR-Mediated Immunities: Conserved Signaling Components across the Plant Kingdom That Communicate Both Pathways

“…The autoimmunity observed in some of these mutants is caused by the activation of multiple NLRs [ 121 , 122 , 123 ]. Accordingly, the activation of NLR sensors is a consequence of modifications or deletions of the monitored cellular component (guardee or a decoy), which is either a key node within the PTI- or the ETI-mediated immunity [ 124 , 125 ]. For instance, the HR-like cell death observed in bak1 bkk1 is caused by the activation of NLR-mediated ETI rather than the reduction of PTI [ 126 , 127 ].…”