Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor"immune receptor functions.

Isai Salas-Gonzáles,Farid El Kasmi,Svenja C Saile,Xinnian Dong,Lance M Jubic,Baptiste Castel,Jonathan D G Jones,Marcel Bäcker,Pierre Jacob,Jeffery L Dangl

doi:10.1371/journal.pbio.3000783

Abstract

Plant nucleotide-binding (NB) leucine-rich repeat (LRR) receptor (NLR) proteins function as intracellular immune receptors that perceive the presence of pathogen-derived virulence proteins (effectors) to induce immune responses. The 2 major types of plant NLRs that "sense" pathogen effectors differ in their N-terminal domains: these are Toll/interleukin-1 receptor resistance (TIR) domain-containing NLRs (TNLs) and coiled-coil (CC) domain-containing NLRs (CNLs). In many angiosperms, the RESISTANCE TO POWDERY MILDEW 8 (RPW8)-CC domain containing NLR (RNL) subclass of CNLs is encoded by 2 gene families, ACTIVATED DISEASE RESISTANCE 1 (ADR1) and N REQUIREMENT GENE 1 (NRG1), that act as "helper" NLRs during multiple sensor NLR-mediated immune responses. Despite their important role in sensor NLR-mediated immunity, knowledge of the specific, redundant, and synergistic functions of helper RNLs is limited. We demonstrate that the ADR1 and NRG1 families act in an unequally redundant manner in basal resistance, effector-triggered immunity (ETI) and regulation of defense gene expression. We define RNL redundancy in ETI conferred by some TNLs and in basal resistance against virulent pathogens. We demonstrate that, in Arabidopsis thaliana, the 2 RNL families contribute specific functions in ETI initiated by specific CNLs and TNLs. Time-resolved whole genome expression profiling revealed that RNLs and "classical" CNLs trigger similar transcriptome changes, suggesting that RNLs act like other CNLs to mediate ETI downstream of sensor NLR activation. Together, our genetic data confirm that RNLs contribute to basal resistance, are fully required for TNL signaling, and can also support defense activation during CNL-mediated ETI.

Highlights

Plant defense responses, once initiated, thwart attacking and invading pathogens via multiple mechanisms [1,2]
It has been reported that the ACTIVATED DISEASE RESISTANCE 1 (ADR1) and N REQUIREMENT GENE 1 (NRG1) function downstream of some TNLs [11,12,13,14,27], we lack a detailed comparison of the different requirements for the ADR1s and NRG1s during TNL-mediated effector-triggered immunity (ETI)
Recognition of pathogen-derived effectors by intracellular sensor NB LRR receptor (NLR) triggers ETI, in many cases a strong immune response eventually leading to disease resistance and to hypersensitive response (HR)

Summary

Introduction

Once initiated, thwart attacking and invading pathogens via multiple mechanisms [1,2]. Microbial pathogens can trigger a first defense response upon detection by plasma membrane (PM)-localized leucine-rich repeat (LRR) receptor kinases (RKs) or receptor-like proteins (RLPs). The Toll/interleukin-1 receptor resistance (TIR) domain-containing NLRs (TNLs) and the coiled-coil (CC) domain-containing NLRs (CNLs) can directly or indirectly sense the presence of pathogen effectors [9] They are usually designated “sensor” NLRs. Further, there is a unique subclade of CNLs that exhibit an atypical CC-R N-terminal domain sequence-related to the resistance protein RESISTANCE TO POWDERY MILDEW 8 (RPW8), termed RNLs. RNLs are required for the function of many sensor NLRs and are referred to as helper NLRs [10,11,12,13,14,15]. CNL and TNL activation by effectors may involve NLR oligomerization—the formation of a so-called resistosome—that is required for NLR function in immunity, as was shown for the Arabidopsis thaliana CNL HOPZ-ACTIVATED RESISTANCE 1 (ZAR1) [16,17,18,19]

Methods

Results

Conclusion