NLR network mediates immunity to diverse plant pathogens

Abstract

Both plants and animals rely on nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins to respond to invading pathogens and activate immune responses. An emerging concept of NLR function is that "sensor" NLR proteins are paired with "helper" NLRs to mediate immune signaling. However, our fundamental knowledge of sensor/helper NLRs in plants remains limited. In this study, we discovered a complex NLR immune network in which helper NLRs in the NRC (NLR required for cell death) family are functionally redundant but display distinct specificities toward different sensor NLRs that confer immunity to oomycetes, bacteria, viruses, nematodes, and insects. The helper NLR NRC4 is required for the function of several sensor NLRs, including Rpi-blb2, Mi-1.2, and R1, whereas NRC2 and NRC3 are required for the function of the sensor NLR Prf. Interestingly, NRC2, NRC3, and NRC4 redundantly contribute to the immunity mediated by other sensor NLRs, including Rx, Bs2, R8, and Sw5. NRC family and NRC-dependent NLRs are phylogenetically related and cluster into a well-supported superclade. Using extensive phylogenetic analysis, we discovered that the NRC superclade probably emerged over 100 Mya from an NLR pair that diversified to constitute up to one-half of the NLRs of asterids. These findings reveal a complex genetic network of NLRs and point to a link between evolutionary history and the mechanism of immune signaling. We propose that this NLR network increases the robustness of immune signaling to counteract rapidly evolving plant pathogens.immunity | host-microbe interactions | evolution

The intracellular nucleotide‐binding leucine‐rich repeat receptor (SlNRC4a) enhances immune signalling elicited by extracellular perception

“…Both Solyc04g007070 and Solyc04g007060 belong to clade CNL‐14 of tomato, which contains 240 NLRs (Andolfo et al, ). Three members of this clade have been previously studied and reported as SlNRC1‐3 (for NLR protein required for HR‐associated cell death) (Gabriels et al, ; Wu et al, ). Recently, two NRC members from N .…”

“…An emerging concept proposes that NLRs can function together, where “sensor” NLR proteins require “helper” NLRs to initiate immune signalling (Cesari, Bernoux, Moncuquet, Kroj, & Dodds, ). Recently, exciting work by Wu et al () demonstrated that NbNRC family members are “helper” NLRs, required for the function of multiple “sensor” CNLs with various degrees of redundancy and specificity, creating a complex signalling network (Wu et al, ). NbNRC4s were required for the function of the Rpi‐blb2, Mi‐1.2, and R1 sensor CNLs (Wu et al, ).…”

“…In Arabidopsis thaliana , TNLs form the largest group of NLRs (Yu et al, ), whereas most solanaceous NLRs belong to the CNL class (Andolfo et al, ). Recently, the NLR protein required for hypersensitive response (HR)‐associated cell death (NRC) family of NLRs has been demonstrated to act as helper NLRs that contribute to sensor NLR perception in solanaceous plants (Gabriels et al, ; Wu et al, ). NbNRC4 in particular has been demonstrated to be a helper NLR that contributes to immunity mediated by sensor NLRs that perceive distinct effectors from bacterial, viral, filamentous nematodes, and insect pathogens and pests (Wu et al, ).…”

“…Recently, the NLR protein required for hypersensitive response (HR)‐associated cell death (NRC) family of NLRs has been demonstrated to act as helper NLRs that contribute to sensor NLR perception in solanaceous plants (Gabriels et al, ; Wu et al, ). NbNRC4 in particular has been demonstrated to be a helper NLR that contributes to immunity mediated by sensor NLRs that perceive distinct effectors from bacterial, viral, filamentous nematodes, and insect pathogens and pests (Wu et al, ). Within plant genomes, NLRs are organized either as isolated genes or as linked clusters that are thought to enable rapid evolution of intracellular immune receptors (McDowell & Simon, ).…”

“…Here, we report the isolation and identification of a tomato LeEIX2‐associated NLR protein that is a member of the NRC family. We have named this protein SlNRC4a according to its close orthologs in Nicotiana benthamiana (NbNRC4a,b) (Wu et al, ). Here, we show an intriguing and noncanonical involvement of SlNRC4a in PTI, as a positive regulator of LeEIX2/EIX‐mediated defence responses.…”