Abstract Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 . Since then, many cell-surface pattern recognition receptors (PRRs) have been identified, and R genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) have been cloned. Here, we provide a list of characterized PRRs and NLRs. In addition to immune receptors, many components of immune signaling networks were discovered over the last 30 years. We review the signaling pathways, physiological responses, and molecular regulation of both PRR- and NLR-mediated immunity. Recent studies have reinforced the importance of interactions between the two immune systems. We provide an overview of interactions between PRR- and NLR-mediated immunity, highlighting challenges and perspectives for future research.

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Thirty years of resistance: Zig-zag through the plant immune system

Abstract Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 . Since then, many cell-surface pattern recognition receptors (PRRs) have been identified, and R genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) have been cloned. Here, we provide a list of characterized PRRs and NLRs. In addition to immune receptors, many components of immune signaling networks were discovered over the last 30 years. We review the signaling pathways, physiological responses, and molecular regulation of both PRR- and NLR-mediated immunity. Recent studies have reinforced the importance of interactions between the two immune systems. We provide an overview of interactions between PRR- and NLR-mediated immunity, highlighting challenges and perspectives for future research. 

/pdf/oup-accepted-manuscript-1lfjzrt2.pdf

OUP accepted manuscript

The nucleotide-binding domain and leucine-rich repeats containing proteins (NLRs) serve as immune receptors in both plants and animals. Overaccumulation of NLRs often leads to autoimmune responses, suggesting that the levels of these immune receptors must be tightly controlled. However, the mechanism by which NLR protein levels are regulated is unknown. Here we report that the F-box protein CPR1 controls the stability of plant NLR resistance proteins. Loss-of-function mutations in CPR1 lead to higher accumulation of the NLR proteins SNC1 and RPS2, as well as autoactivation of immune responses. The autoimmune responses in cpr1 mutant plants can be largely suppressed by knocking out SNC1. Furthermore, CPR1 interacts with SNC1 and RPS2 in vivo, and overexpressing CPR1 results in reduced accumulation of SNC1 and RPS2, as well as suppression of immunity mediated by these two NLR proteins. Our data suggest that SKP1-CULLIN1-F-box (SCF) complex-mediated stability control of plant NLR proteins plays an important role in regulating their protein levels and preventing autoimmunity.

Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation

Plant immune responses are mainly activated by two types of receptor. Plasma membrane-localized pattern recognition receptors (PRRs) perceive extracellular microbial features, and nucleotide-binding leucine-rich repeat receptors (NLRs) recognize intracellular effector proteins from pathogens1. NLRs possessing N-terminal Toll/interleukin-1 receptor (TIR) domains activate defence responses via the NADase activity of the TIR domain2,3. Here we report that activation of TIR signalling plays a key role in PRR-mediated pattern-triggered immunity (PTI). TIR signalling mutants exhibit attenuated PTI responses and decreased resistance against pathogens. Consistently, PTI is compromised in plants with reduced NLR levels. Treatment with PTI elicitor flg22 or nlp20 rapidly induces many genes encoding TIR domain-containing proteins, which is likely to be responsible for activating TIR signalling during PTI. Overall, our study reveals that TIR signalling activation is an important mechanism for boosting plant defence during PTI.

Activation of TIR signalling boosts pattern-triggered immunity.

Plant immune networks

TIR signaling promotes the interactions between lipase-like proteins EDS1/PAD4 and ADR1-L1 immune receptor, and oligomerization of ADR1-L1.

TIR signal promotes interactions between lipase-like proteins and ADR1-L1 receptor and ADR1-L1 oligomerization

In both plants and animals, nucleotide-binding leucine-rich repeat (NLR) immune receptors perceive pathogen-derived molecules to trigger immunity. Global NLR homeostasis must be tightly controlled to ensure sufficient and timely immune output while avoiding aberrant activation, the mechanisms of which are largely unclear. In a previous reverse genetic screen, we identified two novel E3 ligases, SNIPER1 and its homolog SNIPER2, both of which broadly control the levels of NLR immune receptors in Arabidopsis. Protein levels of sensor NLRs (sNLRs) are inversely correlated with SNIPER1 amount and the interactions between SNIPER1 and sNLRs seem to be through the common nucleotide-binding (NB) domains of sNLRs. In support, SNIPER1 can ubiquitinate the NB domains of multiple sNLRs in vitro. Our study thus reveals a novel process of global turnover of sNLRs by two master E3 ligases for immediate attenuation of immune output to effectively avoid autoimmunity. Such unique mechanism can be utilized in the future for engineering broad-spectrum resistance in crops to fend off pathogens that damage our food supply.

https://www.embopress.org/doi/epdf/10.15252/embj.2020104915

Plant E3 ligases SNIPER1 and SNIPER2 broadly regulate the homeostasis of sensor NLR immune receptors.

Botrytis cinerea is one of the most destructive fungal pathogens affecting numerous plant hosts, including many important crop species. As a molecularly under-studied organism, its genome was only sequenced at the beginning of this century and it was recently updated with improved gene annotation and completeness. In this review, we summarize key molecular studies on B. cinerea developmental and pathogenesis processes, specifically on genes studied comprehensively with mutant analysis. Analyses of these studies have unveiled key genes in the biological processes of this pathogen, including hyphal growth, sclerotial formation, conidiation, pathogenicity and melanization. In addition, our synthesis has uncovered gaps in the present knowledge regarding development and virulence mechanisms. We hope this review will serve to enhance the knowledge of the biological mechanisms behind this notorious fungal pathogen.

The Destructive Fungal Pathogen Botrytis cinerea—Insights from Genes Studied with Mutant Analysis

Engineering plant disease resistance against biotrophic pathogens.

Both plants and animals use nucleotide-binding leucine-rich repeat (NLR) immune receptors to perceive pathogens and trigger immunity. Toll/interleukin-1 receptor (TIR)-type plant NLRs (TNLs) require the lipase-like protein family members Enhanced Disease Susceptibility 1 (EDS1)/ Phytoalexin Deficient 4 (PAD4)/ Senescence-Associated Gene 101 (SAG101) and helper NLRs (hNLRs) for downstream signaling, the biochemical mechanisms of which remain unclear. Here, we report that TIR signaling promotes the association of EDS1 and PAD4 with hNLR ACTIVATED DISEASE RESISTANCE 1-Like 1 (ADR1-L1), and the oligomerization of ADR1-L1s for downstream immune activation and cell death.

/pdf/tir-signaling-promotes-the-interactions-between-eds1-pad4-kbnk682ano.pdf

Xueru Liu

Papers

TIR signal promotes interactions between lipase-like proteins and ADR1-L1 receptor and ADR1-L1 oligomerization

Plant E3 ligases SNIPER1 and SNIPER2 broadly regulate the homeostasis of sensor NLR immune receptors.

The Destructive Fungal Pathogen Botrytis cinerea—Insights from Genes Studied with Mutant Analysis

Engineering plant disease resistance against biotrophic pathogens.

TIR signaling promotes the interactions between EDS1/PAD4 and ADR1-L1 and oligomerization of ADR1-L1