NLRs guard metabolism to coordinate pattern- and effector-triggered immunity.

Pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) in plants enable them to respond to pathogens by activating the production of defence metabolites that orchestrate immune responses1-4. How the production of defence metabolites is promoted by immune receptors and coordinated with broad-spectrum resistance remains elusive. Here we identify the deubiquitinase PICI1 as an immunity hub for PTI and ETI in rice (Oryza sativa). PICI1 deubiquitinates and stabilizes methionine synthetases to activate methionine-mediated immunity principally through biosynthesis of the phytohormone ethylene. PICI1 is targeted for degradation by blast fungal effectors, including AvrPi9, to dampen PTI. Nucleotide-binding domain, leucine-rich-repeat-containing receptors (NLRs) in the plant immune system, such as PigmR, protect PICI1 from effector-mediated degradation to reboot the methionine-ethylene cascade. Natural variation in the PICI1 gene contributes to divergence in basal blast resistance between the rice subspecies indica and japonica. Thus, NLRs govern an arms race with effectors, using a competitive mode that hinges on a critical defence metabolic pathway to synchronize PTI with ETI and ensure broad-spectrum resistance.

Ca2+ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector.

Plant immunity is activated upon pathogen perception and often affects growth and yield when it is constitutively active. How plants fine-tune immune homeostasis in their natural habitats remains elusive. Here, we discover a conserved immune suppression network in cereals that orchestrates immune homeostasis, centering on a Ca2+-sensor, RESISTANCE OF RICE TO DISEASES1 (ROD1). ROD1 promotes reactive oxygen species (ROS) scavenging by stimulating catalase activity, and its protein stability is regulated by ubiquitination. ROD1 disruption confers resistance to multiple pathogens, whereas a natural ROD1 allele prevalent in indica rice with agroecology-specific distribution enhances resistance without yield penalty. The fungal effector AvrPiz-t structurally mimics ROD1 and activates the same ROS-scavenging cascade to suppress host immunity and promote virulence. We thus reveal a molecular framework adopted by both host and pathogen that integrates Ca2+ sensing and ROS homeostasis to suppress plant immunity, suggesting a principle for breeding disease-resistant, high-yield crops.

Molecular Basis of Disease Resistance and Perspectives on Breeding Strategies for Resistance Improvement in Crops.

Crop diseases are major factors responsible for substantial yield losses worldwide, which affects global food security. The use of resistance (R) genes is an effective and sustainable approach to controlling crop diseases. Here, we review recent advances on R gene studies in the major crops and related wild species. Current understanding of the molecular mechanisms underlying R gene activation and signaling, and susceptibility (S) gene-mediated resistance in crops are summarized and discussed. Furthermore, we propose some new strategies for R gene discovery, how to balance resistance and yield, and how to generate crops with broad-spectrum disease resistance. With the rapid development of new genome-editing technologies and the availability of increasing crop genome sequences, the goal of breeding next-generation crops with durable resistance to pathogens is achievable, and will be a key step toward increasing crop production in a sustainable way.

RRM Transcription Factors Interact with NLRs and Regulate Broad-Spectrum Blast Resistance in Rice.

Nucleotide-binding site leucine-rich repeat (NLR) receptors perceive pathogen effectors and trigger plant immunity. However, the mechanisms underlying NLR-triggered defense responses remain obscure. The recently discovered Pigm locus in rice encodes a cluster of NLRs, including PigmR, which confers broad-spectrum resistance to blast fungus. Here, we identify PIBP1 (PigmR-INTERACTING and BLAST RESISTANCE PROTEIN 1), an RRM (RNA-recognition motif) protein that specifically interacts with PigmR and other similar NLRs to trigger blast resistance. PigmR-promoted nuclear accumulation of PIBP1 ensures full blast resistance. We find that PIBP1 and a homolog, Os06 g02240, bind DNA and function as unconventional transcription factors at the promoters of the defense genes OsWAK14 and OsPAL1, activating their expression. Knockout of PIBP1 and Os06 g02240 greatly attenuated blast resistance. Collectively, our study discovers previously unappreciated RRM transcription factors that directly interact with NLRs to activate plant defense, establishing a direct link between transcriptional activation of immune responses with NLR-mediated pathogen perception.

A nucleotide-binding site-leucine-rich repeat receptor pair confers broad-spectrum disease resistance through physical association in rice.

Rice blast caused by Magnaporthe oryzae is the most destructive fungal disease in crops, greatly threatening rice production and food security worldwide. The identification and utilization of broad-spectrum resistance genes are considered to be the most economic and effective method to control the disease. In the past decade, many blast resistance ( R) genes have been identified, which mainly encode nucleotide-binding leucine-rich repeat (NLR) receptor family and confer limited race-specific resistance to the fungal pathogen. Resistance genes conferring broad-spectrum blast resistance are still largely lacking. In this study, we carried out a map-based cloning of the new blast R locus Pizh in variety ZH11. A bacterial artificial chromosome (BAC) clone of 165 kb spanning the Pizh locus was sequenced and identified 9 NLR genes, among which only Pizh-1 and Pizh-2 were expressed. Genetic complementation experiments indicated that Pizh-1 but not Pizh-2 alone could confer blast resistance. Intriguingly, both mutations on Pizh-1 and Pizh-2 by CRISPR-Cas9 abolished the Pizh-mediated resistance. We also observed that Pizh-1-mediated resistance was partially dependent on Pizh-2. Pizh-1 and Pizh-2 form a complex of NLRs through direct interaction. This suggests that Pizh-1 may function as the executor NLR and Pizh-2 as a 'helper' NLR that shares functional redundancy with other NLRs. Our current study provides not only a good tool for rice disease resistance breeding but also deep insight into NLR association and function in plant immunity. This article is part of the theme issue 'Biotic signalling sheds light on smart pest management'.

Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance.

Crop breeding aims to balance disease resistance with yield; however, single resistance (R) genes can lead to resistance breakdown, and R gene pyramiding may affect growth fitness. Here we report that the rice Pigm locus contains a cluster of genes encoding nucleotide-binding leucine-rich repeat (NLR) receptors that confer durable resistance to the fungus Magnaporthe oryzae without yield penalty. Among these NLR receptors, PigmR confers broad-spectrum resistance, whereas PigmS competitively attenuates PigmR homodimerization to suppress resistance. PigmS expression, and thus PigmR-mediated resistance, are subjected to tight epigenetic regulation. PigmS increases seed production to counteract the yield cost induced by PigmR Therefore, our study reveals a mechanism balancing high disease resistance and yield through epigenetic regulation of paired antagonistic NLR receptors, providing a tool to develop elite crop varieties.

An E3 Ubiquitin Ligase-BAG Protein Module Controls Plant Innate Immunity and Broad-Spectrum Disease Resistance.

Programmed cell death (PCD) and immunity in plants are tightly controlled to promote antimicrobial defense while preventing autoimmunity. However, the mechanisms contributing to this immune homeostasis are poorly understood. Here, we isolated a rice mutant ebr1 (enhanced blight and blast resistance 1) that shows enhanced broad-spectrum bacterial and fungal disease resistance, but displays spontaneous PCD, autoimmunity, and stunted growth. EBR1 encodes an E3 ubiquitin ligase that interacts with OsBAG4, which belongs to the BAG (Bcl-2-associated athanogene) family that functions in cell death, growth arrest, and immune responses in mammals. EBR1 directly targets OsBAG4 for ubiquitination-mediated degradation. Elevated levels of OsBAG4 in rice are necessary and sufficient to trigger PCD and enhanced disease resistance to pathogenic infection, most likely by activating pathogen-associated molecular patterns-triggered immunity (PTI). Together, our study suggests that an E3-BAG module orchestrates innate immune homeostasis and coordinates the trade-off between defense and growth in plants.