A better mousetrap to guard against anthracnose disease in bean

Nature Immunology, 2006

Plant proteins belonging to the nucleotide-binding site-leucine-rich repeat (NBS-LRR) family are used for pathogen detection. Like the mammalian Nod-LRR protein 'sensors' that detect intracellular conserved pathogen-associated molecular patterns, plant NBS-LRR proteins detect pathogen-associated proteins, most often the effector molecules of pathogens responsible for virulence. Many virulence proteins are detected indirectly by plant NBS-LRR proteins from modifications the virulence proteins inflict on host target proteins. However, some NBS-LRR proteins directly bind pathogen proteins. Association with either a modified host protein or a pathogen protein leads to conformational changes in the amino-terminal and LRR domains of plant NBS-LRR proteins. Such conformational alterations are thought to promote the exchange of ADP for ATP by the NBS domain, which activates 'downstream' signaling, by an unknown mechanism, leading to pathogen resistance.

Plants activate an immune response in defense against microbial pathogens. The first layer of immunity consists in the recognition of microbial fingerprints, called Pathogen Associated Molecular Pattern (PAMP), by a set of Pattern Recognition Receptors (PRR). In addition, the degradation products from fungi, bacteria and plant cells are recognised as Damage Associated Molecular Pattern (DAMP). The first layer of plant defence is based on Pattern Recognition Receptors (PRR) on the membrane. These receptors, either receptor kinases or receptor-like proteins (RLPs), associating with cytoplasmic kinases, recognize the presence of PAMPs, thus activating a local response named PAMP-triggered immunity (PTI), that is not strong but effective towards many pathogen species. Here we discuss and focus on Elongation Factor Tu Receptors (EFR) and flagellin sensing (FLS) receptors. In leucine-rich repeat (LRR) receptor proteins, the hydrophobic LLR domains are exposed on external membranes, providing the protein-protein interaction modules. Plants evolved this protein-protein interaction domain several times during the development of mechanisms to defend themselves from viruses, virulence factors, enzymes and effectors of bacterial and fungal pathogens. Pathogens in addition evolved proteins and enzymes that are injected in the plant cell to counterfight plant immune signaling pathways. These effectors are recognised by plant receptors sensing their presence of their cognate avirulence genes. These receptors originated from recombination during evolution and only occur in some specific tomato genotypes, instead of the widely occurring PPRs. Effector Triggered Immunity (ETI) allows a plant response to effector proteins that is more strong, but is race specific. It leads to local necrosis and apoptosis, and to the establishment of the hypersensitive response (HR). For biotrophic or hemibiotrophic pathogens, necrosis is an effective way to limit their spread, while for necrotrophic pathogens this is not efficient and sufficient way to limit their spread, since depends on the timing of infection and on the plant development phase. Pathogenic fungi strategy relies on the formation of specialised structures, or haustoria, that facilitate the nutrient uptake form plant cells. In this review, we summarize the most recent knowledge on plant pathogens and the mechanisms they evolved to circumvent plant defences among which pathogen effectors, protein decoys inactivating plant defence signals. Effectors are recognised through their binding to plant proteins by means of plant receptors, that activate the Effector Triggered Immunity (ETI). In particular, we focus on the Solanaceae, discussing general mechanisms and specific pathways that confer resistance to various pathogens. There is an arm race between plants and fungal and bacterial pathogens that has led to new protein variants and protein decoys (pseudokinases, inhibitors and sponges blocking glucanases, and Transcription Activator Like Effectors). Advances in understanding the function of pathogen effectors will provide new ways to improve plant immunity and mechanisms of defence against their pests. Finally, we present possible combinations of interventions, from gene engineering to chemical priming, acting on signaling pathways regulated by jasmonate and salicylate hormones, to increase plant resistance and activate plant defences without affecting crop yields.

Current Opinion in Plant Biology, 2019

Plant nucleotide-binding domain and leucine-rich repeatcontaining (NLR) proteins function as intracellular receptors in response to pathogens and activate effector-triggered immune responses (ETI). The activation of some sensor NLRs (sNLR) by their corresponding pathogen effector is well studied. However, the mechanisms by which the recently defined helper NLRs (hNLR) function to transduce sNLR activation into ETIassociated cell death and disease resistance remains poorly understood. We briefly summarize recent examples of sNLR activation and we then focus on hNLR requirements in sNLRinitiated immune responses. We further discuss how shared sequence homology with fungal self-incompatibility proteins and the mammalian mixed lineage kinase domain like pseudokinase (MLKL) proteins informs a plausible model for the structure and function of an ancient clade of plant hNLRs, called RNLs.

Cell, 1997

2017

A diversity of plant-associated organisms secrete effectors—proteins and metabolites that modulate plant physiology to favor host infection and colonization. However, effectors can also activate plant immune receptors, notably nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins, enabling plants to fight off invading organisms. This interplay between effectors, their host targets, and the matching immune receptors is shaped by intricate molecular mechanisms and exceptionally dynamic coevolution. In this article, we focus on three effectors, AVR-Pik, AVR-Pia, and AVR-Pii, from the rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae), and their corresponding rice NLR immune receptors, Pik, Pia, and Pii, to highlight general concepts of plant-microbe interactions. We draw 12 lessons in effector and NLR biology that have emerged from studying these three little effectors and are broadly applicable to other plant-microbe systems.

Biotechnology Research and Innovation, 2019

In order to meet global food security demands in the next decades, considerable changes are required for sustainable agriculture in the context of plant disease, with sufficient food production depending on the development of durable genetically disease resistant crops. For this, further advances are required in our understanding of the plant innate immune system and how plants respond to invading pathogenic microorganisms. Over the past 20 years, considerable research has been conducted into the characterization and cloning of plant nucleotide-binding, leucine-rich repeat (NLR) immune receptors. These intracellular receptors can recognize directly or indirectly pathogen effector proteins, resulting in effector-triggered immunity (ETI). Elucidation, however, of the diversity of NLR resistance gene families and the molecular basis of NLR-driven effector recognition and defense signaling is incomplete. Here, we present a summary of the understanding of NLR structure, function, genomic organization and diversity in plants. Recent advances in target enrichment approaches for NLR characterization and function validation are highlighted in the context of NLR engineering possibilities for accelerated durable genetic resistance to biotic stresses.

There is an arm race between plants and their pathogens, by fungi, and bacteria, as well as between plants and insects. Plant proteases are hydrolytic enzymes, grouped on the basis of the catalytic amino acid, as serine, cysteine, aspartic acid, or metal dependent activity. Plant-fungi interactions, as well as plants with other invaders, have been elucidated in recent years, showing an evolutionary adaptation of hosts and invaders to produce proteases and evolve new protease inhibitors. Interactions between protease inhibitors and the target proteases provide information on the ways organisms interact and defend themselves from pathogens, recognizing symbionts from parasite organisms. A comparative analysis of protease inhibitors in plants with sequenced genomes have been recently performed. In the analysis of PIs, protease biochemical assays, protein-protein interaction studies and protease chips were used to analyze constitutive and inducible inhibitors under different conditions. Recently, activity-based protease profiling (ABPP) was used to differentiate enzymes tissue specificity, and roles in various physiological and pathological states. Specificities of PIs toward different protease (serine and cysteine proteases) can allow to selectively and differentially bind and detect various proteases. In this review we summarize the most recent knowledge on plant pathogens and the mechanisms they evolved to circumvent plant defences among which pathogen effectors, proteases and proteases inhibitors. Finally, we introduce the recent findings on pathogen bodyguards, proteins interfering with plant defence mechanisms or decoys, mimicking Transcription Activator Like Effectors (TALE). It is envisaged that further advances in understanding the function of pathogen effectors will provide new ways to improve plant immunity and mechanisms of defence against their pests.

Current Opinion in Plant Biology, 2004

Most plant disease resistance (R) proteins contain a series of leucine-rich repeats (LRRs), a nucleotide-binding site (NBS), and a putative amino-terminal signaling domain. They are termed NBS-LRR proteins. The LRRs of a wide variety of proteins from many organisms serve as protein interaction platforms, and as regulatory modules of protein activation. Genetically, the LRRs of plant R proteins are determinants of response specificity, and their action can lead to plant cell death in the form of the familiar hypersensitive response (HR). A total of 149 R genes are potentially expressed in the Arabidopsis genome, and plant cells must deal with the difficult task of assembling many of the proteins encoded by these genes into functional signaling complexes. Eukaryotic cells utilize several strategies to deal with this problem. First, proteins are spatially restricted to their sub-cellular site of function, thus improving the probability that they will interact with their proper partners. Second, these interactions are architecturally organized to avoid inappropriate signaling events and to maintain the fidelity and efficiency of the response when it is initiated. Recent results provide new insights into how the signaling potential of R proteins might be created, managed and held in check until specific stimulation following infection. Nevertheless, the roles of the R protein partners in these regulatory events that have been defined to date are unclear.

Journal of Receptors and Signal Transduction, 1997

Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues Vol. III, 2006

Plants have evolved sophisticated innate immunity system to resist constant attacks from microbes. This system consists of multi-layered defense programs. Milestone advances have been achieved in the last fifteen years towards an understanding of the molecular mechanisms by which plants recognize the invading microbes and activate appropriate defense programs. Over 60 plant disease resistance (R) genes have been cloned from model and crop species. The majority of these genes encode proteins containing domains (e.g. "TIR", "NBS" and "LRR") that appear to be conserved in the plant and animal kingdoms for innate immunity function. The molecular basis for the long-standing enigma of the so called "gene-for-gene" interaction between a plant R protein and a cognate pathogen-encoded effector is being elucidated with increasing evidence for a recent model-the "guard hypothesis": Plant R proteins are part of a protein complex that functions in the plant surveillance system to detect the activities of pathogen effectors inside the host cell, rather than receptors for the pathogen-derived ligands. Many components of the complex defense signaling pathways have been identified and characterized. Moreover, biochemical cascades involved in some of the genetically defined signaling steps are being revealed. Finally, with more R genes and regulatory components of the innate immunity system are being characterized, greater efforts are to be made in exploiting plant natural disease resistance through genetic engineering of plant R genes and their signaling pathways.