Pattern-triggered Immunity Signaling Research Articles

A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity.

Since signaling machineries for two modes of plant-induced immunity, pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), extensively overlap, PTI and ETI signaling likely interact. In an Arabidopsis quadruple mutant, in which four major sectors of the signaling network, jasmonate, ethylene, PAD4, and salicylate, are disabled, the hypersensitive response (HR) typical of ETI is abolished when the Pseudomonas syringae effector AvrRpt2 is bacterially delivered but is intact when AvrRpt2 is directly expressed in planta These observations led us to discovery of a network-buffered signaling mechanism that mediates HR signaling and is strongly inhibited by PTI signaling. We named this mechanism the ETI-Mediating and PTI-Inhibited Sector (EMPIS). The signaling kinetics of EMPIS explain apparently different plant genetic requirements for ETI triggered by different effectors without postulating different signaling machineries. The properties of EMPIS suggest that information about efficacy of the early immune response is fed back to the immune signaling network, modulating its activity and limiting the fitness cost of unnecessary immune responses.

RESISTANCE TO POWDERY MILDEW8.1 boosts pattern-triggered immunity against multiple pathogens in Arabidopsis and rice.

SummaryThe Arabidopsis gene RESISTANCE TO POWDERY MILDEW8.1 (RPW8.1) confers resistance to virulent fungal and oomycete pathogens that cause powdery mildew and downy mildew, respectively. However, the underlying mechanism remains unclear. Here, we show that ectopic expression of RPW8.1 boosts pattern‐triggered immunity (PTI) resulting in enhanced resistance against different pathogens in both Arabidopsis and rice. In Arabidopsis, transcriptome analysis revealed that ectopic expression of RPW8.1‐YFP constitutively up‐regulates expression of many pathogen‐associated molecular pattern (PAMP‐)‐inducible genes. Consistently, upon PAMP application, the transgenic line expressing RPW8.1‐YFP exhibited more pronounced PTI responses such as callose deposition, production of reactive oxygen species, expression of defence‐related genes and hypersensitive response‐like cell death. Accordingly, the growth of a virulent bacterial pathogen was significantly inhibited in the transgenic lines expressing RPW8.1‐YFP. Conversely, impairment of the PTI signalling pathway from PAMP cognition to the immediate downstream relay of phosphorylation abolished or significantly compromised RPW8.1‐boosted PTI responses. In rice, heterologous expression of RPW8.1‐YFP also led to enhanced resistance to the blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae) and the bacterial pathogen Xanthomonas oryzae pv. oryzae (Xoo). Taken together, our data suggest a surprising mechanistic connection between RPW8.1 function and PTI, and demonstrate the potential of RPW8.1 as a transgene for engineering disease resistance across wide taxonomic lineages of plants.

An incoherent feed-forward loop mediates robustness and tunability in a plant immune network.

Immune signaling networks must be tunable to alleviate fitness costs associated with immunity and, at the same time, robust against pathogen interferences. How these properties mechanistically emerge in plant immune signaling networks is poorly understood. Here, we discovered a molecular mechanism by which the model plant species Arabidopsis thaliana achieves robust and tunable immunity triggered by the microbe-associated molecular pattern, flg22. Salicylic acid (SA) is a major plant immune signal molecule. Another signal molecule jasmonate (JA) induced expression of a gene essential for SA accumulation, EDS5 Paradoxically, JA inhibited expression of PAD4, a positive regulator of EDS5 expression. This incoherent type-4 feed-forward loop (I4-FFL) enabled JA to mitigate SA accumulation in the intact network but to support it under perturbation of PAD4, thereby minimizing the negative impact of SA on fitness as well as conferring robust SA-mediated immunity. We also present evidence for evolutionary conservation of these gene regulations in the family Brassicaceae Our results highlight an I4-FFL that simultaneously provides the immune network with robustness and tunability in A.thaliana and possibly in its relatives.

Multiple Xanthomonas euvesicatoria Type III Effectors Inhibit flg22-Triggered Immunity.

Xanthomonas euvesicatoria is the causal agent of bacterial spot disease in pepper and tomato. X. euvesicatoria bacteria interfere with plant cellular processes by injecting effector proteins into host cells through the type III secretion (T3S) system. About 35 T3S effectors have been identified in X. euvesicatoria 85-10, and a few of them were implicated in suppression of pattern-triggered immunity (PTI). We used an Arabidopsis thaliana pathogen-free protoplast-based assay to identify X. euvesicatoria 85-10 effectors that interfere with PTI signaling induced by the bacterial peptide flg22. Of 33 tested effectors, 17 inhibited activation of a PTI-inducible promoter. Among them, nine effectors also interfered with activation of an abscisic acid-inducible promoter. However, effectors that inhibited flg22-induced signaling did not affect phosphorylation of mitogen-activated protein (MAP) kinases acting downstream of flg22 perception. Further investigation of selected effectors revealed that XopAJ, XopE2, and XopF2 inhibited activation of a PTI-inducible promoter by the bacterial peptide elf18 in Arabidopsis protoplasts and by flg22 in tomato protoplasts. The effectors XopF2, XopE2, XopAP, XopAE, XopH, and XopAJ inhibited flg22-induced callose deposition in planta and enhanced disease symptoms caused by attenuated Pseudomonas syringae bacteria. Finally, selected effectors were found to localize to various plant subcellular compartments. These results indicate that X. euvesicatoria bacteria utilize multiple T3S effectors to suppress flg22-induced signaling acting downstream or in parallel to MAP kinase cascades and suggest they act through different molecular mechanisms.

The GSK3/Shaggy-Like Kinase ASKα Contributes to Pattern-Triggered Immunity.

The first layer of immunity against pathogenic microbes relies on the detection of conserved pathogen-associated molecular patterns (PAMPs) that are recognized by pattern recognition receptors (PRRs) to activate pattern-triggered immunity (PTI). Despite the increasing knowledge of early PTI signaling mediated by PRRs and their associated proteins, many downstream signaling components remain elusive. Here, we identify the Arabidopsis (Arabidopsis thaliana) GLYCOGEN SYNTHASE KINASE3 (GSK3)/Shaggy-like kinase ASKα as a positive regulator of plant immune signaling. The perception of several unrelated PAMPs rapidly induced ASKα kinase activity. Loss of ASKα attenuated, whereas its overexpression enhanced, diverse PTI responses, ultimately affecting susceptibility to the bacterial pathogen Pseudomonas syringae Glucose-6-phosphate dehydrogenase (G6PD), the key enzyme of the oxidative pentose phosphate pathway, provides reducing equivalents important for defense responses and is a direct target of ASKα. ASKα phosphorylates cytosolic G6PD6 on an evolutionarily conserved threonine residue, thereby stimulating its activity. Plants deficient for or overexpressing G6PD6 showed a modified immune response, and the insensitivity of g6pd6 mutant plants to PAMP-induced growth inhibition was complemented by a phosphomimetic but not by a phosphonegative G6PD6 version. Overall, our data provide evidence that ASKα and G6PD6 constitute an immune signaling module downstream of PRRs, linking protein phosphorylation cascades to metabolic regulation.

Root-knot nematodes induce pattern-triggered immunity in Arabidopsis thaliana roots.

Root-knot nematodes (RKNs; Meloidogyne spp.) are plant parasites with a broad host range causing great losses worldwide. To parasitize their hosts, RKNs establish feeding sites in roots known as giant cells. The majority of work studying plant-RKN interactions in susceptible hosts addresses establishment of the giant cells and there is limited information on the early defense responses. Here we characterized early defense or pattern-triggered immunity (PTI) against RKNs in Arabidopsis thaliana. To address PTI, we evaluated known canonical PTI signaling mutants with RKNs and investigated the expression of PTI marker genes after RKN infection using both quantitative PCR and β-glucuronidase reporter transgenic lines. We showed that PTI-compromised plants have enhanced susceptibility to RKNs, including the bak1-5 mutant. BAK1 is a common partner of distinct receptors of microbe- and damage-associated molecular patterns. Furthermore, our data indicated that nematode recognition leading to PTI responses involves camalexin and glucosinolate biosynthesis. While the RKN-induced glucosinolate biosynthetic pathway was BAK1-dependent, the camalexin biosynthetic pathway was only partially dependent on BAK1. Combined, our results indicate the presence of BAK1-dependent and -independent PTI against RKNs in A.thaliana, suggesting the existence of diverse nematode recognition mechanisms.

Enhancing crop innate immunity: new promising trends.

Plants are constantly exposed to potentially pathogenic microbes present in their surrounding environment. Due to the activation of the pattern-triggered immunity (PTI) response that largely relies on accurate detection of pathogen- or microbe-associated molecular patterns by pattern-recognition receptors (PRRs), plants are resistant to the majority of potential pathogens. However, adapted pathogens may avoid recognition or repress plant PTI and resulting diseases significantly affect crop yield worldwide. PTI provides protection against a wide range of pathogens. Reinforcement of PTI through genetic engineering may thus generate crops with broad-spectrum field resistance. In this review, new approaches based on fundamental discoveries in PTI to improve crop immunity are discussed. Notably, we highlight recent studies describing the interfamily transfer of PRRs or key regulators of PTI signaling.

Plant immune response to pathogens differs with changing temperatures

Temperature fluctuation is a key determinant for microbial invasion and host evasion. In contrast to mammals that maintain constant body temperature, plant temperature oscillates on a daily basis. It remains elusive how plants operate inducible defenses in response to temperature fluctuation. Here we report that ambient temperature changes lead to pronounced shifts of the following two distinct plant immune responses: pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). Plants preferentially activate ETI signaling at relatively low temperatures (10-23 °C), whereas they switch to PTI signaling at moderately elevated temperatures (23-32 °C). The Arabidopsis arp6 and hta9hta11 mutants, phenocopying plants grown at elevated temperatures, exhibit enhanced PTI and yet reduced ETI responses. As the secretion of bacterial effectors favours low temperatures, whereas bacteria multiply vigorously at elevated temperatures accompanied with increased microbe-associated molecular pattern production, our findings suggest that temperature oscillation might have driven dynamic co-evolution of distinct plant immune signaling responding to pathogen physiological changes.

The peptide growth factor, phytosulfokine, attenuates pattern‐triggered immunity

Pattern-triggered immunity (PTI) is triggered by recognition of elicitors called microbe-associated molecular patterns (MAMPs). Although immune responses may provide good protection of plants from pathogen attack, excessive immune responses have negative impacts on plant growth and development. Thus, a good balance between positive and negative effects on the immune signaling network is important for plant fitness. However, little information is known about the molecular mechanisms that are involved in attenuation of PTI. Here, we describe a growth-promoting peptide hormone, phytosulfokine (PSK), as attenuating PTI signaling in Arabidopsis. This research was motivated by the observation that expression of the PSK Receptor 1 (PSKR1) gene was induced by MAMP treatment. Plants homozygous for pskr1 T-DNA insertions showed enhanced defense gene expression and seedling growth inhibition triggered by MAMPs. The pskr1 plants also showed enhanced PTI against the bacterial pathogen Pseudomonas syringae. These results indicate that the PSKR-mediated signaling attenuates immune responses. Tyrosyl protein sulfotransferase (TPST) is an enzyme required for production of the mature sulfated PSK. Like pskr1 mutants, a tpst T-DNA insertion line exhibited enhanced MAMP-triggered seedling growth inhibition, which was suppressed by exogenous application of PSK. Thus, PSK signaling mediated by PSKR1 attenuates PTI but stimulates growth.

Physical association of pattern‐triggered immunity (PTI) and effector‐triggered immunity (ETI) immune receptors in Arabidopsis

Plants possess two distinct types of immune receptor. The first type, pattern recognition receptors (PRRs), recognizes microbe-associated molecular patterns (MAMPs) and initiates pattern-triggered immunity (PTI) on recognition. FLS2 is a PRR, which recognizes a part of bacterial flagellin. The second type, resistance (R) proteins, recognizes pathogen effectors and initiates effector-triggered immunity (ETI) on recognition. RPM1, RPS2 and RPS5 are R proteins. Here, we provide evidence that FLS2 is physically associated with all three R proteins. Our findings suggest that signalling interactions occur between PTI and ETI at very early stages and/or that FLS2 forms a PTI signalling complex, some components of which are guarded by R proteins.