PAMP recognition and the plant-pathogen arms race

Plants have evolved systems analogous to animal innate immunity that recognise pathogen-associated molecular patterns (PAMPs). PAMP detection is an important component of non-host resistance in plants and serves as an early warning system for the presence of potential pathogens. Binding of a PAMP to the appropriate pattern recognition receptor leads to downstream signalling events and, ultimately, to the induction of basal defence systems. To overcome non-host resistance, pathogens have evolved effectors that target specific regulatory components of the basal defence system. In turn, this has led to the evolution in plants of cultivar-specific resistance mediated by R proteins, which guard the targets of effectors against pathogen manipulation; the arms race continues.     

Toward understanding of rice innate immunity against Magnaporthe oryzae

The blast fungus, Magnaporthe oryzae, causes serious disease on a wide variety of grasses including rice, wheat and barley. The recognition of pathogens is an amazing ability of plants including strategies for displacing virulence effectors through the adaption of both conserved and variable pathogen elicitors. The pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) were reported as two main innate immune responses in plants, where PTI gives basal resistance and ETI confers durable resistance. The PTI consists of extracellular surface receptors that are able to recognize PAMPs. PAMPs detect microbial features such as fungal chitin that complete a vital function during the organism’s life. In contrast, ETI is mediated by intracellular receptor molecules containing nucleotide-binding (NB) and leucine rich repeat (LRR) domains that specifically recognize effector proteins produced by the pathogen. To enhance crop resistance, understanding the host resistance mechanisms against pathogen infection strategies and having a deeper knowledge of innate immunity system are essential. This review summarizes the recent advances on the molecular mechanism of innate immunity systems of rice against M. oryzae. The discussion will be centered on the latest success reported in plant–pathogen interactions and integrated defense responses in rice.     

Toll-like receptors control autophagy

Autophagy is a newly recognized innate defense mechanism, acting as a cell-autonomous system for elimination of intracellular pathogens. The signals and signalling pathways inducing autophagy in response to pathogen invasion are presently not known. Here we show that autophagy is controlled by recognizing conserved pathogen-associated molecular patterns (PAMPs). We screened a PAMP library for effects on autophagy in RAW 264.7 macrophages and found that several prototype Toll-like receptor (TLR) ligands induced autophagy. Single-stranded RNA and TLR7 generated the most potent effects. Induction of autophagy via TLR7 depended on MyD88 expression. Stimulation of autophagy with TLR7 ligands was functional in eliminating intracellular microbes, even when the target pathogen was normally not associated with TLR7 signalling. These findings link two innate immunity defense systems, TLR signalling and autophagy, provide a potential molecular mechanism for induction of autophagy in response to pathogen invasion, and show that the newly recognized ability of TLR ligands to stimulate autophagy can be used to treat intracellular pathogens.     

Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells

PAMP (pathogen-associated molecular pattern) recognition plays an important role during the innate immune response in both plants and animals. Lipopolysaccharides (LPS) derived from Gram-negative bacteria are representative of typical PAMP molecules and have been reported to induce defense-related responses, including the suppression of the hypersensitive response, the expression of defense genes and systemic resistance in plants. However, the details regarding the precise molecular mechanisms underlying these cellular responses, such as the molecular machinery involved in the perception and transduction of LPS molecules, remain largely unknown. Furthermore, the biological activities of LPS on plants have so far been reported only in dicots and no information is thus available regarding their functions in monocots. In our current study, we report that LPS preparations for various becteria, including plant pathogens and non-pathogens, can induce defense responses in rice cells, including reactive oxygen generation and defense gene expression. In addition, global analysis of gene expression induced by two PAMPs, LPS and chitin oligosaccharide, also reveals a close correlation between the gene responses induced by these factors. This indicates that there is a convergence of signaling cascades downstream of their corresponding receptors. Furthermore, we show that the defense responses induced by LPS in the rice cells are associated with programmed cell death (PCD), which is a finding that has not been previously reported for the functional role of these molecules in plant cells. Interestingly, PCD induction by the LPS was not detected in cultured Arabidopsis thaliana cells.     

水稻免疫机制研究进展

植物先天免疫主要由两部分组成：一类是通过细胞膜上的病原菌分子模式识别受体识别病原微生物表面存在的分子特征激发的免疫反应（PTI）;另一类是专化性的抗病R蛋白识别病原微生物的效应蛋白,从而激发下游的病原菌小种特异性的防卫反应过程（ETI）．随着水稻抗病信号途径中越来越多的抗病基因以及关键的调控基因被克隆和功能鉴定,同时多种水稻病原菌效应蛋白的发现,水稻抗病机理的研究也越来越深入．本文阐述了水稻的PTI,ETI及其下游参与免疫信号转导的关键性组分,从而形成一个初步的水稻免疫调控网络．     

Self/nonself perception and recognition mechanisms in plants: a comparison of self-incompatibility and innate immunity

Analyses of emerging concepts indicate that parallels exist between self-incompatibility and pathogen recognition. In the case of surveillance of 'nonself', plant immune responses are triggered either by pattern recognition receptors (PRRs) that detect conserved pathogen-associated molecular patterns (PAMPs) or by resistance (R) proteins recognizing isolate-specific pathogen effectors. PAMP detection is an important component of innate immunity in plants and serves as an early warning system for the presence of potential pathogens and activation of plant defense mechanisms. In the Brassicaceae, the recognition of 'self' and self-incompatibility are components of a receptor-ligand based mechanism that utilizes an S receptor kinase (SRK) to perceive and reject 'self'-pollen. SRK is an S-domain receptor-like kinase (RLK), which in turn is part of the RLK family, some members of which represent PRRs involved in the detection of PAMPs. S-domain RLKs also occur in species that do not exhibit self-incompatibility and are up-regulated in response to wounding, PAMPs and pathogen recognition. Although evolution may have driven expansion of certain RLK families to serve roles in particular physiological processes, this may not exclude these receptor types from functioning in different programs. Recent findings on self/nonself recognition are reviewed and conceptual and mechanistic links between microbial recognition and self-incompatibility are discussed.     

Impaired fungicide activity in plants blocked in disease resistance signal transduction.

Fungicide action is generally assumed to be dependent on an antibiotic effect on a target pathogen, although a role for plant defense mechanisms as mediators of fungicide action has not been excluded. Here, we demonstrate that in Arabidopsis, the innate plant defense mechanism contributes to the effectiveness of fungicides. In NahG and nim1 (for noninducible immunity) Arabidopsis plants, which normally exhibit increased susceptibility to pathogens, the fungicides metalaxyl, fosetyl, and Cu(OH)2 are much less active and fail to control Peronospora parasitica. In contrast, the effectiveness of these fungicides is not altered in Arabidopsis mutants defective in the ethylene or jasmonic acid signal transduction pathways. Application of the systemic acquired resistance activator benzothiadiazole (BTH) in combination with these fungicides results in a synergistic effect on pathogen resistance in wild-type plants and an additive effect in NahG and BTH-unresponsive nim1 plants. Interestingly, BTH treatment normally induces long-lasting pathogen protection; however, in NahG plants, the protection is transient. These observations suggest that BTH treatment can compensate only partially for an impaired signal transduction pathway and support the idea that pathogen defense mechanisms are under positive feedback control. These observations are strikingly reminiscent of the reduced efficacy of antifungal agents in immunocompromised animals.     

昆虫先天性免疫信号通路研究进展

昆虫体内形成了强大的免疫防御系统,其被各种微生物攻击时能依靠病原相关分子模式识别蛋白对感染进行区分和激活体内信号通路诱导如抗菌肽之类的效应分子.昆虫体内控制先天性免疫的信号通路分别是:Toll通路、IMD通路和JAS/STAT通路,这3条通路在信号传递过程中存在协作,并且,这些通路与脊椎动物体内某些通路存在惊人相似、在免疫调控通路方面存在共同的进化起源.这揭示了先天性免疫在动物体内存在的普遍性和机体抵御病原感染的重要性.     

Programmed cell death in the plant immune system

Cell death has a central role in innate immune responses in both plants and animals. Besides sharing striking convergences and similarities in the overall evolutionary organization of their innate immune systems, both plants and animals can respond to infection and pathogen recognition with programmed cell death. The fact that plant and animal pathogens have evolved strategies to subvert specific cell death modalities emphasizes the essential role of cell death during immune responses. The hypersensitive response (HR) cell death in plants displays morphological features, molecular architectures and mechanisms reminiscent of different inflammatory cell death types in animals (pyroptosis and necroptosis). In this review, we describe the molecular pathways leading to cell death during innate immune responses. Additionally, we present recently discovered caspase and caspase-like networks regulating cell death that have revealed fascinating analogies between cell death control across both kingdoms.     

Regulatory role of nitric oxide in lipopolysaccharides-triggered plant innate immunity

Recent studies have suggested that lipopolysaccharides (LPS) induce nitric oxide (NO) production and defense gene expression in plants. Our current work investigated the signaling mechanism of NO and the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1) in LPS-induced innate immunity of Arabidopsis (Arabidopsis thaliana). We have provided evidence that LPS-elicited NO generation as well as increased antioxidant enzyme activities capable of maintaining the redox state could be important to protect plants against oxidative damage from pathogen attack. In addition, LPS-activated defense responses, including callose deposition and defense-related gene expression, are regulated through an NPR1-dependent signaling pathway. Our results contribute to elucidation of the signaling mechanism of NO and highlight an important role of NPR1 in modulating LPS-triggered innate immunity in plants. However, further research is necessary to clarify the cross-talk between mitochondria and NO on activating LPS-induced defense responses, and the regulatory mechanism of NO in LPS-induced innate immunity needs further improvement.     

Modulation of innate immune responses by Yersinia type III secretion system translocators and effectors

The innate immune system of mammals responds to microbial infection through detection of conserved molecular determinants called ‘pathogen‐associated molecular patterns’ (PAMPs). Pathogens use virulence factors to counteract PAMP‐directed responses. The innate immune system can in turn recognize signals generated by virulence factors, allowing for a heightened response to dangerous pathogens. Many Gram‐negative bacterial pathogens encode type III secretion systems (T3SSs) that translocate effector proteins, subvert PAMP‐directed responses and are critical for infection. A plasmid‐encoded T3SS in the human‐pathogenic Yersinia species translocates seven effectors into infected host cells. Delivery of effectors by the T3SS requires plasma membrane insertion of two translocators, which are thought to form a channel called a translocon. Studies of the Yersinia T3SS have provided key advances in our understanding of how innate immune responses are generated by perturbations in plasma membrane and other signals that result from translocon insertion. Additionally, studies in this system revealed that effectors function to inhibit innateimmune responses resulting from insertion of translocons into plasma membrane. Here, we review these advances with the goal of providing insight into how a T3SS can activate and inhibit innate immune responses, allowing a virulent pathogen to bypass host defences.     

Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives

Much is known about the evolution of plant immunity components directed against specific pathogen strains: They show pervasive functional variation and have the potential to coevolve with pathogen populations. However, plants are effectively protected against most microbes by generalist immunity components that detect conserved pathogen-associated molecular patterns (PAMPs) and control the onset of PAMP-triggered immunity. In Arabidopsis thaliana, the receptor kinase flagellin sensing 2 (FLS2) confers recognition of bacterial flagellin (flg22) and activates a manifold defense response. To decipher the evolution of this system, we performed functional assays across a large set of A. thaliana genotypes and Brassicaceae relatives. We reveal extensive variation in flg22 perception, most of which results from changes in protein abundance. The observed variation correlates with both the severity of elicited defense responses and bacterial proliferation. We analyzed nucleotide variation segregating at FLS2 in A. thaliana and detected a pattern of variation suggestive of the rapid fixation of a novel adaptive allele. However, our study also shows that evolution at the receptor locus alone does not explain the evolution of flagellin perception; instead, components common to pathways downstream of PAMP perception likely contribute to the observed quantitative variation. Within and among close relatives, PAMP perception evolves quantitatively, which contrasts with the changes in recognition typically associated with the evolution of R genes.     

Molecular crosstalk between PAMP-triggered immunity and photosynthesis

The innate immune system allows plants to respond to potential pathogens in an appropriate manner while minimizing damage and energy costs. Photosynthesis provides a sustained energy supply and, therefore, has to be integrated into the defense against pathogens. Although changes in photosynthetic activity during infection have been described, a detailed and conclusive characterization is lacking. Here, we addressed whether activation of early defense responses by pathogen-associated molecular patterns (PAMPs) triggers changes in photosynthesis. Using proteomics and chlorophyll fluorescence measurements, we show that activation of defense by PAMPs leads to a rapid decrease in nonphotochemical quenching (NPQ). Conversely, NPQ also influences several responses of PAMP-triggered immunity. In a mutant impaired in NPQ, apoplastic reactive oxygen species production is enhanced and defense gene expression is differentially affected. Although induction of the early defense markers WRKY22 and WRKY29 is enhanced, induction of the late markers PR1 and PR5 is completely abolished. We propose that regulation of NPQ is an intrinsic component of the plant's defense program.     

Natural History of Innate Host Defense Peptides

Host defense peptides act on the forefront of innate immunity, thus playing a central role in the survival of animals and plants. Despite vast morphological changes in species through evolutionary history, all animals examined to date share common features in their innate immune defense strategies, hereunder expression of host defense peptides (HDPs). Most studies on HDPs have focused on humans, domestic and laboratory animals. More than a thousand different sequences have been identified, yet data on HDPs in wild-living animals are sparse. The biological functions of HDPs include broad-spectrum antimicrobial activity and immunomodulation. Natural selection and coevolutionary host-pathogen arms race theory suggest that the extent and specificity of the microbial load influences the spectrum and potency of HDPs in different species. Individuals of extant species—that have lived for an extended period in evolutionary history amid populations with intact processes of natural selection—likely possess the most powerful and well-adapted “natural antibiotics”. Research on the evolutionary history of the innate defense system and the host in context of the consequences of challenges as well as the efficacy of the innate immune system under natural conditions is therefore of immediate interest. This review focuses on evolutionary aspects of immunophysiology, with emphasis on innate effector molecules. Studies on host defense in wild-living animals may significantly enhance our understanding of inborn immune mechanisms, and help identify molecules that may assist us to cope better with the increasing microbial challenges that likely follow from the continuous amplification of biodiversity levels on Earth.