Salicylic acid: an old hormone up to new tricks

Salicylic acid (SA) acts as a signalling molecule in plant defence against biotrophic and hemibiotrophic phytopathogens. The biosynthesis of SA on pathogen detection is essential for local and systemic acquired resistance, as well as the accumulation of pathogenesis‐related (PR) proteins. SA biosynthesis can occur via several different substrates, but is predominantly accomplished by isochorismate synthase (ICS1) following pathogen recognition. The roles of BTB domain‐containing proteins, NPR1, NPR3 and NPR4, in SA binding and signal transduction have been re‐examined recently and are elaborated upon in this review. The pathogen‐mediated manipulation of SA‐dependent defences, as well as the crosstalk between the SA signalling pathway, other plant hormones and defence signals, is also discussed in consideration of recent research. Furthermore, the recent links established between SA, pathogen‐triggered endoplasmic reticulum stress and the unfolded protein response are highlighted.     

In the trenches of plant pathogen recognition: Role of NB-LRR proteins

As in nearly every discipline of plant biology, new insights are constantly changing our understanding of plant immunity. It is now clear that plant immunity is controlled by two layers of inducible responses: basal responses triggered by conserved microbial features and specific responses triggered by gene-for-gene recognition of pathogen effector proteins by host resistance (R) proteins. The nucleotide-binding domain leucine-rich repeat (NB-LRR) class of R proteins plays a major role in the combat against a wide range of plant pathogens. The variation that has been generated and is maintained within these conserved proteins has diversified their specificity, subcellular localisations, activation and recognition mechanisms, allowing them to specifically adapt to different plant–pathogen interaction systems. This review addresses recent advances in the molecular role of NB-LRR proteins in pathogen recognition and activation of plant defence responses.     

Proteomic analysis of differentially expressed proteins in fungal elicitor-treated Arabidopsis cell cultures

Slow progress has been made in discovering plant genes governing the interaction of plant pathogens and their hosts using classical genetic approaches. Extensive studies employing DNA microarray techniques to identify global changes in gene expression during pathogen-host interaction have greatly enhanced discovery of genetic components regulating the plant defence response to pathogen attack. In this study, a complementary approach was used to identify changes in protein abundance during interaction of Arabidopsis cell cultures with a pathogen-derived elicitor. The soluble protein fractions were analysed by two-dimensional difference gel electrophoresis and proteins differentially expressed in response to treatment with fungal elicitor were identified via matrix-assisted laser desorption ionization-time of flight mass spectrometry. Elicitor responsive proteins included molecular chaperones, oxidative stress defence proteins, mitochondrial proteins, and enzymes of a diverse number of metabolic pathways. The findings, in combination with currently available microarray data, will form the basis of a filter to identify pivotal genes whose role in pathogen defence systems will require confirmation using gene knockout mutants.     

Review of innate and specific immunity in plants and animals

Innate immunity represents a trait common to plants and animals, based on the recognition of pathogen associated molecular patterns (PAMPs) by the host pattern recognition receptors (PRRs). It is generally assumed that a pathogen strain, or race, may have elaborated mechanisms to suppress, or evade, the PAMP-triggered immunity. Once this plan was successful, the colonization would have been counteracted by an adaptive strategy that a plant cultivar must have evolved as a second line of defence. In this co-evolutionary context, adaptive immunity and host resistance (cultivar-pathogen race/strain-specific) has been differently selected, in animals and plants respectively, to face specialized pathogens. Notwithstanding, plant host resistance, based on matching between resistance (R) and avirulence (avr) genes, represents a form of innate immunity, being R proteins similar to PRRs, although able to recognize specific virulence factors (avr proteins) rather than PAMPs. Besides, despite the lack of adaptive immunity preserved plants from autoimmune disorders, inappropriate plant immune responses may occur, producing some side-effects, in terms of fitness costs of induced resistance and autotoxicity. A set of similar defence responses shared from plants and animals, such as defensins, reactive oxygen species (ROS), oxylipins and programmed cell death (PCD) are briefly described.     

Role of extracytoplasmic leucine rich repeat proteins in plant defence mechanisms

Plant-pathogen interactions involve highly complex series of reactions in disease development. Plants are endowed with both, resistance and defence genes. The activation of defence genes after contact with avirulence gene products of pathogens depends on signals transduced by leucine-rich repeats (LRRs) contained in resistance genes. Additionally, LRRs play roles for various actions following ligand recognition. Polygalacturonase inhibiting proteins (PGIPs), the only plant LRR protein with known ligands, are pectinase inhibitors, bound by ionic interactions to the extracellular matrix (ECM) of plant cells. They have a high affinity for fungal endopolygalacturonases (endoPGs). PGIP genes are organised in families encoding proteins with similar physical characteristics but different specificities. They are induced by infection and stress related signals. The molecular basis of PG-PGIP interaction serves as a model to understand the evolution of plant LRR proteins in recognising non-self-molecules. Extensins form a different class of structural proteins with repetitive sequences. They are also regulated by wounding and pathogen infection. Linkage of extensins with LRR motifs is highly significant in defending host tissues against pathogen invasion. Overexpression of PGIPs or expression of several PGIPs in a plant tissue, and perhaps manipulation of extensin expression could be possible strategies for disease management.     

New insights into the regulation of plant immunity by amino acid metabolic pathways

Besides defence pathways regulated by classical stress hormones, distinct amino acid metabolic pathways constitute integral parts of the plant immune system. Mutations in several genes involved in Asp‐derived amino acid biosynthetic pathways can have profound impact on plant resistance to specific pathogen types. For instance, amino acid imbalances associated with homoserine or threonine accumulation elevate plant immunity to oomycete pathogens but not to pathogenic fungi or bacteria. The catabolism of Lys produces the immune signal pipecolic acid (Pip), a cyclic, non‐protein amino acid. Pip amplifies plant defence responses and acts as a critical regulator of plant systemic acquired resistance, defence priming and local resistance to bacterial pathogens. Asp‐derived pyridine nucleotides influence both pre‐ and post‐invasion immunity, and the catabolism of branched chain amino acids appears to affect plant resistance to distinct pathogen classes by modulating crosstalk of salicylic acid‐ and jasmonic acid‐regulated defence pathways. It also emerges that, besides polyamine oxidation and NADPH oxidase, Pro metabolism is involved in the oxidative burst and the hypersensitive response associated with avirulent pathogen recognition. Moreover, the acylation of amino acids can control plant resistance to pathogens and pests by the formation of protective plant metabolites or by the modulation of plant hormone activity.     

Transport and secretion in plant-microbe interactions

Microbial elicitors and effectors, as well as plant receptors and defence compounds, traffic at the interface of plants and microbes in pathogenic or mutualistic interactions. Net exocytosis appears to be required for surface enlargement of plasma membrane during accommodation of microbes in intact plant cells. By contrast, ligand-induced endocytosis of surface receptors operates in basal defence. The first layer of plant defence appears to depend on polarized transport of small molecules and on local secretion of defence proteins. In return, pathogen effectors target plasma membrane bound and intracellular proteins to inhibit extracellular host defences.     

Primed plants do not forget

In their struggle for life, plants can employ sophisticated strategies to defend themselves against potentially harmful pathogens and insects. One mechanism by which plants can increase their level of resistance is by intensifying the responsiveness of their immune system upon recognition of selected signals from their environment. This so-called priming of defence can provide long-lasting resistance, which is based on a faster and/or stronger defence reaction upon pathogen or pest attack. Priming can target various layers of induced defence that are active during different stages of the plant–attacker interaction. Recent discoveries have extended our knowledge about the mechanistic basis of defence priming and suggest that a primed defence state can be inherited epi-genetically from defence-expressing plants. In this review, we provide an overview of the latest insights about defence priming, ranging from early responses controlled by adjustments in hormone-dependent signalling pathways and availability of signal transduction proteins, to longer lasting mechanisms that involve possible regulation chromatin modification or DNA methylation.     

Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana

Bacterial pathogens deliver type III effector proteins into plant cells during infection. On susceptible host plants, type III effectors contribute to virulence, but on resistant hosts they betray the pathogen to the plant's immune system and are functionally termed avirulence (Avr) proteins. Recognition induces a complex suite of cellular and molecular events comprising the plant's inducible defence response. As recognition of type III effector proteins occurs inside host cells, defence responses can be elicited by in planta expression of bacterial type III effectors. We demonstrate that recognition of either of two type III effectors, AvrRpm1 or AvrRpt2 from Pseudomonas syringae , induced biphasic accumulation of phosphatidic acid (PA). The first wave of PA accumulation correlated with disappearance of monophosphatidylinosotol (PIP) and is thus tentatively attributed to activation of a PIP specific phospholipase C (PLC) in concert with diacylglycerol kinase (DAGK) activity. Subsequent activation of phospholipase D (PLD) produced large amounts of PA from structural phospholipids. This later wave of PA accumulation was several orders of magnitude higher than the PLC-dependent first wave. Inhibition of phospholipases blocked the response, and feeding PA directly to leaf tissue caused cell death and defence-gene activation. Inhibitor studies ordered these events relative to other known signalling events during the plant defence response. Influx of extracellular Ca²⁺ occurred downstream of PIP-degradation, but upstream of PLD activation. Production of reactive oxygen species occurred downstream of the phospholipases. The data presented indicate that PA is a positive regulator of RPM1- or RPS2-mediated disease resistance signalling, and that the biphasic PA production may be a conserved feature of signalling induced by the coiled-coil nucleotide binding domain leucine-rich repeat class of resistance proteins.     

The role of plant defence proteins in fungal pathogenesis

It is becoming increasingly evident that a plant–pathogen interaction may be compared to an open warfare, whose major weapons are proteins synthesized by both organisms. These weapons were gradually developed in what must have been a multimillion-year evolutionary game of ping-pong. The outcome of each battle results in the establishment of resistance or pathogenesis. The plethora of resistance mechanisms exhibited by plants may be grouped into constitutive and inducible, and range from morphological to structural and chemical defences. Most of these mechanisms are defensive, exhibiting a passive role, but some are highly active against pathogens, using as major targets the fungal cell wall, the plasma membrane or intracellular targets. A considerable overlap exists between pathogenesis-related (PR) proteins and antifungal proteins. However, many of the now considered 17 families of PR proteins do not present any known role as antipathogen activity, whereas among the 13 classes of antifungal proteins, most are not PR proteins. Discovery of novel antifungal proteins and peptides continues at a rapid pace. In their long coevolution with plants, phytopathogens have evolved ways to avoid or circumvent the plant defence weaponry. These include protection of fungal structures from plant defence reactions, inhibition of elicitor-induced plant defence responses and suppression of plant defences. A detailed understanding of the molecular events that take place during a plant–pathogen interaction is an essential goal for disease control in the future.     

How do oomycete effectors interfere with plant life?

Oomycete genomes have yielded a large number of predicted effector proteins that collectively interfere with plant life in order to create a favourable environment for pathogen infection. Oomycetes secrete effectors that can be active in the host's extracellular environment, for example inhibiting host defence enzymes, or inside host cells where they can interfere with plant processes, in particular suppression of defence. Two classes of effectors are known to be host-translocated: the RXLRs and Crinklers. Many effectors show defence-suppressive activity that is important for pathogen virulence. A striking example is AVR3a of Phytophthora infestans that targets an ubiquitin ligase, the stabilisation of which may prevent host cell death. The quest for other effector targets and mechanisms is in full swing.     

Transcriptomic and Proteomic Analyses of Resistant Host Responses in Arachis diogoi Challenged with Late Leaf Spot Pathogen,Phaeoisariopsis personata

Late leaf spot is a serious disease of peanut caused by the imperfect fungus, Phaeoisariopsis personata. Wild diploid species, Arachis diogoi. is reported to be highly resistant to this disease and asymptomatic. The objective of this study is to investigate the molecular responses of the wild peanut challenged with the late leaf spot pathogen using cDNA-AFLP and 2D proteomic study. A total of 233 reliable, differentially expressed genes were identified in Arachis diogoi. About one third of the TDFs exhibit no significant similarity with the known sequences in the data bases. Expressed sequence tag data showed that the characterized genes are involved in conferring resistance in the wild peanut to the pathogen challenge. Several genes for proteins involved in cell wall strengthening, hypersensitive cell death and resistance related proteins have been identified. Genes identified for other proteins appear to function in metabolism, signal transduction and defence. Nineteen TDFs based on the homology analysis of genes associated with defence, signal transduction and metabolism were further validated by quantitative real time PCR (qRT-PCR) analyses in resistant wild species in comparison with a susceptible peanut genotype in time course experiments. The proteins corresponding to six TDFs were differentially expressed at protein level also. Differentially expressed TDFs and proteins in wild peanut indicate its defence mechanism upon pathogen challenge and provide initial breakthrough of genes possibly involved in recognition events and early signalling responses to combat the pathogen through subsequent development of resistivity. This is the first attempt to elucidate the molecular basis of the response of the resistant genotype to the late leaf spot pathogen, and its defence mechanism.     

The grateful dead: calcium and cell death in plant innate immunity

Plant cells sensing pathogenic microorganisms evoke defence systems that can confer resistance to infection. This innate immune reaction can include triggering of basal defence responses as well as programmed cell death, or hypersensitive response (HR). In both cases (basal defence and HR), pathogen perception is translated into elevated cytosolic Ca(2+) (mediated by plasma membrane and intracellular channels) as an early step in a signalling cascade. Cyclic nucleotide-gated channels contribute to this influx of Ca(2+) into the cell. The molecular nature of other transport proteins contributing to the Ca(2+) elevation is unclear. Pathogen recognition occurs at two levels: the perception of pathogen-associated molecular pattern (PAMP) molecules widely present in microorganisms, and an interaction between pathogen avirulence gene products (if present) and corresponding plant R (resistance) gene products. The Ca(2+) elevation occurring in response to PAMP perception or R gene interactions could occur due to phosphorylation events, G-protein signalling and/or an increase in cyclic nucleotides. Downstream from the initial Ca(2+) rise, the signalling cascade includes: activation of calmodulin and protein kinases, and nitric oxide and reactive oxygen species generation. Some of these downstream events amplify the Ca(2+) signal by further activation of Ca(2+) transporters.     

Mammalian NLR proteins; discriminating foe from friend

Eukaryotic organisms of the plant and animal kingdoms have developed evolutionarily conserved systems of defence against microbial pathogens. These systems depend on the specific recognition of microbial products or structures by molecules of the host innate immune system. The first mammalian molecules shown to be involved in innate immune recognition of, and defence against, microbial pathogens were the Toll-like receptors (TLRs). These proteins are predominantly but not exclusively located in the transmembrane region of host cells. Interestingly, mammalian hosts were subsequently found to also harbour cytosolic proteins with analogous structures and functions to plant defence molecules. The members of this protein family exhibit a tripartite domain structure and are characterized by a central nucleotide-binding oligomerization domain (NOD). Moreover, in common with TLRs, most NOD proteins possess a C-terminal leucine-rich repeat (LRR) domain, which is required for the sensing of microbial products and structures. Recently, the name 'nucleotide-binding domain and LRR' (NLR) was coined to describe this family of proteins. It is now clear that NLR proteins play key roles in the cytoplasmic recognition of whole bacteria or their products. Moreover, it has been demonstrated in animal studies that NLRs are important for host defence against bacterial infection. This review will particularly focus on two subfamilies of NLR proteins, the NODs and 'NALPs', which specifically recognize bacterial products, including cell wall peptidoglycan and flagellin. We will discuss the downstream signalling events and host cell responses to NLR recognition of such products, as well as the strategies that bacterial pathogens employ to trigger NLR signalling in host cells. Cytosolic recognition of microbial factors by NLR proteins appears to be one mechanism whereby the innate immune system is able to discriminate between pathogenic bacteria ('foe') and commensal ('friendly') members of the host microflora.     

植物NLR免疫受体的识别、免疫激活与信号调控

高等植物进化出大量膜表面和胞内免疫受体以感知各种病原信号,抵御病原物入侵。其中,细胞表面的模式识别受体感知模式分子后激活基础免疫反应,核苷酸结合和富亮氨酸重复蛋白(NLRs)则通过感知病原微生物分泌的效应蛋白激活特异免疫反应,导致超敏反应与细胞死亡。该文主要综述了NLRs对效应蛋白的识别、植物免疫激活及下游信号调控的最新研究进展。     

The conserved oligomeric Golgi complex is involved in penetration resistance of barley to the barley powdery mildew fungus

Membrane trafficking is vital to plant development and adaptation to the environment. It is suggested that post‐Golgi vesicles and multivesicular bodies are essential for plant defence against directly penetrating fungal parasites at the cell wall. However, the actual plant proteins involved in membrane transport for defence are largely unidentified. We applied a candidate gene approach and single cell transient‐induced gene silencing for the identification of membrane trafficking proteins of barley involved in the response to the fungal pathogen Blumeria graminis f.sp. hordei. This revealed potential components of vesicle tethering complexes [putative exocyst subunit HvEXO70F‐like and subunits of the conserved oligomeric Golgi (COG) complex] and Golgi membrane trafficking (COPIγ coatomer and HvYPT1‐like RAB GTPase) as essential for resistance to fungal penetration into the host cell.     

Induced resistance during the interaction pathogen x plant and the use of resistance inducers

Plants react to aggressions through different defence responses. Mechanical barriers consist in the increase of production and deposition of substances capable of containing pathogen invasion. Chemical barriers consist in the increase of concentration or activity of defence proteins and synthesis of phenolic compounds and phytoalexins. Elicitor substances have been widely used in plant disease control showing impressive results and a low impact to the environment and man. This review contains information about plant defence mechanisms and shows the use of inducers of resistance in the control of pathogens and prospects of advance towards sustainable agriculture.