Cell wall degrading enzymes,inhibitory proteins,and oligosaccharides participate in the molecular dialogue between plants and pathogens

The wall interface between plants and pathogens plays an important role in the outcome of their interactions. Studying the degradation of plant pectic polysaccharides by microbial pectinases, and of microbial β-glucans by plant glucanases has shown that these polymers are a source of oligosaccharides which elicit defence responses in plants. The extent of degradation appears to be controlled by the presence of inhibitory proteins which counteract enzyme hydrolysis. Thus, plant cell walls participate in the molecular dialogue established between plants and pathogens.     

Antibiotic activities of peptides, hydrogen peroxide and peroxynitrite in plant defence.

Genes encoding plant antibiotic peptides show expression patterns that are consistent with a defence role. Transgenic over-expression of defence peptide genes is potentially useful to engineer resistance of plants to relevant pathogens. Pathogen mutants that are sensitive to plant peptides in vitro have been obtained and a decrease of their virulence in planta has been observed, which is consistent with their hypothetical defence role. A similar approach has been followed to elucidate the potential direct anti-microbial role of hydrogen peroxide. Additionally, a scavenger of peroxynitrite has been used to investigate its involvement in plant defence.     

Catabolism of polyamines

Summary. Owing to the establishment of cells and transgenic animals which either lack or over-express acetylCoA:spermidine N¹-acetyltransferase a major progress was made in our understanding of the role of polyamine acetylation. Cloning of polyamine oxidases of mammalian cell origin revealed the existence of several enzymes with different substrate and molecular properties. One appears to be identical with the polyamine oxidase that was postulated to catalyse the conversion of spermidine to putrescine within the interconversion cycle. The other oxidases are presumably spermine oxidases, because they prefer free spermine to its acetyl derivatives as substrate. Transgenic mice and cells which lack spermine synthase revealed that spermine is not of vital importance for the mammalian organism, but its transformation into spermidine is a vitally important reaction, since in the absence of active polyamine oxidase, spermine accumulates in blood and causes lethal toxic effects.Numerous metabolites of putrescine, spermidine and spermine, which are presumably the result of diamine oxidase-catalysed oxidative deaminations, are known as normal constituents of organs of vertebrates and of urine. Reasons for the apparent contradiction that spermine is in vitro a poor substrate of diamine oxidase, but is readily transformed into N⁸-(2-carboxyethyl)spermidine in vivo, will need clarification.Several attempts were made to establish diamine oxidase as a regulatory enzyme of polyamine metabolism. However, diamine oxidase has a slow turnover. This, together with the efficacy of the homeostatic regulation of the polyamines via the interconversion reactions and by transport pathways renders a role of diamine oxidase in the regulation of polyamine concentrations unlikely. 4-Aminobutyric acid, the product of putrescine catabolism has been reported to have antiproliferative properties. Since ornithine decarboxylase and diamine oxidase activities are frequently elevated in tumours, it may be hypothesised that diamine oxidase converts excessive putrescine into 4-aminobutyric acid and thus restricts tumour growth and prevents malignant transformation. This function of diamine oxidase is to be considered as part of a general defence function, of which the prevention of histamine and cadaverine accumulation from the gastrointestinal tract is a well-known aspect.     

Apoplastic polyamine oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas viridiflava

The role of polyamine (PA) metabolism in tobacco (Nicotiana tabacum) defense against pathogens with contrasting pathogenic strategies was evaluated. Infection by the necrotrophic fungus Sclerotinia sclerotiorum resulted in increased arginine decarboxylase expression and activity in host tissues, as well as putrescine and spermine accumulation in leaf apoplast. Enhancement of leaf PA levels, either by using transgenic plants or infiltration with exogenous PAs, led to increased necrosis due to infection by S. sclerotiorum. Specific inhibition of diamine and PA oxidases attenuated the PA-induced enhancement of leaf necrosis during fungal infection. When tobacco responses to infection by the biotrophic bacterium Pseudomonas viridiflava were investigated, an increase of apoplastic spermine levels was detected. Enhancement of host PA levels by the above-described experimental approaches strongly decreased in planta bacterial growth, an effect that was blocked by a PA oxidase inhibitor. It can be concluded that accumulation and further oxidation of free PAs in the leaf apoplast of tobacco plants occurs in a similar, although not identical way during tobacco defense against infection by microorganisms with contrasting pathogenesis strategies. This response affects the pathogen's ability to colonize host tissues and results are detrimental for plant defense against necrotrophic pathogens that feed on necrotic tissue; on the contrary, this response plays a beneficial role in defense against biotrophic pathogens that depend on living tissue for successful host colonization. Thus, apoplastic PAs play important roles in plant-pathogen interactions, and modulation of host PA levels, particularly in the leaf apoplast, may lead to significant changes in host susceptibility to different kinds of pathogens.     

Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks

Resource sharing between ramets of clonal plants is a well-known phenomenon, which allows stoloniferous and rhizomatous species to internally translocate water, mineral nutrients and carbohydrates from sites of high supply to sites of high demand. The mechanisms and implications of resource integration in clonal plants have extensively been studied in the past. Vascular ramet connections are likely to provide an excellent means to share substances other than resources, such as systemic defence signals and pathogens. The aim of this paper is to propose the idea that physical ramet connections of clonal plants can be used (1) to transmit signals, which enable members of clonal plant networks to share information about their biotic and abiotic environments, and (2) to facilitate the internal distribution of systemic pathogens in clonal plant networks and populations. We will focus on possible mechanisms as well as on potential ecological and evolutionary implications of clonal integration beyond resource sharing. More specifically, we will explore the role of physiological integration in clonal plant networks for the systemic transmission of direct and indirect defence signals after localized herbivore attack. We propose that sharing defence induction signals among ramets may be the basis for an efficient early warning system, and it may allow for effective indirect defence signalling to herbivore enemies through a systemic release of volatiles from entire clonal fragments. In addition, we will examine the role of clonal integration for the internal spread of systemic pathogens and pathogen defence signals within clonal plants. Clonal plants may use developmental mechanisms such as increased flowering and clone fragmentation, but also specific biochemical defence strategies to fight pathogens. We propose that clonal plant networks can act as stores and vectors of diseases in plant populations and communities and that clonal life histories favour the evolution of pathogens with a low virulence.     

Molecular and physiological stages of priming: how plants prepare for environmental challenges

Being sessile organisms, plants must respond to various challenges in the environment. The priming process consists of three clear stages. The first stage includes all the cellular changes in the absence of the challenge so-called pre-challenge priming stage. These changes are expected to be rather subtle, affecting the preparation of the plant to properly manage subsequent responses to pathogens with no major fitness costs. Most of the research that has been conducted at this stage has been dedicated to the study of changes in gene expression and protein phosphorylation. However, the metabolic changes that occur during the pre-challenge priming stage are poorly understood. The second stage affects the early to late stages of the defence response, which occurs after the interaction with a pathogen has been established. Most studies involving priming are dedicated to the molecular events that take place during this stage. Most studies have shown that defence priming is strongly hormonally regulated; however, there is also evidence of the involvement of phenolic derivative compounds and many other secondary metabolites, leading to stronger and faster plant responses. The third priming phase ranges from long lasting defence priming to trans-generational acquired resistance. Long-term metabolic transitions, that occur in the offspring of primed plants, remain to be elucidated. Here we review existing information in the literature that relates to the metabolic changes that occur during all three defence priming stages and highlight the metabolic transitions that are associated with the stimulation of priming and the characteristics of the pathogens whenever possible.     

Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation

Biotic stress has a major impact on the process of natural selection in plants. As plants have evolved under variable environmental conditions, they have acquired a diverse spectrum of defensive strategies against pathogens and herbivores. Genetic variation in the expression of plant defence offers valuable insights into the evolution of these strategies. The 'zigzag' model, which describes an ongoing arms race between inducible plant defences and their suppression by pathogens, is now a commonly accepted model of plant defence evolution. This review explores additional strategies by which plants have evolved to cope with biotic stress under different selective circumstances. Apart from interactions with plant-beneficial micro-organisms that can antagonize pathogens directly, plants have the ability to prime their immune system in response to selected environmental signals. This defence priming offers disease protection that is effective against a broad spectrum of virulent pathogens, as long as the augmented defence reaction is expressed before the invading pathogen has the opportunity to suppress host defences. Furthermore, priming has been shown to be a cost-efficient defence strategy under relatively hostile environmental conditions. Accordingly, it is possible that selected plant varieties have evolved a constitutively primed immune system to adapt to levels of disease pressure. Here, we examine this hypothesis further by evaluating the evidence for natural variation in the responsiveness of basal defence mechanisms, and discuss how this genetic variation can be exploited in breeding programmes to provide sustainable crop protection against pests and diseases.     

Switching on plant genes by external chemical signals

During the past decade there has been rapidly increasing interest in the role of plant volatiles in insect-plant interactions and the induction of plant defence systems by both pathogens and herbivores. Scientists are striving to link the proximate studies elucidating pathways and genes with the ultimate adaptive studies that attempt to explain their ecological role. However, we still do not know whether plants 'talk' to one another by employing 'phytopheromones'.     

Subtilisin‐like proteases in plant defence: the past,the present and beyond

Subtilisin‐like proteases (or subtilases) are a very diverse family of serine peptidases present in many organisms, but mostly in plants. With a broad spectrum of biological functions, ranging from protein turnover and plant development to interactions with the environment, subtilases have been gaining increasing attention with regard to their involvement in plant defence responses against the most diverse pathogens. Over the last 5 years, the number of published studies associating plant subtilases with pathogen resistance and plant immunity has increased tremendously. In addition, the observation of subtilases and serine protease inhibitors secreted by pathogens has also gained prominence. In this review, we focus on the active participation of subtilases in the interactions established by plants with the environment, highlighting their role in plant–pathogen communication.     

The arms race continues: battle strategies between plants and fungal pathogens

Plants are under constant attack by a vast array of pathogens. To impede their attackers they use both broad-spectrum and pathogen-specific defence mechanisms. The arms race between plants and fungal pathogens is fascinatingly varied, and what might be elicited as a plant defence mechanism against a pathogen could promote or enhance the virulence of other pathogens. Fungi use countermeasures to detoxify plant antimicrobial compounds and to evade host resistance mechanisms. Certain fungal species also manipulate the host hormone balance to create an environment that is beneficial to their survival. Several lines of evidence indicate a co-evolutionary arms race in which both plants and fungi can respond to changes that occur in their opponents.     

Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant

In their defence against pathogens, herbivorous insects, and mites, plants employ many induced responses. One of these responses is the induced emission of volatiles upon herbivory. These volatiles can guide predators or parasitoids to their herbivorous prey, and thus benefit both plant and carnivore. This use of carnivores by plants is termed indirect defence and has been reported for many plant species, including elm, pine, maize, Lima bean, cotton, cucumber, tobacco, tomato, cabbage, and Arabidopsis thaliana. Herbivory activates an intricate signalling web and finally results in defence responses such as increased production of volatiles. Although several components of this signalling web are known (for example the plant hormones jasmonic acid, salicylic acid, and ethylene), our understanding of how these components interact and how other components are involved is still limited. Here we review the knowledge on elicitation and signal transduction of herbivory-induced volatile production. Additionally, we discuss how use of the model plant Arabidopsis thaliana can enhance our understanding of signal transduction in indirect defence and how cross-talk and trade-offs with signal transduction in direct defence against herbivores and pathogens influences plant responses.     

Pathogens pulling the strings: Effectors manipulating salicylic acid and phenylpropanoid biosynthesis in plants

During evolution, plants have developed sophisticated ways to cope with different biotic and abiotic stresses. Phytohormones and secondary metabolites are known to play pivotal roles in defence responses against invading pathogens. One of the key hormones involved in plant immunity is salicylic acid (SA), of which the role in plant defence is well established and documented. Plants produce an array of secondary metabolites categorized in different classes, with the phenylpropanoids as major players in plant immunity. Both SA and phenylpropanoids are needed for an effective immune response by the plant. To successfully infect the host, pathogens secrete proteins, called effectors, into the plant tissue to lower defence. Secreted effectors can interfere with several metabolic or signalling pathways in the host to facilitate infection. In this review, we will focus on the different strategies pathogens have developed to affect the levels of SA and phenylpropanoids to increase plant susceptibility.     

Cell biology of plant-oomycete interactions

The last 4 years have seen significant advances in our understanding of the cellular processes that underlie the infection of plants by a range of biotrophic and necrotrophic oomycete pathogens. Given that oomycete and fungal pathogens must overcome the same sets of physical and chemical barriers presented by plants, it is not surprising that many aspects of oomycete infection strategies are similar to those of fungal pathogens. A major difference, however, centres on the role of motile oomycete zoospores in actively moving the pathogen to favourable infection sites. Recent studies have shown that the plant defence response to invading oomycetes is similar to that mounted against fungi, but biochemical differences between oomycete and fungal surface molecules must have implications for plant recognition of and defence against oomycete pathogens. The aim of this short review is to provide a cell biological framework within which emerging data on the molecular basis of oomycete-plant interactions may be placed.     

The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity

Nitrogen plays an essential role in the nutrient relationship between plants and pathogens. Some studies report that the nitrogen-mobilizing plant metabolism that occurs during abiotic and biotic stress could be a 'slash-and-burn' defence strategy. In order to study nitrogen recycling and mobilization in host plants during pathogen attack and invasion, the Colletotrichum lindemuthianum/Phaseolus vulgaris interaction was used as a model. C. lindemuthianum is a hemibiotroph that causes anthracnose disease on P. vulgaris. Non-pathogenic mutants and the pathogenic wild-type strain were used to compare their effects on plant metabolism. The deleterious effects of infection were monitored by measuring changes in chlorophyll, protein, and amino acid concentrations. It was shown that amino acid composition changed depending on the plant-fungus interaction and that glutamine accumulated mainly in the leaves infected by the pathogenic strain. Glutamine accumulation correlated with the accumulation of cytosolic glutamine synthetase (GS1 alpha) mRNA. The most striking result was that the GS1 alpha gene was induced in all the fungus-infected leaves, independent of the strain used for inoculation, and that GS1 alpha expression paralleled the PAL3 and CHS defence gene expression. It is concluded that a role of GS1 alpha in plant defence has to be considered.     

Role of ubiquitination in the regulation of plant defence against pathogens

Ubiquitination is emerging as a common regulatory mechanism that controls a range of cellular processes in plants. Recent exciting discoveries from several laboratories suggest that ubiquitination may also play an important role in plant disease resistance. Several putative ubiquitin ligases have been identified as defence regulators. In addition, a combination of genetic screens and gene-silencing technologies has identified subunits and proposed regulators of SCF ubiquitin ligases as essential components of resistance (R)-gene-mediated resistance. Although no ubiquitin ligase targets that are associated with disease resistance have yet been identified in plants, there is evidence that this well-known protein-modification system may regulate plant defences against pathogens.     

Activation of defence reactions in Solanaceae: where is the specificity?

When a potential pathogen attempts to infect a plant, biochemical and molecular communication takes place and leads to the induction of plant defence mechanisms. In the case of efficient defence, visible symptoms are restricted and the pathogen does not multiply (incompatible interaction); when defence is inefficient, the plant becomes rapidly infected (compatible interaction). During the last 30 years, a growing body of knowledge on plant-pathogen interactions has been gathered, and a large number of studies investigate the induction of various plant defence reactions by pathogens or by pathogen-derived compounds. However, as most papers focus on incompatible interactions, there is still a lack of understanding about the similarities and differences between compatible and incompatible situations. This review targets the question of specificity in Solanaceae-pathogen interactions, by comparing defence patterns in plants challenged with virulent or avirulent pathogens (or with pathogen-associated molecular patterns from these). A special emphasis is made on analysing whether defence reactions in Solanaceae depend primarily on the type of elicitor, on the plant genotype/species, or on the type of interaction (compatible or incompatible).     

Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids

Direct and indirect plant defences are well studied, particularly in the Brassicaceae. Glucosinolates (GS) are secondary plant compounds characteristic in this plant family. They play an important role in defence against herbivores and pathogens. Insect herbivores that are specialists on brassicaceous plant species have evolved adaptations to excrete or detoxify GS. Other insect herbivores may even sequester GS and employ them as defence against their own antagonists, such as predators. Moreover, high levels of GS in the food plants of non-sequestering herbivores can negatively affect the growth and survival of their parasitoids. In addition to allelochemicals, plants produce volatile chemicals when damaged by herbivores. These herbivore induced plant volatiles (HIPV) have been demonstrated to play an important role in foraging behaviour of insect parasitoids. In addition, biosynthetic pathways involved in the production of HIPV are being unraveled using the model plant Arabidopsis thialiana. However, the majority of studies investigating the attractiveness of HIPV to parasitoids are based on experiments mainly using crop plant species in which defence traits may have changed through artificial selection. Field studies with both cultivated and wild crucifers, the latter in which defence traits are intact, are necessary to reveal the relative importance of direct and indirect plant defence strategies on parasitoid and plant fitness. Future research should also consider the potential conflict between direct and indirect plant defences when studying the evolution of plant defences against insect herbivory.     

Role of plant stomata in bacterial invasion

Stomata are microscopic pores in the epidermis of the aerial parts of terrestrial plants. These pores are essential for photosynthesis, as they allow CO(2) to diffuse into the plant. The size of the stomatal pore changes in response to environmental conditions, such as light intensity, air humidity and CO(2) concentrations, as part of the plant's adaptation to maximize photosynthetic efficiency and, at the same time, to minimize water loss. Historically, stomata have been considered as passive portal of entry for plant pathogenic bacteria. However, recent studies suggest that stomata can play an active role in restricting bacterial invasion as part of the plant innate immune system. Some plant pathogens have evolved specific virulence factors to overcome stomata-based defence. Interestingly, many bacterial disease outbreaks require high humidity, rain, or frost damage, which could promote stomatal opening and/or bypass stomatal defence by creating wounds as alternative entry sites. Further studies on microbial and environmental regulation of stomata-based defence should fill gaps in our understanding of bacterial pathogenesis, disease epidemiology and phyllosphere microbiology.