Proteasomal degradation in plant–pathogen interactions

The ubiquitin/26S proteasome pathway is a basic biological mechanism involved in the regulation of a multitude of cellular processes. Increasing evidence indicates that plants utilize the ubiquitin/26S proteasome pathway in their immune response to pathogen invasion, emphasizing the role of this pathway during plant–pathogen interactions. The specific functions of proteasomal degradation in plant–pathogen interactions are diverse, and do not always benefit the host plant. Although in some cases, proteasomal degradation serves as an effective barrier to help plants ward off pathogens, in others, it is used by the pathogen to enhance the infection process. This review discusses the different roles of the ubiquitin/26S proteasome pathway during interactions of plants with pathogenic viruses, bacteria, and fungi.     

Structural specificity in plant–filamentous pathogen interactions

Plant diseases bear names such as leaf blights, root rots, sheath blights, tuber scabs, and stem cankers, indicating that symptoms occur preferentially on specific parts of host plants. Accordingly, many plant pathogens are specialized to infect and cause disease in specific tissues and organs. Conversely, others are able to infect a range of tissues, albeit often disease symptoms fluctuate in different organs infected by the same pathogen. The structural specificity of a pathogen defines the degree to which it is reliant on a given tissue, organ, or host developmental stage. It is influenced by both the microbe and the host but the processes shaping it are not well established. Here we review the current status on structural specificity of plant–filamentous pathogen interactions and highlight important research questions. Notably, this review addresses how constitutive defence and induced immunity as well as virulence processes vary across plant organs, tissues, and even cells. A better understanding of the mechanisms underlying structural specificity will aid targeted approaches for plant health, for instance by considering the variation in the nature and the amplitude of defence responses across distinct plant organs and tissues when performing selective breeding.     

The roles of ABA in plant–pathogen interactions

Defence against abiotic and biotic stresses is crucial for the fitness and survival of plants under adverse or suboptimal growth conditions. The phytohormone abscisic acid (ABA) is not only important for mediating abiotic stress responses, but also plays a multifaceted and pivotal role in plant immunity. This review presents examples demonstrating the importance of crosstalk between ABA and the key biotic stress phytohormone salicylic acid in determining the outcome of plant–pathogen interactions. We then provide an overview of how ABA influences plant defence responses against various phytopathogens with particular emphasis on the Arabidopsis–Pseudomonas syringae model pathosystem. Lastly, we discuss future directions for studies of ABA in plant immunity with emphasis on, its role in the crosstalk between biotic and abiotic stress responses, the importance of distinguishing direct and indirect effects of ABA, as well as the prospect of utilizing the recently elucidated core ABA signaling network to gain further insights into the roles of ABA in plant immunity.     

Pseudomonas corrugata: plant pathogen and/or biological resource?

Pseudomonas corrugata is the causal agent of tomato pith necrosis yet it is also used in the biological control of plant pathogenic bacteria and fungi. Potentially it could be used in other fields, such as the production of commercial biomolecules with a wide range of application and including bioremediation. This review reports the multiple characteristics of the bacterium, highlights its known molecular features and speculates on the possible underlying mechanisms of action.
Taxonomy:  Bacteria; Proteobacteria ; γ subdivision; order Pseudomonadales ; family Pseudomonadaceae ; genus Pseudomonas .
Microbiological properties:  Gram-negative, oxidase-positive, non-spore forming rods; non-fluorescent on King's B medium; produces wrinkled and rarely smooth colonies on yeast peptone glucose agar or nutrient dextrose agar; yellow to brown diffusible pigments are frequently produced.
Disease symptoms:  The typical symptom on tomato is necrosis and/or hollowing of the pith of the stem; the syndrome determines loss of turgidity of the plant, hydropic/necrotic areas and long conspicuous adventitious roots on the stem.
Biological control agent: In vitro assessed against plant pathogenic fungi and bacteria, as well as the phytotoxin indicator microorganims Rhodotorula pilimanae and Bacillus megaterium ; in vivo used against pre- and post-harvest plant pathogens.     

Vacuolar membrane structures and their roles in plant–pathogen interactions

Plant Molecular Biology - Short review focussing on the role and targeting of vacuolar substructure in plant immunity and pathogenesis. Plants lack specialized immune cells, therefore each plant...     

Dual metabolomics: A novel approach to understanding plant–pathogen interactions

One of the most well-characterised plant pathogenic interactions involves Arabidopsis thaliana and the bacteria Pseudomonas syringae pathovar tomato (Pst). The standard Pst inoculation procedure involves infiltration of large populations of bacteria into plant leaves which means that metabolite changes cannot be readily assigned to the host or pathogen. A plant cell–pathogen co-culture based approach has been developed where the plant and pathogen cells are separated after 12 h of co-culture via differential filtering and centrifugation. Fourier transform infrared (FT-IR) spectroscopy was employed to assess the intracellular metabolomes (metabolic fingerprints) of both host and pathogen and their extruded (extracellular) metabolites (metabolic footprints) under conditions relevant to disease and resistance. We propose that this system will enable the metabolomic profiling of the separated host and pathogen (i.e. ‘dual metabolomics’) and will facilitate the modelling of reciprocal responses.     

Nitric oxide: an effective weapon of the plant or the pathogen?

An explosion of research in plant nitric oxide (NO) biology during the last two decades has revealed that NO is a key signal involved in plant development, abiotic stress responses and plant immunity. During the course of evolutionary changes, microorganisms parasitizing plants have developed highly effective offensive strategies, in which NO also seems to be implicated. NO production has been demonstrated in several plant pathogens, including fungi, but the origin of NO seems to be as puzzling as in plants. So far, published studies have been spread over multiple species of pathogenic microorganisms in various developmental stages; however, the data clearly indicate that pathogen‐derived NO is an important regulatory molecule involved not only in developmental processes, but also in pathogen virulence and its survival in the host. This review also focuses on the search for potential mechanisms by which pathogens convert NO messages into a physiological response or detoxify both endo‐ and exogenous NO. Finally, taking into account the data available from model bacteria and yeast, a basic draft for the mode of NO action in phytopathogenic microorganisms is proposed.     

The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction

Plant resistance to pathogens requires the activation of complex metabolic pathways in the infected cells, aimed at recognizing pathogen presence and hindering its propagation within plant tissues. In spite of this both compatible and incompatible responses induce alterations in plant metabolism, only in the latter the plant is able to efficiently block pathogen penetration without suffering excessive damage. One of the most studied incompatible responses is based on the hypersensitive response (HR), in which cells surrounding the site of pathogen penetration switch on genes encoding for phytoalexin synthesis and other pathogenesis related proteins before activating programmed cell death (PCD). The production of reactive oxygen species (ROS) is a key event in HR. Several enzymatic systems have been proposed to be responsible for the oxidative burst characterizing HR. In this review, the involvement of antioxidant redox systems, in particular those related to ascorbate (ASC) and glutathione (GSH), in activating both compatible and incompatible plant responses is analysed. Increasing lines of evidence indicate that alterations in the levels and/or redox state of ASC and/or GSH, as well as in the activity of their redox enzymes, occur during the HR programme. These alterations do not seem to be a mere consequence of the oxidative stress induced by the massive ROS production, but they are induced as part of the transduction pathways triggering defence responses and PCD. The possibility that ASC and GSH systems are links in a redox signalling chain activating defence strategies is also discussed.     

Advances in proteomic technologies and their scope of application in understanding plant–pathogen interactions

Proteomics, one of the major tools of ‘omics’ is evolving phenomenally since the development and application of two-dimensional gel electrophoresis coupled with mass spectrometry at the end of twentieth century. However, the adoption and application of advanced proteomic technologies in understanding plant–pathogen interactions are far less, when compared to their application in other related fields of systems biology. Hence, this review is diligently focused on the advances in various proteomic approaches and their gamut of applications in different facets of phyto-pathoproteomics. Especially, the scope and application of proteomics in understanding fundamental concepts of plant–pathogen interactions such as identification of pathogenicity determinants (effector proteins), disease resistance proteins (resistance and pathogenesis-related proteins) and their regulation by post-translational modifications have been portrayed. This review, for the first time, presents a critical appraisal of various proteomic applications by assessing all phyto-pathoproteomics-related research publications that were published in peer-reviewed journals, during the period 2000–2016. This assessment has revealed the present status and contribution of proteomic applications in different categories of phyto-pathoproteomics, namely, cellular components, host–pathogen interactions, model and non-model plants, and utilization of different proteomic approaches. Comprehensively, the analysis highlights the burgeoning application of global proteome approaches in various crop diseases, and demand for acceleration in deploying advanced proteomic technologies to thoroughly comprehend the intricacies of complex and rapidly evolving plant–pathogen interactions.     

A negative effect of a pathogen on its vector? A plant pathogen increases the vulnerability of its vector to attack by natural enemies

Plant pathogens that are dependent on arthropod vectors for transmission from host to host may enhance their own success by promoting vector survival and/or performance. The effect of pathogens on vectors may be direct or indirect, with indirect effects mediated by increases in host quality or reductions in the vulnerability of vectors to natural enemies. We investigated whether the bird cherry-oat aphid Rhopalosiphum padi, a vector of cereal yellow dwarf virus (CYDV) in wheat, experiences a reduction in rates of attack by the parasitoid wasp Aphidius colemani when actively harboring the plant pathogen. We manipulated the vector status of aphids (virus carrying or virus free) and evaluated the impact on the rate of attack by wasps. We found that vector status did not influence the survival or fecundity of aphids in the absence of parasitoids. However, virus-carrying aphids experienced higher rates of parasitism and greater overall population suppression by parasitoid wasps than virus-free aphids. Moreover, virus-carrying aphids were accepted as hosts by wasps more often than virus-free aphids, with a greater number of wasps stinging virus-carrying aphids following assessment by antennal palpations than virus-free aphids. Therefore, counter to the prevailing idea that persistent vector-borne pathogens enhance the performance of their vectors, we found that infectious aphids actively carrying a plant pathogen experience greater vulnerability to natural enemies. Our results suggest that parasitoids may contribute to the successful biological control of CYDV by disproportionately impacting virus-carrying vectors, and thus reducing the proportion of vectors in the population that are infectious.     

Fungal pathogen species richness: why do some plant species have more pathogens than others?

Variation among plant species in the number of associated herbivore and pathogen species is predicted to fit a species-area relationship in which the area or biomass embodied by a plant species is a function of individual size and geographic range size. This hypothesis is tested using published estimates of geographic range, individual size, and species richness of fungal pathogens for 490 plant species occurring in the United States and controlling for sampling intensity and phylogenetic effects. The number of pathogens found on a plant species increases with the metrics of area and/or habitat diversity of plant species, and their effects are similar between gymnosperm and angiosperm lineages. The strength of this pattern across a diverse set of plant lineages suggests that accumulation and persistence of pathogen species on plant species are governed by similar processes among temperate plants.     

Plant-mediated effects on an insect–pathogen interaction vary with intraspecific genetic variation in plant defences

Baculoviruses are food-borne microbial pathogens that are ingested by insects on contaminated foliage. Oxidation of plant-derived phenolics, activated by insect feeding, can directly interfere with infections in the gut. Since phenolic oxidation is an important component of plant resistance against insects, baculoviruses are suggested to be incompatible with plant defences. However, plants among and within species invest differently in a myriad of chemical and physical defences. Therefore, we hypothesized that among eight soybean genotypes, some genotypes would be able to maintain both high resistance against an insect pest and high efficacy of a baculovirus. Soybean constitutive (non-induced) and jasmonic acid (JA)-induced (anti-herbivore response) resistance was measured against the fall armyworm Spodoptera frugiperda (weight gain, leaf consumption and utilization). Indicators of phenolic oxidation were measured as foliar phenolic content and peroxidase activity. Levels of armyworm mortality inflicted by baculovirus (SfMNPV) did not vary among soybean genotypes when the virus was ingested with non-induced foliage. Ingestion of the virus on JA-induced foliage reduced armyworm mortality, relative to non-induced foliage, on some soybean genotypes. Baculovirus efficacy was lower when ingested with foliage that contained higher phenolic content and defensive properties that reduced armyworm weight gain and leaf utilization. However, soybean genotypes that defended the plant by reducing consumption rate and strongly deterred feeding upon JA-induction did not reduce baculovirus efficacy, indicating that these defences may be more compatible with baculoviruses to maximize plant protection. Differential compatibility of defence traits with the third trophic level highlights an important cost/trade-off associated with plant defence strategies.     

Brothers in arms? Common and contrasting themes in pathogen perception by plant NB-LRR and animal NACHT-LRR proteins

Both plant and animal genomes encode proteins with nucleotide binding domains fused to leucine-rich repeat domains that are involved in responses to pathogens. While these domain structures are probably an example of convergent evolution, there are a number of similarities in the core mechanisms by which these proteins are regulated.     

Testing of life history traits of a soilborne pathogen in vitro: Do characteristics of oospores change according the strains of Aphanomyces euteiches and the host plant infected by the pathogen?

Aphanomyces euteiches is a polyphagous, homothallic soilborne pathogen producing asexual (zoospores) and sexual (oospores) spores. Even if oospores are essential for disease development and survival, to date, no study has focused on the production rates of oospores or the quality of the offspring produced by oospores. In this study, a nonabrasive oospore extraction method from infected roots of leguminous species (pea, faba bean and vetch) was developed. This methodology includes steps of grinding and filtration. The quality of oospores (viable, dormant and dead) was assessed with tetrazolium bromide staining, and germination of oospores was tested using exudates of peas, faba bean and vetch. The average yield of the extraction method was approximately 21%. Staining revealed some differences between strains and between leguminous species. The germination percentage of oospores extracted from pea, faba bean and vetch was 25%, 62% and 70%, respectively, and a significant difference was observed according to the origin of A. euteiches‐inoculated strains. Application of exudates seems to stimulate the germination of oospores (2% for the control, 18% for pea exudates and 1% for vetch exudates). Differences observed between A. euteiches strains and leguminous species indicate that more knowledge concerning the biology of oospores is needed. This will help to better estimate evolution process of the pathogen and manage resistance and crop successions.     

Using functional–structural plant models to study, understand and integrate plant development and ecophysiology

Functional–structural plant models (FSPMs) explore and integrate relationships between a plant’s structure and processes that underlie its growth and development. In recent years, the range of topics being addressed by scientists interested in functional–structural plant modelling has expanded greatly. FSPM techniques are now being used to dynamically simulate growth and development occurring at the microscopic scale involving cell division in plant meristems to the macroscopic scales of whole plants and plant communities. The plant types studied also cover a broad spectrum from algae to trees. FSPM is highly interdisciplinary and involves scientists with backgrounds in plant physiology, plant anatomy, plant morphology, mathematics, computer science, cellular biology, ecology and agronomy. This special issue of Annals of Botany features selected papers that provide examples of comprehensive functional–structural models, models of key processes such as partitioning of resources, software for modelling plants and plant environments, data acquisition and processing techniques and applications of functional–structural plant models for agronomic purposes.     

Microbial endoxylanases: effective weapons to breach the plant cell-wall barrier or, rather, triggers of plant defense systems?

Endo-beta-1,4-xylanases (EC 3.2.1.8) are key enzymes in the degradation of xylan, the predominant hemicellulose in the cell walls of plants and the second most abundant polysaccharide on earth. A number of endoxylanases are produced by microbial phytopathogens responsible for severe crop losses. These enzymes are considered to play an important role in phytopathogenesis, as they provide essential means to the attacking organism to break through the plant cell wall. Plants have evolved numerous defense mechanisms to protect themselves against invading pathogens, amongst which are proteinaceous inhibitors of cell wall-degrading enzymes. These defense mechanisms are triggered when a pathogen-derived elicitor is recognized by the plant. In this review, the diverse aspects of endoxylanases in promoting virulence and in eliciting plant defense systems are highlighted. Furthermore, the role of the relatively recently discovered cereal endoxylanase inhibitor families TAXI (Triticum aestivum xylanase inhibitor) and XIP (xylanase inhibitor protein) in plant defense is discussed.