Resistance and Susceptibility of Plants to Fungal Pathogens

Plants are under continuous threat of infection by pathogens endowed with diverse strategies to colonize their host. Comprehensive biochemical and genetic approaches are now starting to reveal the complex signaling pathways that mediate plant disease resistance. Initiation of defense signaling often involves specific recognition of invading pathogens by the products of specialized host resistance (R) genes. Potential resistance signaling components have been identified by mutational analyses to be required for specific resistance in the model Arabidopsis and some crop species. Strikingly, many of the components share similarity to that of innate immune systems in animals. Evidence is also accumulating that plant pathogens have a number of ways to evade host defenses during the early stages of infection, similar to animal pathogens. These strategies are becoming much better understood in a number of plant–pathogen interactions. In this review, we focus on the current knowledge of host factors that control plant resistance and susceptibility to fungal pathogens. The knowledge accumulated in these studies will serve a fundamental basis for combating diseases in strategic molecular agriculture.     

Microbial Pathogens in the Fungal Kingdom

The fungal kingdom is vast, spanning ~1.5 to as many as 5 million species diverse as unicellular yeasts, filamentous fungi, mushrooms, lichens, and both plant and animal pathogens. The fungi are closely aligned with animals in one of the six to eight supergroups of eukaryotes, the opisthokonts. The animal and fungal kingdoms last shared a common ancestor ~1 billion years ago, more recently than other groups of eukaryotes. As a consequence of their close evolutionary history and shared cellular machinery with metazoans, fungi are exceptional models for mammalian biology, but prove more difficult to treat in infected animals. The last common ancestor to the fungal/metazoan lineages is thought to have been unicellular, aquatic, and motile with a posterior flagellum, and certain extant species closely resemble this hypothesized ancestor. Species within the fungal kingdom were traditionally assigned to four phyla, including the basal fungi (Chytridiomycota, Zygomycota) and the more recently derived monophyletic lineage, the dikarya (Ascomycota, Basidiomycota). The fungal tree of life project has revealed that the basal lineages are polyphyletic, and thus there are as many as eight to ten fungal phyla. Fungi that infect vertebrates are found in all of the major lineages, and virulence arose multiple times independently. A sobering recent development involves the species Batrachochytrium dendrobatidis from the basal fungal phylum, the Chytridiomycota, which has emerged to cause global amphibian declines and extinctions. Genomics is revolutionizing our view of the fungal kingdom, and genome sequences for zygomycete pathogens (Rhizopus, Mucor), skin-associated fungi (dermatophytes, Malassezia), and the Candida pathogenic species clade promise to provide insights into the origins of virulence. Here we survey the diversity of fungal pathogens and illustrate key principles revealed by genomics involving sexual reproduction and sex determination, loss of conserved pathways in derived fungal lineages that are retained in basal fungi, and shared and divergent virulence strategies of successful human pathogens, including dimorphic and trimorphic transitions in form. The overarching conclusion is that fungal pathogens of animals have arisen repeatedly and independently throughout the fungal tree of life, and while they share general properties, there are also unique features to the virulence strategies of each successful microbial pathogen.     

Imbalanced Lignin Biosynthesis Promotes the Sexual Reproduction of Homothallic Oomycete Pathogens

Lignin is incorporated into plant cell walls to maintain plant architecture and to ensure long-distance water transport. Lignin composition affects the industrial value of plant material for forage, wood and paper production, and biofuel technologies. Industrial demands have resulted in an increase in the use of genetic engineering to modify lignified plant cell wall composition. However, the interaction of the resulting plants with the environment must be analyzed carefully to ensure that there are no undesirable side effects of lignin modification. We show here that Arabidopsis thaliana mutants with impaired 5-hydroxyguaiacyl O-methyltransferase (known as caffeate O-methyltransferase; COMT) function were more susceptible to various bacterial and fungal pathogens. Unexpectedly, asexual sporulation of the downy mildew pathogen, Hyaloperonospora arabidopsidis, was impaired on these mutants. Enhanced resistance to downy mildew was not correlated with increased plant defense responses in comt1 mutants but coincided with a higher frequency of oomycete sexual reproduction within mutant tissues. Comt1 mutants but not wild-type Arabidopsis accumulated soluble 2-O-5-hydroxyferuloyl-l-malate. The compound weakened mycelium vigor and promoted sexual oomycete reproduction when applied to a homothallic oomycete in vitro. These findings suggested that the accumulation of 2-O-5-hydroxyferuloyl-l-malate accounted for the observed comt1 mutant phenotypes during the interaction with H. arabidopsidis. Taken together, our study shows that an artificial downregulation of COMT can drastically alter the interaction of a plant with the biotic environment.     

Fungicidal Activity of Volatiles from Selected Cruciferous Plants against Resting Propagules of Soil-borne Fungal Pathogens

The efficacy of volatiles evolved from tissues of nine cruciferous plants against resting propagules of Fusarium oxysporum var radicis f. sp. lycopersici, Sclerotium cepivorum, and Sclerotinia sclerotiorum was tested. The cruciferous plants released biocidal compounds, mainly isothiocyanates, produced during the enzymatic degradation of glucosinolates present in the plant cells. Among the plants investigated, the highest fungicidal activity and also the highest concentration of isothiocyanates were found in Brassica juncea. The resting propagules of tested fungi differed significantly in their sensitivity towards volatiles released from plant tissues.     

Influence of Pythium oligandrum Biocontrol on Fungal and Oomycete Population Dynamics in the Rhizosphere

Fungal and oomycete populations and their dynamics were investigated following the introduction of the biocontrol agent Pythium oligandrum into the rhizosphere of tomato plants grown in soilless culture. Three strains of P. oligandrum were selected on the basis of their ability to form oospores (resting structures) and to produce tryptamine (an auxin-like compound) and oligandrin (a glycoprotein elicitor). Real-time PCR and plate counting demonstrated the persistence of large amounts of the antagonistic oomycete in the rhizosphere throughout the cropping season (April to September). Inter-simple-sequence-repeat analysis of the P. oligandrum strains collected from root samples at the end of the cropping season showed that among the three strains used for inoculation, the one producing the smallest amount of oospores was detected at 90%. Single-strand conformational polymorphism analysis revealed increases in the number of members and the complexity of the fungal community over time. There were no significant differences between the microbial ecosystems inoculated with P. oligandrum and those that were not treated, except for a reduction of Pythium dissotocum (ubiquitous tomato root minor pathogen) populations in inoculated systems during the last 3 months of culture. These findings raise interesting issues concerning the use of P. oligandrum strains producing elicitor and auxin molecules for plant protection and the development of biocontrol.In soilless cultures, the recycling of drainage water within a system is the consequence of new laws concerning water saving and limitation of pollution. Such closed systems minimize costs by conserving water and reducing fertilizer input; however, they may favor the dissemination of pathogens (13). When pathogens manage to enter recirculation systems, they are rapidly disseminated and may cause disease epidemics, particularly during periods of stress, e.g., stress due to high temperatures and/or to low levels of dissolved oxygen in the nutrient solution. Thus, numerous facultative pathogens commonly found in conventional cultures may become economically significant (53). Several of them, e.g., Pythium spp. and Phytophthora spp., are well adapted to the aquatic environment of hydroponic systems: they produce flagellate zoospores which enable them to swim in the nutrient solution, facilitating the spread of infection (18, 21, 36, 54, 61).Various methods are used to reduce the risks to plant health. Over recent years, the disinfection of nutrient solutions by physical or chemical treatments, e.g., ozonization, UV irradiation, chlorination, and thermo-disinfection, has been developed (13, 38). These methods effectively destroy pathogenic microorganisms but are harmful to species liable to benefit the plant, to be used as biocontrol agents, or both. Indeed, recirculation of nutrient solutions in closed hydroponic systems favors the establishment of a potentially suppressive microflora besides the pathogenic microflora (16, 28, 39, 41). The development of a beneficial microflora may thus be impeded by treatments used to destroy pathogenic microorganisms. Consequently, interest has been focused on the management of microorganisms in soilless cultures (12). Postma and coworkers (40) found that the extent of root disease is increased by the use of autoclaved rock wool. Tu and coworkers (59) observed that root rot disease was less severe in closed hydroponic systems than in open cultures and suggested that the difference was due to a higher density of bacteria in the closed systems. According to Paulitz (34), the diversity of microorganisms in soilless cultures is more limited than that in conventional soil cultures, such that conditions are more suitable for beneficial microorganisms, and consequently for effective biological control, in soilless than in conventional soil cultures.Biocontrol strategies are promising (7, 35). However, both biotic and abiotic factors may affect the performance of biocontrol methods. Relevant biotic factors include interactions with nontarget microorganisms (6), poor implantation of the biocontrol agent due to nonadaptation to the hydroponic system or resistance from the native microflora, shelf life and formulation, and host plant species and cultivar effects. Abiotic factors include climatic, chemical, and physical conditions of the soil or rhizosphere.Despite the limitations, various studies report evidence of the suppression of disease following the inoculation of hydroponic systems with antagonistic microorganisms. In particular, Pythium oligandrum is an effective biocontrol agent (2, 14, 49, 64). This oomycete colonizes roots without damaging the host plant cells (24, 45) and survives in the rhizosphere, where it exerts its biocontrol (57). P. oligandrum acts through both direct effects (mycoparasitism, antibiosis, and competition for nutrients and space) and indirect effects (stimulation of plant defense reactions and plant growth promotion) (49). The operating effects seem to depend on the type of pathogenic fungi being controlled (3, 48, 49). Le Floch and coworkers suggested that mycoparasitism is not the main mode of action (23). Root colonization by P. oligandrum may induce systemic resistance associated with the synthesis of elicitors protecting the plant from its aggressors (4, 17, 31, 37, 56). Several studies have investigated formulations of P. oligandrum oospores applied to soil or seeds, and their production and use, to optimize the efficacy of biocontrol (9, 30).Effective biocontrol by P. oligandrum may be limited by its heterogeneous implantation in the rhizosphere (46). Therefore, enhanced implantation and persistence of P. oligandrum in the rhizosphere should improve plant protection. We report an investigation of the persistence of P. oligandrum and its impact on the native fungal microflora of the roots. Three strains with characteristic traits were selected to constitute an inoculum applied to tomato plant roots. The characteristics of the strains were the production of oospores to allow root colonization and favor persistence, the synthesis of tryptamine, a plant growth enhancer (22), and the production of oligandrin, a plant-protective elicitor (37). The inoculated rhizospheres were monitored to evaluate the persistence of the strains and their effects on the microflora. The populations of the common tomato root pathogen P. dissotocum (endemic in the studied systems) and of P. oligandrum were both assessed by plate counting and real-time PCR. The strain(s) of P. oligandrum responsible for the colonization of the rhizosphere was identified by inter-simple-sequence-repeat (ISSR) methodology. Single-strand conformational polymorphism (SSCP) investigations were used to study the effects of P. oligandrum on the fungal populations colonizing the rhizosphere and the fungal dynamics throughout the cropping season.     

Genetic Susceptibility to Fungal Infections in Humans

Most fungal infections in humans occur in the setting of iatrogenic immunosuppression or HIV infection. In the absence of these factors, fungi cause mild, self-limited infections that typically involve mucocutaneous surfaces. Hence, when persistent or recurrent mucocutaneous infections (chronic mucocutaneous candidiasis [CMC]) or invasive fungal infections (IFIs) develop in a “normal” host, they are indicative of genetic defects causing innate or adaptive immune dysfunction. In this review, recent developments concerning genetic and immunologic factors that affect the risk for IFIs and CMC are critically discussed.