Nucleotide-binding leucine-rich repeat network underlies nonhost resistance of pepper against the Irish potato famine pathogen Phytophthora infestans.

Nonhost resistance (NHR) is a robust plant immune response against non-adapted pathogens. A number of nucleotide-binding leucine-rich repeat (NLR) proteins that recognize non-adapted pathogens have been identified, although the underlying molecular mechanisms driving robustness of NHR are still unknown. Here, we screened 57 effectors of the potato late blight pathogen Phytophthora infestans in nonhost pepper (Capsicum annuum) to identify avirulence effector candidates. Selected effectors were tested against 436 genome-wide cloned pepper NLRs, and we identified multiple functional NLRs that recognize P. infestans effectors and confer disease resistance in the Nicotiana benthamiana as a surrogate system. The identified NLRs were homologous to known NLRs derived from wild potatoes that recognize P. infestans effectors such as Avr2, Avrblb1, Avrblb2, and Avrvnt1. The identified CaRpi-blb2 is a homologue of Rpi-blb2, recognizes Avrblb2 family effectors, exhibits feature of lineage-specifically evolved gene in microsynteny and phylogenetic analyses, and requires pepper-specific NRC (NLR required for cell death)-type helper NLR for proper function. Moreover, CaRpi-blb2-mediated hypersensitive response and blight resistance were more tolerant to suppression by the PITG_15 278 than those mediated by Rpi-blb2. Combined results indicate that pepper has stacked multiple NLRs recognizing effectors of non-adapted P. infestans, and these NLRs could be more tolerant to pathogen-mediated immune suppression than NLRs derived from the host plants. Our study suggests that NLRs derived from nonhost plants have potential as untapped resources to develop crops with durable resistance against fast-evolving pathogens by stacking the network of nonhost NLRs into susceptible host plants.

Natural variation in Avr3D1 from Zymoseptoria sp. contributes to quantitative gene-for-gene resistance and to host specificity.

Successful host colonization by plant pathogens requires the circumvention of host defense responses, frequently through sequence modifications in secreted pathogen proteins known as avirulence factors (Avrs). Although Avr sequences are often polymorphic, the contribution of these polymorphisms to virulence diversity in natural pathogen populations remains largely unexplored. We used molecular genetic tools to determine how natural sequence polymorphisms of the avirulence factor Avr3D1 in the wheat pathogen Zymoseptoria tritici contributed to adaptive changes in virulence. We showed that there is a continuous distribution in the magnitude of resistance triggered by different Avr3D1 isoforms and demonstrated that natural variation in an Avr gene can lead to a quantitative resistance phenotype. We further showed that homologues of Avr3D1 in two nonpathogenic sister species of Z. tritici are recognized by some wheat cultivars, suggesting that Avr-R gene-for-gene interactions can contribute to nonhost resistance. We suggest that the mechanisms underlying host range, qualitative resistance, and quantitative resistance are not exclusive.

Differential Virulence Contributions of the Efflux Transporter MexAB-OprM in Pseudomonas syringae Infecting a Variety of Host Plants.

Efflux transporters such as MexAB-OprM contribute to bacterial resistance to diverse antimicrobial compounds. Here, we show that MexB contributes to epiphytic and late-stage apoplastic growth of Pseudomonas syringae strain B728a, as well as lesion formation in common bean (Phaseolus vulgaris). Although a ∆mexB mutant formed fewer lesions after topical application to common bean, these lesions contain the same number of cells (105 to 107 cells) as those caused by the wild-type strain. The internalized population size of both the wild-type and the ∆mexB mutant within small samples of surface-sterilized asymptomatic portions of leaves varied from undetectably low to as high as 105 cells/cm2. Localized bacterial populations within individual lesions consistently exceeded 105 cells/cm2. Strain B728a was capable of moderate to extensive apoplastic growth in diverse host plants, including lima bean (P. lunatus), fava bean (Vicia faba), pepper (Capsicum annuum), Nicotiana benthamiana, sunflower (Helianthus annuus), and tomato (Solanum lycopersicum), but MexB was not required for growth in a subset of these plant species. A model is proposed that MexB provides resistance to as-yet-unidentified antimicrobials that differ between plant species. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Maize and Common Bean Seed Exudates Mediate Part of Nonhost Resistance to Phytophthora sojae Prior to Infection.

Phytophthora sojae does not infect nonhost maize (Zea mays) but infects nonhost common bean (Phaseolus vulgaris) under inoculation. Soybean seed exudates participate in mediating host resistance to P. sojae before infection. This study aims to elucidate the role of seed exudates in mediating the nonhost resistance of maize and common bean to P. sojae before infection. The behaviors of P. sojae zoospores in response to the seed exudates were determined using an assay chamber and a concave slide. The proteomes of P. sojae zoospores in response to the seed exudates were analyzed with the tandem mass tag method. The key proteins were quantitatively verified by parallel reaction monitoring. Maize seed exudates exerted a repellent effect on zoospores of P. sojae. This result explains why zoospores sense repelling signaling molecules in maize seed exudates that weaken and strongly inhibit chemotaxis signals in the phosphatidylinositol signaling pathway and arachidonic acid metabolism pathway. Common bean seed exudates did not exhibit any attraction to the zoospores because the guanine nucleotide-binding protein signaling pathway, which is responsible for transmitting chemotactic signals, had no significant change. The proteins protecting the cell membrane structure were significantly downregulated, and the early apoptosis signal glutathione was enhanced in zoospores responding to common bean seed exudates, which resulted in dissolution of the cysts. Maize and common bean seed exudates mediate part of the nonhost resistance to P. sojae via different mechanisms before infection. The immunity of maize to P. sojae is caused by the repellent effect of maize seed exudates on zoospores. Common bean seed exudates participate in mediating nonhost resistance by dissolving the cysts.

Epidermal CCA1 and PMR5 contribute to nonhost resistance in Arabidopsis.

Nonhost resistance (NHR) is the most robust and durable resistance in plants, but its spatiotemporal regulation is poorly understood. The circadian clock functions in a tissue-specific manner and regulates individual physiological processes in plants. Using mutant and RNA-seq analyses, we revealed a role of CIRCADIAN CLOCK ASSOCIATED1 (CCA1) in tissue-specific and time-of-day-specific regulation of NHR to Pyricularia oryzae (syn. Magnaporthe oryzae) in Arabidopsis thaliana (Arabidopsis). Targeted perturbation of CCA1 function in epidermis compromised time-of-day-specific regulation of NHR to P. oryzae in Arabidopsis. RNA-seq analysis showed that P. oryzae inoculation alters the transcriptome in penetration 2 (pen2) plants and identified POWDERY MILDEW RESISTANCE 5 (PMR5) as a candidate gene of direct targets of CCA1. Time-of-day-specific penetration resistance to P. oryzae was reduced in Arabidopsis pen2 pmr5 mutant plants. These findings suggest that epidermal CCA1 and PMR5 contribute to the establishment of time-of-day-specific NHR to P. oryzae in Arabidopsis.

Transgressive segregation reveals mechanisms of Arabidopsis immunity to Brassica-infecting races of white rust (Albugo candida).

Arabidopsis thaliana accessions are universally resistant at the adult leaf stage to white rust (Albugo candida) races that infect the crop species Brassica juncea and Brassica oleracea We used transgressive segregation in recombinant inbred lines to test if this apparent species-wide (nonhost) resistance in A. thaliana is due to natural pyramiding of multiple Resistance (R) genes. We screened 593 inbred lines from an Arabidopsis multiparent advanced generation intercross (MAGIC) mapping population, derived from 19 resistant parental accessions, and identified two transgressive segregants that are susceptible to the pathogen. These were crossed to each MAGIC parent, and analysis of resulting F2 progeny followed by positional cloning showed that resistance to an isolate of A. candida race 2 (Ac2V) can be explained in each accession by at least one of four genes encoding nucleotide-binding, leucine-rich repeat (NLR) immune receptors. An additional gene was identified that confers resistance to an isolate of A. candida race 9 (AcBoT) that infects B. oleracea Thus, effector-triggered immunity conferred by distinct NLR-encoding genes in multiple A. thaliana accessions provides species-wide resistance to these crop pathogens.

Emerging Roles of Motile Epidermal Chloroplasts in Plant Immunity.

Plant epidermis contains atypical small chloroplasts. However, the physiological role of this organelle is unclear compared to that of large mesophyll chloroplasts, the well-known function of which is photosynthesis. Although knowledge of the involvement of chloroplasts in the plant immunity has been expanded to date, the differences between the epidermal and mesophyll chloroplasts are beyond the scope of this study. Given the role of the plant epidermis as a barrier to environmental stresses, including pathogen attacks, and the immune-related function of chloroplasts, plant defense research on epidermal chloroplasts is an emerging field. Recent studies have revealed the dynamic movements of epidermal chloroplasts in response to fungal and oomycete pathogens. Furthermore, epidermal chloroplast-associated proteins and cellular events that are tightly linked to epidermal resistance against pathogens have been reported. In this review, I have focused on the recent progress in epidermal chloroplast-mediated plant immunity.

Photoperiod Following Inoculation of Arabidopsis with Pyricularia oryzae (syn. Magnaporthe oryzae) Influences on the Plant-Pathogen Interaction.

In plant-pathogen interactions, a proper light environment affects the establishment of defense responses in plants. In our previous experiments, we found that nonhost resistance (NHR) to Pyricularia oryzae Cav. in Arabidopsis thaliana (L.) Heynh. (Arabidopsis), in diurnal conditions, varies with the inoculation time. Moreover, we indicated that the circadian clock plays an important role in regulating time-of-day differences in NHR to P. oryzae in Arabidopsis. However, the involvement of photoperiod in regulating NHR was still not understood. To determine the photoperiod role, we performed the experiments in continuous light and darkness during the early Arabidopsis-P. oryzae interaction. We found that the light period after the inoculation in the evening enhanced the resistance to penetration. However, the dark period after the inoculation in the morning suppressed the penetration resistance. Furthermore, the genetic analysis indicated that jasmonic acid, reactive oxygen species, and tryptophan-derived metabolite(s) contribute to the photoperiod regulation of NHR in Arabidopsis. The present results denote that photoperiod plays an important role in regulating time-of-day differences in NHR to P. oryzae in Arabidopsis.

A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in Arabidopsis thaliana.

Nonhost resistance of Arabidopsis thaliana against Phytophthora infestans, a filamentous eukaryotic microbe and the causal agent of potato late blight, is based on a multilayered defense system. Arabidopsis thaliana controls pathogen entry through the penetration-resistance genes PEN2 and PEN3, encoding an atypical myrosinase and an ABC transporter, respectively, required for synthesis and export of unknown indole compounds. To identify pathogen-elicited leaf surface metabolites and further unravel nonhost resistance in Arabidopsis, we performed untargeted metabolite profiling by incubating a P. infestans zoospore suspension on leaves of WT or pen3 mutant Arabidopsis plants. Among the plant-secreted metabolites, 4-methoxyindol-3-yl-methanol and S-(4-methoxy-indol-3-yl-methyl) cysteine were detected in spore suspensions recollected from WT plants, but at reduced levels from the pen3 mutant plants. In both whole-cell and microsome-based assays, 4-methoxyindol-3-yl-methanol was transported in a PEN3-dependent manner, suggesting that this compound is a PEN3 substrate. The syntheses of both compounds were dependent on functional PEN2 and phytochelatin synthase 1. None of these compounds inhibited mycelial growth of P. infestans in vitro Of note, exogenous application of 4-methoxyindol-3-yl methanol slightly elevated cytosolic Ca2+ levels and enhanced callose deposition in hydathodes of seedlings treated with a bacterial pathogen-associated molecular pattern (PAMP), flagellin (flg22). Loss of flg22-induced callose deposition in leaves of pen3 seedlings was partially reverted by the addition of 4-methoxyindol-3-yl methanol. In conclusion, we have identified a specific indole compound that is a substrate for PEN3 and contributes to the plant defense response against microbial pathogens.

What are the Top 10 Unanswered Questions in Molecular Plant-Microbe Interactions?

This article is part of the Top 10 Unanswered Questions in MPMI invited review series.The past few decades have seen major discoveries in the field of molecular plant-microbe interactions. As the result of technological and intellectual advances, we are now able to answer questions at a level of mechanistic detail that we could not have imagined possible 20 years ago. The MPMI Editorial Board felt it was time to take stock and reassess. What big questions remain unanswered? We knew that to identify the fundamental, overarching questions that drive our research, we needed to do this as a community. To reach a diverse audience of people with different backgrounds and perspectives, working in different areas of plant-microbe interactions, we queried the more than 1,400 participants at the 2019 International Congress on Molecular Plant-Microbe Interactions meeting in Glasgow. This group effort resulted in a list of ten, broad-reaching, fundamental questions that influence and inform our research. Here, we introduce these Top 10 unanswered questions, giving context and a brief description of the issues. Each of these questions will be the subject of a detailed review in the coming months. We hope that this process of reflecting on what is known and unknown and identifying the themes that underlie our research will provide a framework to use going forward, giving newcomers a sense of the mystery of the big questions and inspiring new avenues and novel insights.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

What is the Molecular Basis of Nonhost Resistance?

This article is part of the Top 10 Unanswered Questions in MPMI invited review series.Nonhost resistance is typically considered the ability of a plant species to repel all attempts of a pathogen species to colonize it and reproduce on it. Based on this common definition, nonhost resistance is presumed to be very durable and, thus, of great interest for its potential use in agriculture. Despite considerable research efforts, the molecular basis of this type of plant immunity remains nebulous. We here stress the fact that "nonhost resistance" is a phenomenological rather than a mechanistic concept that comprises more facets than typically considered. We further argue that nonhost resistance essentially relies on the very same genes and pathways as other types of plant immunity, of which some may act as bottlenecks for particular pathogens on a given plant species or under certain conditions. Thus, in our view, the frequently used term "nonhost genes" is misleading and should be avoided. Depending on the plant-pathogen combination, nonhost resistance may involve the recognition of pathogen effectors by host immune sensor proteins, which might give rise to host shifts or host range expansions due to evolutionary-conditioned gains and losses in respective armories. Thus, the extent of nonhost resistance also defines pathogen host ranges. In some instances, immune-related genes can be transferred across plant species to boost defense, resulting in augmented disease resistance. We discuss future routes for deepening our understanding of nonhost resistance and argue that the confusing term "nonhost resistance" should be used more cautiously in the light of a holistic view of plant immunity.

Plasticity of Phymatotrichopsis omnivora infection strategies is dependent on host and nonhost plant responses.

Necrotrophic fungi constitute the largest group of plant fungal pathogens that cause heavy crop losses worldwide. Phymatotrichopsis omnivora is a broad host, soil-borne necrotrophic fungal pathogen that infects over 2,000 dicotyledonous plants. The molecular basis of such broad host range is unknown. We conducted cell biology and transcriptomic studies in Medicago truncatula (susceptible), Brachypodium distachyon (resistant/nonhost), and Arabidopsis thaliana (partially resistant) to understand P. omnivora virulence mechanisms. We performed defence gene analysis, gene enrichments, and correlational network studies during key infection stages. We identified that P. omnivora infects the susceptible plant as a traditional necrotroph. However, it infects the partially resistant plant as a hemi-biotroph triggering salicylic acid-mediated defence pathways in the plant. Further, the infection strategy in partially resistant plants is determined by the host responses during early infection stages. Mutant analyses in A. thaliana established the role of small peptides PEP1 and PEP2 in defence against P. omnivora. The resistant/nonhost B. distachyon triggered stress responses involving sugars and aromatic acids. Bdwat1 mutant analysis identified the role of cell walls in defence. This is the first report that describes the plasticity in infection strategies of P. omnivora providing insights into broad host range.

CCA1 and LHY contribute to nonhost resistance to Pyricularia oryzae (syn. Magnaporthe oryzae) in Arabidopsis thaliana.

The circadian clock enables plants to adapt to their environment and control numerous physiological processes, including plant-pathogen interactions. However, it is unknown if the circadian clock controls nonhost resistance (NHR) in plants. To find out, we analyzed microarray data with the web-based tool DIURNAL to reveal that NHR-related genes show rhythmic expression patterns in the absence of a pathogen challenge. Our clock mutant analyses found that cca1-1 lhy-11 double mutant showed compromised NHR to Pyricularia oryzae, suggesting that two components of the circadian clock, CCA1 and LHY, are involved in regulating penetration resistance in Arabidopsis thaliana. By analyzing pen2 double mutants, we revealed that CCA1 contributes to time-of-day-dependent penetration resistance as a positive regulator and that LHY regulates post-penetration resistance as a positive regulator. Taken together, our results suggest that the circadian clock regulates the time-of-day-dependent NHR to P. oryzae and thus enables A. thaliana to counteract pathogen attacks.Abbreviations: EE: evening element; ETI: effector-triggered immunity; NHR: nonhost resistance; PAMP: pathogen-associated molecular pattern; PTI: PAMP-triggered immunity; SAR: systemic acquired resistance.

Morpho-Pathological and Global Transcriptomic Analysis Reveals the Robust Nonhost Resistance Responses in Chickpea Interaction with Alternaria brassicae.

Alternaria blight, caused by Alternaria brassicae, causes considerable yield loss in Brassica crops. While several blight-resistant varieties have been developed using resistance sources from host germplasm, none of them are entirely successful in imparting durable resistance. This has prompted the exploration of novel gene pools of nonhost plant species. Nonhost resistance (NHR) is a durable form of resistance, comprising pre- and postinvasion layers of defense. We aimed to identify the molecular basis of NHR to A. brassicae and identify the layers of NHR operating in a nonhost, chickpea (Cicer arietinum). To elucidate the layers of NHR operating against A. brassicae, we compared the histopathology and infection patterns of A. brassicae in C. arietinum and Brassica juncea. Delayed conidial germination, impeded hyphal growth, suppressed appressorium formation, and limited hyphal penetration occurred in the nonhost plant compared with the host plant, implying the involvement of the preinvasion layer of NHR in C. arietinum. Next, we investigated the molecular basis of robust NHR, in C. arietinum challenged with A. brassicae, by microarray-based global transcriptome profiling. Genes involved in stomatal closure, cuticular wax biosynthesis, cell-wall modification, and secondary metabolite production (contributing to preinvasion NHR) as well as reactive oxygen species (ROS) and cell death (contributing to postinvasion NHR) were found to be upregulated. Consistent with transcriptomic analysis, the morpho-pathological analysis revealed stomatal closure, ROS accumulation, and localized cell death in C. arietinum as the defense strategies against A. brassicae. Thus, we identified NHR-contributing genes with potential applications in blight resistance gene transfer to B. juncea.

Whole Genome Sequence Resource of the Asian Pear Scab Pathogen Venturia nashicola.

Venturia nashicola, the cause of scab disease of Asian pears, is a host-specific, biotrophic fungus. It is restricted to Asia and is regarded as a quarantine threat outside this region. European pear displays nonhost resistance (NHR) to V. nashicola and Asian pears are nonhosts of V. pyrina (the cause of European pear scab disease). The host specificity of these two fungi is likely governed by differences in their effector arsenals, with a subset hypothesized to activate NHR. The Pyrus-Venturia pathosystem provides an opportunity to dissect the underlying genetics of nonhost interactions in this potentially more durable form of resistance. The V. nashicola genome will enable comparisons to other Venturia spp. genomes to identify effectors that potentially activate NHR in the pear scab pathosystem.

Using forward genetics in Nicotiana benthamiana to uncover the immune signaling pathway mediating recognition of the Xanthomonas perforans effector XopJ4.

The immune pathway responsible for perception of the Xanthomonas perforans effector XopJ4 was identified in the plant Nicotiana benthamiana. This pathogen causes significant yield loss in commercial tomato cultivation. Genetic mapping and viral-induced gene silencing were used to identify immune signaling components of the XopJ4 perception pathway in N. benthamiana. Transient complementation assays were performed to determine the functionality of gene variants and co-immunoprecipitation assays were used to gain insight into the molecular mechanism of the pathway. Two N. benthamiana ethyl methanesulfonate (EMS) mutants deficient for XopJ4 perception were identified as having loss-of-function mutations in the gene encoding the nucleotide binding, leucine-rich repeat (NLR) protein NbZAR1. Silencing of a receptor-like cytoplasmic kinase family XII gene, subsequently named XOPJ4 IMMUNITY 2 (JIM2), blocks perception of XopJ4. This study demonstrates the feasibility of conducting mutant screens in N. benthamiana to investigate the genetic basis of the plant immune system and other processes. The identification of NbZAR1 and JIM2 as mediating XopJ4 perception in N. benthamiana supports the model of ZAR1 being involved in the perception of many different pathogen effector proteins with specificity dictated by associated receptor-like cytoplasmic kinases.

Exploring and exploiting the boundaries of host specificity using the cereal rust and mildew models.

Individual plants encounter a vast number of microbes including bacteria, viruses, fungi and oomycetes through their growth cycle, yet few of these pathogens are able to infect them. Plant species have diverged over millions of years, co-evolving with few specific pathogens. The host boundaries of most pathogen species can be clearly defined. In general, the greater the genetic divergence from the preferred host, the less likely that pathogen would be able to infect that plant species. Co-evolution and divergence also occur within pathogen species, leading to highly specialized subspecies with narrow host ranges. For example, cereal rust and mildew pathogens (Puccinia and Blumeria spp.) display high host specificity as a result of ongoing co-evolution with a narrow range of grass species. In rare cases, however, some plant species are in a transition from host to nonhost or are intermediate hosts (near nonhost). Barley was reported as a useful model for genetic and molecular studies of nonhost resistance due to rare susceptibility to numerous heterologous rust and mildew fungi. This review evaluates host specificity in numerous Puccinia/Blumeria-cereal pathosystems and discusses various approaches for transferring nonhost resistance (NHR) genes between crop species to reduce the impact of important diseases in food production.

SOBIR1 and AGB1 independently contribute to nonhost resistance to Pyricularia oryzae (syn. Magnaporthe oryzae) in Arabidopsis thaliana.

Rice blast caused by Pyricularia oryzae (syn. Magnaporthe oryzae) is a disease devastating to rice. We have studied the Arabidopsis-P. oryzae pathosystem as a model system for nonhost resistance (NHR) and found that SOBIR1, but not BAK1, is a positive regulator of NHR to P. oryzae in Arabidopsis. AGB1 is also involved in NHR. However, the genetic interactions between SOBIR1, BAK1, and AGB1 are uncharacterized. In this study, we delineated the genetic interactions between SOBIR1, BAK1, and AGB1 in NHR to P. oryzae in Arabidopsis and found SOBIR1 and AGB1 independently control NHR to P. oryzae in Arabidopsis pen2-1 mutant plants. Furthermore, XLG2, but not TMM, has a positive role in penetration resistance to P. oryzae in Arabidopsis pen2-1 mutant plants. Our study characterized genetic interactions in Arabidopsis NHR. Abbreviations: PRR: pattern recognition receptor, RLK: receptor-like kinase, RLP: receptor-like protein, BAK1: BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED RECEPTOR KINASE 1, BIR1: BAK1-INTERACTING RECEPTOR-LIKE KINASE 1, SOBIR1: SUPPRESSOR OF BIR1-1-1, AGB1: ARABIDOPSIS G PROTEIN ß-SUBUNIT 1, XLG2: EXTRA-LARGE G PROTEIN 2.

A comparative analysis of nonhost resistance across the two Triticeae crop species wheat and barley.

BACKGROUND: Nonhost resistance (NHR) protects plants against a vast number of non-adapted pathogens which implicates a potential exploitation as source for novel disease resistance strategies. Aiming at a fundamental understanding of NHR a global analysis of transcriptome reprogramming in the economically important Triticeae cereals wheat and barley, comparing host and nonhost interactions in three major fungal pathosystems responsible for powdery mildew (Blumeria graminis ff. ssp.), cereal blast (Magnaporthe sp.) and leaf rust (Puccinia sp.) diseases, was performed. RESULTS: In each pathosystem a significant transcriptome reprogramming by adapted- or non-adapted pathogen isolates was observed, with considerable overlap between Blumeria, Magnaporthe and Puccinia. Small subsets of these general pathogen-regulated genes were identified as differentially regulated between host and corresponding nonhost interactions, indicating a fine-tuning of the general pathogen response during the course of co-evolution. Additionally, the host- or nonhost-related responses were rather specific for each pair of adapted and non-adapted isolates, indicating that the nonhost resistance-related responses were to a great extent pathosystem-specific. This pathosystem-specific reprogramming may reflect different resistance mechanisms operating against non-adapted pathogens with different lifestyles, or equally, different co-option of the hosts by the adapted isolates to create an optimal environment for infection. To compare the transcriptional reprogramming between wheat and barley, putative orthologues were identified. Within the wheat and barley general pathogen-regulated genes, temporal expression profiles of orthologues looked similar, indicating conserved general responses in Triticeae against fungal attack. However, the comparison of orthologues differentially expressed between host and nonhost interactions revealed fewer commonalities between wheat and barley, but rather suggested different host or nonhost responses in the two cereal species. CONCLUSIONS: Taken together, our results suggest independent co-evolutionary forces acting on host pathosystems mirrored by barley- or wheat-specific nonhost responses. As a result of evolutionary processes, at least for the pathosystems investigated, NHR appears to rely on rather specific plant responses.

Expansion of sesquiterpene biosynthetic gene clusters in pepper confers nonhost resistance to the Irish potato famine pathogen.

Chemical barriers contribute to nonhost resistance, which is defined as the resistance of an entire plant species to nonadapted pathogen species. However, the molecular basis of metabolic defense in nonhost resistance remains elusive. Here, we report genetic evidence for the essential role of phytoalexin capsidiol in nonhost resistance of pepper (Capsicum spp.) to potato late blight Phytophthora infestans using transcriptome and genome analyses. Two different genes for capsidiol biosynthesis, 5-epi-aristolochene synthase (EAS) and 5-epi-aristolochene-1,3-dihydroxylase (EAH), belong to multigene families. However, only a subset of EAS/EAH gene family members were highly induced upon P. infestans infection, which was associated with parallel accumulation of capsidiol in P. infestans-infected pepper. Silencing of EAS homologs in pepper resulted in a significant decrease in capsidiol accumulation and allowed the growth of nonadapted P. infestans that is highly sensitive to capsidiol. Phylogenetic and genomic analyses of EAS/EAH multigene families revealed that the emergence of pathogen-inducible EAS/EAH genes in Capsicum-specific genomic regions rendered pepper a nonhost of P. infestans. This study provides insights into evolutionary aspects of nonhost resistance based on the combination of a species-specific phytoalexin and sensitivity of nonadapted pathogens.