The barley immune receptor Mla recognizes multiple pathogens and contributes to host range dynamics.
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ABSTRACT:
SUBMITTER: Bettgenhaeuser J
PROVIDER: S-EPMC8617247 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Fungal plant pathogens secrete effector molecules to establish disease on their hosts, and plants in turn use immune receptors to try to intercept these effectors. The tomato immune receptor Ve1 governs resistance to race 1 strains of the soil-borne vascular wilt fungi Verticillium dahliae and Verticillium albo-atrum, but the corresponding Verticillium effector remained unknown thus far. By high-throughput population genome sequencing, a single 50-Kb sequence stretch was identified that only occurs in race 1 strains, and subsequent transcriptome sequencing of Verticillium-infected Nicotiana benthamiana plants revealed only a single highly expressed ORF in this region, designated Ave1 (for Avirulence on Ve1 tomato). Functional analyses confirmed that Ave1 activates Ve1-mediated resistance and demonstrated that Ave1 markedly contributes to fungal virulence, not only on tomato but also on Arabidopsis. Interestingly, Ave1 is homologous to a widespread family of plant natriuretic peptides. Besides plants, homologous proteins were only found in the bacterial plant pathogen Xanthomonas axonopodis and the plant pathogenic fungi Colletotrichum higginsianum, Cercospora beticola, and Fusarium oxysporum f. sp. lycopersici. The distribution of Ave1 homologs, coincident with the presence of Ave1 within a flexible genomic region, strongly suggests that Verticillium acquired Ave1 from plants through horizontal gene transfer. Remarkably, by transient expression we show that also the Ave1 homologs from F. oxysporum and C. beticola can activate Ve1-mediated resistance. In line with this observation, Ve1 was found to mediate resistance toward F. oxysporum in tomato, showing that this immune receptor is involved in resistance against multiple fungal pathogens.
| S-EPMC3323992 | biostudies-literature
Project description:Disease-resistance genes encoding intracellular nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are key components of the plant innate immune system and typically detect the presence of isolate-specific avirulence (AVR) effectors from pathogens. NLR genes define the fastest-evolving gene family of flowering plants and are often arranged in gene clusters containing multiple paralogs, contributing to copy number and allele-specific NLR variation within a host species. Barley mildew resistance locus a (Mla) has been subject to extensive functional diversification, resulting in allelic resistance specificities each recognizing a cognate, but largely unidentified, AVRa gene of the powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). We applied a transcriptome-wide association study among 17 Bgh isolates containing different AVRa genes and identified AVRa1 and AVRa13, encoding candidate-secreted effectors recognized by Mla1 and Mla13 alleles, respectively. Transient expression of the effector genes in barley leaves or protoplasts was sufficient to trigger Mla1 or Mla13 allele-specific cell death, a hallmark of NLR receptor-mediated immunity. AVRa1 and AVRa13 are phylogenetically unrelated, demonstrating that certain allelic MLA receptors evolved to recognize sequence-unrelated effectors. They are ancient effectors because corresponding loci are present in wheat powdery mildew. AVRA1 recognition by barley MLA1 is retained in transgenic Arabidopsis, indicating that AVRA1 directly binds MLA1 or that its recognition involves an evolutionarily conserved host target of AVRA1 Furthermore, analysis of transcriptome-wide sequence variation among the Bgh isolates provides evidence for Bgh population structure that is partially linked to geographic isolation.
| S-EPMC5081590 | biostudies-literature
Project description:Nucleotide-binding leucine-rich repeat receptors (NLRs) recognize pathogen effectors to mediate plant disease resistance often involving host cell death. Effectors escape NLR recognition through polymorphisms, allowing the pathogen to proliferate on previously resistant host plants. The powdery mildew effector AVRA13-1 is recognized by the barley NLR MLA13 and activates host cell death. We demonstrate here that a virulent form of AVRA13, called AVRA13-V2, escapes MLA13 recognition by substituting a serine for a leucine residue at the C-terminus. Counterintuitively, this substitution in AVRA13-V2 resulted in an enhanced MLA13 association and prevented the detection of AVRA13-1 by MLA13. Therefore, AVRA13-V2 is a dominant-negative form of AVRA13 and has probably contributed to the breakdown of Mla13 resistance. Despite this dominant-negative activity, AVRA13-V2 failed to suppress host cell death mediated by the MLA13 autoactive MHD variant. Neither AVRA13-1 nor AVRA13-V2 interacted with the MLA13 autoactive variant, implying that the binding moiety in MLA13 that mediates association with AVRA13-1 is altered after receptor activation. We also show that mutations in the MLA13 coiled-coil domain, which were thought to impair Ca2+ channel activity and NLR function, instead resulted in MLA13 autoactive cell death. Our results constitute an important step to define intermediate receptor conformations during NLR activation.
| S-EPMC10540733 | biostudies-literature
Project description:A large-scale parallel expression analysis was conducted to elucidate Mla-specified responses to powdery mildew infection using 22K Barley1 GeneChip probe arrays. Our goal was to identify genes differentially expressed in incompatible (resistant) vs. compatible (susceptible) and Mla-specified Rar1-dependent vs. -independent interactions. A split-split-plot design with 108 experimental units (3 replications x 2 isolates x 3 genotypes x 6 time points) was used to profile near-isogenic lines containing the Mla1, Mla6, and Mla13 resistance specificities in response to inoculation with the Blumeria graminis f. sp. hordei (Bgh) isolates 5874 (AvrMla1, AvrMla6) and K1 (AvrMla1, AvrMla13). ****[PLEXdb(http://www.plexdb.org) has submitted this series at GEO on behalf of the original contributor, Rico Caldo. The equivalent experiment is BB4 at PLEXdb.]
2011-11-22 | GSE33396 | GEO
Project description:Nucleotide-binding domain and leucine-rich repeat (NLR)-containing proteins in plants and animals mediate intracellular pathogen sensing. Plant NLRs typically detect strain-specific pathogen effectors and trigger immune responses often linked to localized host cell death. The barley Mla disease resistance locus has undergone extensive functional diversification in the host population and encodes numerous allelic NLRs each detecting a matching isolate-specific avirulence effector (AVRA) of the fungal pathogen Blumeria graminis f. sp. hordei (Bgh). We report here the isolation of Bgh AVRa7, AVRa9, AVRa10, and AVRa22, which encode small secreted proteins recognized by allelic MLA7, MLA9, MLA10, and MLA22 receptors, respectively. These effectors are sequence-unrelated, except for allelic AVRa10 and AVRa22 that are co-maintained in pathogen populations in the form of a balanced polymorphism. Contrary to numerous examples of indirect recognition of bacterial effectors by plant NLRs, co-expression experiments with matching Mla-AVRa pairs indicate direct detection of the sequence-unrelated fungal effectors by MLA receptors.
| S-EPMC6414202 | biostudies-literature
Project description:A large-scale parallel expression analysis was conducted to elucidate Mla-specified responses to powdery mildew infection using 22K Barley1 GeneChip probe arrays. Our goal was to identify genes differentially expressed in incompatible (resistant) vs. compatible (susceptible) and Mla-specified Rar1-dependent vs. -independent interactions. A split-split-plot design with 108 experimental units (3 replications x 2 isolates x 3 genotypes x 6 time points) was used to profile near-isogenic lines containing the Mla1, Mla6, and Mla13 resistance specificities in response to inoculation with the Blumeria graminis f. sp. hordei (Bgh) isolates 5874 (AvrMla1, AvrMla6) and K1 (AvrMla1, AvrMla13). ****[PLEXdb(http://www.plexdb.org) has submitted this series at GEO on behalf of the original contributor, Rico Caldo. The equivalent experiment is BB4 at PLEXdb.] genotype: CI 16137 (Mla1) - pathogen isolates: Bgh 5874 - time: 0 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh 5874 - time: 8 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh 5874 - time: 16 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh 5874 - time: 20 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh 5874 - time: 24 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh 5874 - time: 32 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh K1 - time: 0 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh K1 - time: 8 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh K1 - time: 16 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh K1 - time: 20 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh K1 - time: 24 hai(3-replications); genotype: CI 16137 (Mla1) - pathogen isolates: Bgh K1 - time: 32 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh 5874 - time: 0 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh 5874 - time: 8 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh 5874 - time: 16 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh 5874 - time: 20 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh 5874 - time: 24 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh 5874 - time: 32 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh K1 - time: 0 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh K1 - time: 8 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh K1 - time: 16 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh K1 - time: 20 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh K1 - time: 24 hai(3-replications); genotype: CI 16151 (Mla6) - pathogen isolates: Bgh K1 - time: 32 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh 5874 - time: 0 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh 5874 - time: 8 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh 5874 - time: 16 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh 5874 - time: 20 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh 5874 - time: 24 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh 5874 - time: 32 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh K1 - time: 0 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh K1 - time: 8 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh K1 - time: 16 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh K1 - time: 20 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh K1 - time: 24 hai(3-replications); genotype: CI 16155 (Mla13) - pathogen isolates: Bgh K1 - time: 32 hai(3-replications)
2011-11-22 | E-GEOD-33396 | biostudies-arrayexpress
Project description:Nucleotide-binding domain leucine-rich repeat-containing receptors (NLRs) in plants can detect avirulence (AVR) effectors of pathogenic microbes. The Mildew locus a (Mla) NLR gene has been shown to confer resistance against diverse fungal pathogens in cereal crops. In barley, Mla has undergone allelic diversification in the host population and confers isolate-specific immunity against the powdery mildew-causing fungal pathogen Blumeria graminis forma specialis hordei (Bgh). We previously isolated the Bgh effectors AVRA1, AVRA7, AVRA9, AVRA13, and allelic AVRA10/AVRA22, which are recognized by matching MLA1, MLA7, MLA9, MLA13, MLA10 and MLA22, respectively. Here, we extend our knowledge of the Bgh effector repertoire by isolating the AVRA6 effector, which belongs to the family of catalytically inactive RNase-Like Proteins expressed in Haustoria (RALPHs). Using structural prediction, we also identified RNase-like folds in AVRA1, AVRA7, AVRA10/AVRA22, and AVRA13, suggesting that allelic MLA recognition specificities could detect structurally related avirulence effectors. To better understand the mechanism underlying the recognition of effectors by MLAs, we deployed chimeric MLA1 and MLA6, as well as chimeric MLA10 and MLA22 receptors in plant co-expression assays, which showed that the recognition specificity for AVRA1 and AVRA6 as well as allelic AVRA10 and AVRA22 is largely determined by the receptors' C-terminal leucine-rich repeats (LRRs). The design of avirulence effector hybrids allowed us to identify four specific AVRA10 and five specific AVRA22 aa residues that are necessary to confer MLA10- and MLA22-specific recognition, respectively. This suggests that the MLA LRR mediates isolate-specific recognition of structurally related AVRA effectors. Thus, functional diversification of multi-allelic MLA receptors may be driven by a common structural effector scaffold, which could be facilitated by proliferation of the RALPH effector family in the pathogen genome.
| S-EPMC7857584 | biostudies-literature
Project description:Traditional treatments for bacterial infection have focused upon directly inhibiting growth of the pathogen. However, an equally important determinant of infection outcome is the host defense response. We previously performed a high-throughput chemical screen to identify small molecules that rescued the nematode Caenorhabditis elegans from infection by Pseudomonas aeruginosa. Over 20 of the hits stimulated host defense gene expression. During in-depth studies of five such molecules using microarray analysis, bioinformatic clustering, and RNAi knockdown of candidate gene targets, we identified PMK-1/p38 MAPK and SKN-1/Nrf2 as two key pathways modulated by these hits. Interestingly, the molecules studied did not depend on a single pathway for ameliorating P. aeruginosa pathogenesis in liquid-based assay, but did rely on the PMK-1/p38 MAPK pathway during a colonization-based infection assay on agar. A subset of these molecules was also protective against Enterococcus faecalis and Staphylococcus aureus. In general, the compounds showed little toxicity against mammalian cells or worms, consistent with their identification in a phenotypic, high-content screen. These molecules possess significant potential for use as tools to study innate immune processes
2020-09-19 | GSE137516 | GEO
Project description:The range of hosts that a parasite can infect in nature is a trait determined by its own evolutionary history and that of its potential hosts. However, knowledge on host range diversity and evolution at the family level is often lacking. Here, we investigate host range variation and diversification trends within the Sclerotiniaceae, a family of Ascomycete fungi. Using a phylogenetic framework, we associate diversification rates, the frequency of host jump events and host range variation during the evolution of this family. Variations in diversification rate during the evolution of the Sclerotiniaceae define three major macro-evolutionary regimes with contrasted proportions of species infecting a broad range of hosts. Host-parasite cophylogenetic analyses pointed towards parasite radiation on distant hosts long after host speciation (host jump or duplication events) as the dominant mode of association with plants in the Sclerotiniaceae. The intermediate macro-evolutionary regime showed a low diversification rate, high frequency of duplication events and the highest proportion of broad host range species. Our findings suggest that the emergence of broad host range fungal pathogens results largely from host jumps, as previously reported for oomycete parasites, probably combined with low speciation rates. These results have important implications for our understanding of fungal parasites evolution and are of particular relevance for the durable management of disease epidemics.
| S-EPMC5900718 | biostudies-literature
Project description:The interaction between the immune system and pathogens is often characterised as a predator-prey interaction. This characterisation ignores the fact that both require host resources to reproduce. Here, we propose novel theory that considers how these resource requirements can modify the interaction between the immune system and pathogens. We derive a series of models to describe the energetic interaction between the immune system and pathogens, from fully independent resources to direct competition for the same resource. We show that increasing within-host resource supply has qualitatively distinct effects under these different scenarios. In particular, we show the conditions for which pathogen load is expected to increase, decrease or even peak at intermediate resource supply. We survey the empirical literature and find evidence for all three patterns. These patterns are not explained by previous theory, suggesting that competition for host resources can have a strong influence on the outcome of disease.
| S-EPMC4264941 | biostudies-literature