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Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism.

ABSTRACT: 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.

SUBMITTER: Saur IM

PROVIDER: S-EPMC6414202 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism.

Saur Isabel Ml IM Bauer Saskia S Kracher Barbara B Lu Xunli X Franzeskakis Lamprinos L Müller Marion C MC Sabelleck Björn B Kümmel Florian F Panstruga Ralph R Maekawa Takaki T Schulze-Lefert Paul P

eLife 20190219

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 (AVR ...[more]

PMID: 30777147

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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.

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)

Project description:Grass powdery mildew (Blumeria graminis, Ascomycota) is a major pathogen of cereal crops and has become a model organism for obligate biotrophic fungal pathogens of plants. The sequenced genomes of two formae speciales (ff.spp.), B.g. hordei and B.g. tritici (pathogens of barley and wheat), were found to be enriched in candidate effector genes (CEGs). Similar to other filamentous pathogens, CEGs in B. graminis are under positive selection. Additionally, effectors are more likely to have presence-absence polymorphisms than other genes among different strains.Here we identified effectors in the genomes of three additional host-specific lineages of B. graminis (B.g. poae, B.g. avenae and B.g. infecting Lolium) which diverged between 24 and 5 million years ago (Mya). We found that most CEGs in B. graminis are clustered in families and that most families are present in both reference genomes (B.g. hordei and B.g. tritici) and in the genomes of all three newly annotated lineages. We identified conserved protein domains including a novel lipid binding domain. The phylogenetic analysis showed that frequent gene duplications and losses shaped the diversity of the effector repertoires of the different lineages through their evolutionary history. We observed several lineage-specific expansions where large clades of CEGs originated in only one lineage from a single gene through repeated gene duplications. When we applied a birth-death model we found that the turnover rate (the rate at which genes are deleted and duplicated) of CEG families is much higher than for non-CEG families. The analysis of genomic context revealed that the immediate surroundings of CEGs are enriched in transposable elements (TE) which could play a role in the duplication and deletion of CEGs.The CEG repertoires of related pathogens diverged dramatically in short evolutionary times because of rapid turnover and of positive selection fixing non-synonymous mutations. While signatures of positive selection on effector sequences are the expected outcome of the evolutionary "arms race" between pathogen and plant immune system, it is more difficult to infer the mechanisms and evolutionary forces that maintained an extreme turnover rate in CEG families of B. graminis for several millions of years.

Dataset Information

Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism.

Publications

Multiple pairs of allelic MLA immune receptor-powdery mildew AVR<sub>A</sub> effectors argue for a direct recognition mechanism.

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