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The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold.

ABSTRACT: 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.

SUBMITTER: Bauer S

PROVIDER: S-EPMC7857584 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold.

Bauer Saskia S Yu Dongli D Lawson Aaron W AW Saur Isabel M L IML Frantzeskakis Lamprinos L Kracher Barbara B Logemann Elke E Chai Jijie J Maekawa Takaki T Schulze-Lefert Paul P

PLoS pathogens 20210203 2

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 isolate ...[more]

PMID: 33534797

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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

The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold.

Publications

The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold.

Similar Datasets

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