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; Yu, Dongli; Lawson, Aaron W.; Saur, Isabel L.; Frantzeskakis, Lamprinos; Kracher, Barbara; Logemann, Elke; Chai, Jijie; Maekawa, Takaki; Schulze-Lefert, Paul

doi:10.1371/journal.ppat.1009223

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

Journal Article · Wed Feb 03 00:00:00 EST 2021 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1009223· OSTI ID:1904138

^[1]; Yu, Dongli ^[2]; Lawson, Aaron W. ^[3]; ^[3]; ^[4]; Kracher, Barbara ^[3]; ^[3]; Chai, Jijie ^[5]; Maekawa, Takaki ^[3]; Schulze-Lefert, Paul ^[3]

Max Planck Institute for Plant Breeding Research, Cologne (Germany); OSTI
Max Planck Institute for Plant Breeding Research, Cologne (Germany); University of Cologne (Germany)
Max Planck Institute for Plant Breeding Research, Cologne (Germany)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
University of Cologne (Germany). Max Planck Institute for Plant Breeding Research; Cluster of Excellence on Plant Sciences, Dusseldorf (Germany)

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 AVR_A1, AVR_A7, AVR_A9, AVR_A13, and allelic AVR_A10/AVR_A22, 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 AVR_A6 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 AVR_A1, AVR_A7, AVR_A10/AVR_A22, and AVR_A13, 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 AVR_A1 and AVR_A6 as well as allelic AVR_A10 and AVR_A22 is largely determined by the receptors’ C-terminal leucine-rich repeats (LRRs). The design of avirulence effector hybrids allowed us to identify four specific AVR_A10 and five specific AVR_A22 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 AVR_A 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.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Daimler and Benz Foundation; German Research Foundation (DFG); Horizon 2020; Max Planck Society; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1904138

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 2 Vol. 17; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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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

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