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

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 resi...

Full description

Bibliographic Details
Main Authors: Isabel ML Saur, Saskia Bauer, Barbara Kracher, Xunli Lu, Lamprinos Franzeskakis, Marion C Müller, Björn Sabelleck, Florian Kümmel, Ralph Panstruga, Takaki Maekawa, Paul Schulze-Lefert
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/44471
_version_ 1811253029685428224
author Isabel ML Saur
Saskia Bauer
Barbara Kracher
Xunli Lu
Lamprinos Franzeskakis
Marion C Müller
Björn Sabelleck
Florian Kümmel
Ralph Panstruga
Takaki Maekawa
Paul Schulze-Lefert
author_facet Isabel ML Saur
Saskia Bauer
Barbara Kracher
Xunli Lu
Lamprinos Franzeskakis
Marion C Müller
Björn Sabelleck
Florian Kümmel
Ralph Panstruga
Takaki Maekawa
Paul Schulze-Lefert
author_sort Isabel ML Saur
collection DOAJ
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.
first_indexed 2024-04-12T16:44:34Z
format Article
id doaj.art-c130121c7d494603a609479323d359e0
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T16:44:34Z
publishDate 2019-02-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-c130121c7d494603a609479323d359e02022-12-22T03:24:39ZengeLife Sciences Publications LtdeLife2050-084X2019-02-01810.7554/eLife.44471Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanismIsabel ML Saur0https://orcid.org/0000-0002-5610-1260Saskia Bauer1https://orcid.org/0000-0003-4559-5063Barbara Kracher2Xunli Lu3Lamprinos Franzeskakis4Marion C Müller5https://orcid.org/0000-0001-5594-2319Björn Sabelleck6Florian Kümmel7Ralph Panstruga8https://orcid.org/0000-0002-3756-8957Takaki Maekawa9Paul Schulze-Lefert10https://orcid.org/0000-0002-8978-1717Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, GermanyDepartment of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, GermanyDepartment of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, GermanyDepartment of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, GermanyUnit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Aachen, GermanyDepartment of Plant and Microbial Biology, University of Zurich, Zurich, SwitzerlandUnit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Aachen, GermanyUnit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Aachen, GermanyUnit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Aachen, GermanyDepartment of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, GermanyDepartment of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Cluster of Excellence on Plant Sciences, Düsseldorf, GermanyNucleotide-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.https://elifesciences.org/articles/44471plant innate immunityNLR receptoravirulence effectorpowdery mildewpathogen population
spellingShingle Isabel ML Saur
Saskia Bauer
Barbara Kracher
Xunli Lu
Lamprinos Franzeskakis
Marion C Müller
Björn Sabelleck
Florian Kümmel
Ralph Panstruga
Takaki Maekawa
Paul Schulze-Lefert
Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
eLife
plant innate immunity
NLR receptor
avirulence effector
powdery mildew
pathogen population
title Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
title_full Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
title_fullStr Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
title_full_unstemmed Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
title_short Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism
title_sort multiple pairs of allelic mla immune receptor powdery mildew avra effectors argue for a direct recognition mechanism
topic plant innate immunity
NLR receptor
avirulence effector
powdery mildew
pathogen population
url https://elifesciences.org/articles/44471
work_keys_str_mv AT isabelmlsaur multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT saskiabauer multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT barbarakracher multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT xunlilu multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT lamprinosfranzeskakis multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT marioncmuller multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT bjornsabelleck multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT floriankummel multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT ralphpanstruga multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT takakimaekawa multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism
AT paulschulzelefert multiplepairsofallelicmlaimmunereceptorpowderymildewavraeffectorsargueforadirectrecognitionmechanism