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

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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 (AVR_A) of the fungal pathogen Blumeria graminis f. sp. hordei (Bgh). We report here the isolation of Bgh AVR_a7, AVR_a9, AVR_a10,and AVR_a22, which encode small secreted proteins recognized by allelic MLA7, MLA9, MLA10, and MLA22 receptors, respectively. These effectors are sequence-unrelated, except for allelic AVR_a10and AVR_a22 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-AVR_a pairs indicate direct detection of the sequence-unrelated fungal effectors by MLA receptors.

Data availability

RNA sequencing data have been deposited in GEO under accession code GSE110266 and improved Blumeria graminis f.sp. hordei isolate K1 assembly is deposited under the accession number PRJEB30373 at EBI-ENA. All data generated or analysed during this study are included in the manuscript and supporting files.

The following data sets were generated

1. Saur IML
2. Bauer S
3. Kracher B
4. Lu X
5. Franzeskakis L
6. Müller MC
7. Sabellack B
8. Kümmel F
9. Panstruga R
10. Maekawa T
11. Schulze-Lefert P
(2018) Identification of the AVRa7,AVRa9, AVRa10 and AVRa22 effector genes from barley powdery mildew fungus (Bgh) association analysis between transcript polymorphisms and AVRa phenotypes from 27 Bgh isolates
NCBI Gene Expression Omnibus, GSE110266.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE110266
1. Saur IML
2. Bauer S
3. Kracher B
4. Lu X
5. Franzeskakis L
6. Müller MC
7. Sabellack B
8. Kümmel F
9. Panstruga R
10. Maekawa T
11. Schulze-Lefert P
(2019) Improved Blumeria graminis f.sp. hordei isolate K1 assembly
European Nucleotide Archive, PRJEB30373.

https://www.ebi.ac.uk/ena

The following previously published data sets were used

1. Lu X
2. Kracher B
3. Saur IML
4. Bauer S
5. Ellwood S
6. Wise R
7. Yaeno T
8. Maekawa T
9. Schulze-Lefert P
(2016) Identification of avirulence genes in the barley powdery mildew fungus (Bgh) by RNA-sequencing and transcriptome-wide association analysis on a set of Bgh isolates
NCBI Gene Expression Omnibus, GSE83237.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?link_type=NCBIGEO&access_num=GSE83237&acc=GSE83237

Article and author information

Author details

Isabel ML Saur

Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

Competing interests
The authors declare that no competing interests exist.
Saskia Bauer

Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4559-5063
Barbara Kracher

Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

Competing interests
The authors declare that no competing interests exist.
Xunli Lu

Department of Plant Pathology, China Agricultural University, Beijing, China

Competing interests
The authors declare that no competing interests exist.
Lamprinos Franzeskakis

Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany

Competing interests
The authors declare that no competing interests exist.
Marion C Müller

Department of Plant and Microbial Biology, University of Zurich, Zürich, Switzerland

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5594-2319
Björn Sabelleck

Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany

Competing interests
The authors declare that no competing interests exist.
Florian Kümmel

Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany

Competing interests
The authors declare that no competing interests exist.
Ralph Panstruga

Institute for Biology I, Unit of Plant Molecular Cell Biology, RWTH Aachen University, Aachen, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3756-8957
Takaki Maekawa

Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

Competing interests
The authors declare that no competing interests exist.
Paul Schulze-Lefert

Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

For correspondence
schlef@mpipz.mpg.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8978-1717

Funding

Deutsche Forschungsgemeinschaft (SFB670)

Barbara Kracher
Takaki Maekawa
Paul Schulze-Lefert

Max-Planck-Gesellschaft (Open-access funding)

Saskia Bauer
Paul Schulze-Lefert

European Molecular Biology Organization (ALTF 368-2016)

Isabel ML Saur

Cluster of Excellence in Plant Sciences (CEPLAS)

Paul Schulze-Lefert

Deutsche Forschungsgemeinschaft (SPP1819)

Lamprinos Franzeskakis
Ralph Panstruga

Daimler und Benz Stiftung

Isabel ML Saur

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.