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Molecular analysis of disease resistance specificity in cereals

English title Molecular analysis of disease resistance specificity in cereals
Applicant Keller Beat
Number 182833
Funding scheme Project funding (Div. I-III)
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Molecular Biology
Start/End 01.01.2019 - 31.12.2021
Approved amount 948'512.00
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Keywords (6)

Wheat; host-pathogen interactions; Powdery mildew; host specificity; Leaf rust; resistance gene

Lay Summary (German)

Lead
Pflanzen werden von einer Vielzahl von Krankheitserregern befallen. Die Züchtung von Nutzpflanzen hat im Verlauf der letzten hundert Jahre zur Entdeckung von natürlicherweise vorkommender Resistenz gegen Pathogene geführt. Die Funktionsweisen dieser Resistenzen sind auf molekularer Ebene noch wenig verstanden. Das Projekt widmet sich der Frage, wie Pflanzen auf molekularer Ebene die Anwesenheit von pilzlichen Pathogenen (z.B. dem Weizenmehltau) erkennen können, und wie dadurch Abwehrreaktionen ausgelöst werden.
Lay summary

Wir haben in den letzten Jahren in Weizen und Mais drei molekular sehr unterschiedliche Resistenzmechanismen gegen pilzliche Krankheitserreger entdeckt. Dabei handelt es sich um Abwehrstrategien, die entweder spezifische Moleküle der mikrobiellen Invasoren entdecken können, oder aber den Stoffwechsel der Pflanze so verändern, dass die Pathogene entweder gar mehr wachsen können, oder zumindest in ihrer Vermehrung stark eingeschränkt sind.

Das vorliegende Projekt soll zum Verständis der Erkennungsmechanismen von Krankheitserregern durch eine Reihe von pflanzliche Immunrezeptoren beitragen. Dabei stehen Pilzpathogene wie z.B. Mehltau und Braunrost bei Weizen im Vordergrund. Die Immunrezeptoren stammen aus Weizen oder Mais und gehören zu ganz unterschiedlichen Proteinklassen. Basierend auf diesen verschiedenen Typen von Rezeptoren wollen wir verstehen, wie die biochemische Erkennung auf Proteinebene stattfindet, welche Strukturen auf Pathogen- wie auf Wirtsseite für die spezifische Erkennung verantwortlich sind, und schliesslich wie diese Erkennung zur einer Abwehrantwort der Pflanze führt  Zudem wollen wir Wege finden, wie diese Erkenntnisse für die praktisch Pflanzenzüchtung nutzbar gemacht werden können.

Das Projekt beschäftigt sich mit der biologischen Funktionsweise von Krankheitsresistenz bei Getreidepflanzen und leistet einen Beitrag zu einer sehr dynamischen, global relevanten Forschungsrichtung. Da Pflanzenkrankheiten und ihre Bekämpfung ökonomisch wie ökologisch von grosser Bedeutung sind, steht diese Forschungsrichtung auch im Brennpunkt gesellschaftlicher Aufmerksamkeit.

Direct link to Lay Summary Last update: 30.11.2018

Responsible applicant and co-applicants

Employees

Publications

Publication
A highly differentiated region of wheat chromosome 7AL encodes a Pm1a immune receptor that recognizes its corresponding AvrPm1a effector from Blumeria graminis
Hewitt Tim, Müller Marion C., Molnár István, Mascher Martin, Holušová Kateřina, Šimková Hana, Kunz Lukas, Zhang Jianping, Li Jianbo, Bhatt Dhara, Sharma Raghvendra, Schudel Seraina, Yu Guotai, Steuernagel Burkhard, Periyannan Sambasivam, Wulff Brande, Ayliffe Mick, McIntosh Robert, Keller Beat, Lagudah Evans, Zhang Peng (2021), A highly differentiated region of wheat chromosome 7AL encodes a Pm1a immune receptor that recognizes its corresponding AvrPm1a effector from Blumeria graminis, in New Phytologist, 229(5), 2812-2826.
A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat
Kolodziej Markus C., Singla Jyoti, Sánchez-Martín Javier, Zbinden Helen, Šimková Hana, Karafiátová Miroslava, Doležel Jaroslav, Gronnier Julien, Poretti Manuel, Glauser Gaétan, Zhu Wangsheng, Köster Philipp, Zipfel Cyril, Wicker Thomas, Krattinger Simon G., Keller Beat (2021), A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat, in Nature Communications, 12(1), 1-12.
Alleles of a wall-associated kinase gene account for three of the major northern corn leaf blight resistance loci in maize
Yang Ping, Scheuermann Daniela, Kessel Bettina, Koller Teresa, Greenwood Julian R., Hurni Severine, Herren Gerhard, Zhou Shenghui, Marande William, Wicker Thomas, Krattinger Simon G., Ouzunova Milena, Keller Beat (2021), Alleles of a wall-associated kinase gene account for three of the major northern corn leaf blight resistance loci in maize, in The Plant Journal, 106(2), 526-535.
Expression of the wheat disease resistance gene Lr34 in transgenic barley leads to accumulation of abscisic acid at the leaf tip
Bräunlich Stephanie, Koller Teresa, Glauser Gaétan, Krattinger Simon G., Keller Beat (2021), Expression of the wheat disease resistance gene Lr34 in transgenic barley leads to accumulation of abscisic acid at the leaf tip, in Plant Physiology and Biochemistry, 166, 950-957.
Host Adaptation Through Hybridization: Genome Analysis of Triticale Powdery Mildew Reveals Unique Combination of Lineage-Specific Effectors
Müller Marion C., Kunz Lukas, Graf Johannes, Schudel Seraina, Keller Beat (2021), Host Adaptation Through Hybridization: Genome Analysis of Triticale Powdery Mildew Reveals Unique Combination of Lineage-Specific Effectors, in Molecular Plant-Microbe Interactions, XX(Xx), 1-8.
Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2
Manser Beatrice, Koller Teresa, Praz Coraline Rosalie, Roulin Anne C., Zbinden Helen, Arora Sanu, Steuernagel Burkhard, Wulff Brande B.H., Keller Beat, Sánchez-Martín Javier (2021), Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2, in The Plant Journal, 106(4), 993-1007.
NLR immune receptors and diverse types of non-NLR proteins control race-specific resistance in Triticeae
Sánchez-Martín Javier, Keller Beat (2021), NLR immune receptors and diverse types of non-NLR proteins control race-specific resistance in Triticeae, in Current Opinion in Plant Biology, 62, 1-10.
Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement
Gaurav Kumar, Arora Sanu, Silva Paula, Sánchez-Martín Javier, Horsnell Richard, Gao Liangliang, Brar Gurcharn S., Widrig Victoria, John Raupp W., Singh Narinder, Wu Shuangye, Kale Sandip M., Chinoy Catherine, Nicholson Paul, Quiroz-Chávez Jesús, Simmonds James, Hayta Sadiye, Smedley Mark A., Harwood Wendy, Pearce Suzannah, Gilbert David, Kangara Ngonidzashe, Gardener Catherine, Forner-Martínez Macarena, Liu Jiaqian, Yu Guotai, Boden Scott A., Pascucci Attilio, Ghosh Sreya, Hafeez Amber N., O'Hara Tom, Waites Joshua, Cheema Jitender, Steuernagel Burkhard, Patpour Mehran, Justesen Annemarie Fejer, Liu Shuyu, Rudd Jackie C., Avni Raz, Sharon Amir, Steiner Barbara, Kirana Rizky Pasthika, Buerstmayr Hermann, Mehrabi Ali A., Nasyrova Firuza Y., Chayut Noam, Matny Oadi, Steffenson Brian J., Sandhu Nitika, Chhuneja Parveen, Lagudah Evans, Elkot Ahmed F., Tyrrell Simon, Bian Xingdong, Davey Robert P., Simonsen Martin, Schauser Leif, Tiwari Vijay K., Randy Kutcher H., Hucl Pierre, Li Aili, Liu Deng Cai, Mao Long, Xu Steven, Brown-Guedira Gina, Faris Justin, Dvorak Jan, Luo Ming Cheng, Krasileva Ksenia, Lux Thomas, Artmeier Susanne, Mayer Klaus F.X., Uauy Cristobal, Mascher Martin, Bentley Alison R., Keller Beat, Poland Jesse, Wulff Brande B.H. (2021), Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement, in Nature Biotechnology, 1-27.
Standing genetic variation of the AvrPm17 avirulence gene in powdery mildew limits the effectiveness of an introgressed rye resistance gene in wheat
Mueller Marion C., Kunz Lukas, Schudel Seraina, Kammerecker Sandrine, Isaksson Jonatan, Wyler Michele, Graf Johannes, Sotiropoulos Alexandros G., Praz Coraline R., Wicker Thomas, Bourras Salim, Keller Beat (2021), Standing genetic variation of the AvrPm17 avirulence gene in powdery mildew limits the effectiveness of an introgressed rye resistance gene in wheat, in bioRxiv, 1-26.
Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins
Sánchez-Martín Javier, Widrig Victoria, Herren Gerhard, Wicker Thomas, Zbinden Helen, Gronnier Julien, Spörri Laurin, Praz Coraline R., Heuberger Matthias, Kolodziej Markus C., Isaksson Jonatan, Steuernagel Burkhard, Karafiátová Miroslava, Doležel Jaroslav, Zipfel Cyril, Keller Beat (2021), Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins, in Nature Plants, 7(3), 327-341.
The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat
Bourras Salim, Kunz Lukas, Xue Minfeng, Praz Coraline Rosalie, Müller Marion Claudia, Kälin Carol, Schläfli Michael, Ackermann Patrick, Flückiger Simon, Parlange Francis, Menardo Fabrizio, Schaefer Luisa Katharina, Ben-David Roi, Roffler Stefan, Oberhaensli Simone, Widrig Victoria, Lindner Stefan, Isaksson Jonatan, Wicker Thomas, Yu Dazhao, Keller Beat (2019), The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat, in Nature Communications, 10(1), 1-16.

Collaboration

Group / person Country
Types of collaboration
Dr. Simon Krattinger, KAUST Saudi Arabia (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Dr. Ralph Panstruga, Aachen Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Dr. Curtis Pozniak Canada (North America)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Ping Yang, Chinese Academy of Agricultural Sciences China (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Dazhao Yu China (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Cyril Zipfel Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Dr. Jaroslav Dolezel Czech Republic (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Pietro Spanu, Imperial College Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Dr. Brande Wulff Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Dr. Evans Lagudah, CSIRO Australia (Oceania)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
University of Kyoto - University of Zürich Workshop in Plant Science 2021 Talk given at a conference Molecular diversity in the resistance interactions of wheat and its fungal pathogens 13.12.2021 online, Japan Keller Beat;
Zurich-Basel Plant Science Center Symposium 2021 - Patterns in Nature and Plant Sciences Poster Unravelling the molecular basis of wheat powdery mildew virulence patterns through ultraviolet mutagenesis 08.12.2021 Online (ETH Zurich), Switzerland Bernasconi Zoe;
Nanjing Agricultural University, Zoom Symposium: The new era of wheat genomics. Invited speaker Talk given at a conference Molecular diversity in the resistance interactions of wheat and its fungal pathogens 04.12.2021 online, China Keller Beat;
Invited Institute Seminar. University of Maryland, College of Agriculture and Natural Resources, Department of Plant Science and Landscape Architecture, Fall 2021 PSLA Lecture Series Individual talk Molecular diversity in the resistance interactions of wheat and its fungal pathogens 18.10.2021 online, United States of America Keller Beat;
Jubiläumskonferenz 30 Jahre Verein Forschung für Leben: Nutzung von Gene Editing bei Pflanzen, Tier und Mensch für die Medizin und Landwirtschaft von morgen Talk given at a conference Gene Editing als Schlüsseltechnologie für eine nachhaltige Landwirtschaft 23.09.2021 Zürich, Switzerland Keller Beat;
8. Fachtagung Dialog Grün. De-novo-Domestikation - Erforschung und Erschliessung pflanzengenetischer Resourcen. Zurich-Basel Plant Science Center PSC Talk given at a conference Die Vielfalt von Weizen beruht auf der Ueberschreitung von Artgrenzen: die Rolle von Wildgräsern und verwandten Kulturpflanzen in gegenwärtiger und zukünftiger Züchtung 03.06.2021 online, Switzerland Keller Beat;
Web symposium on Plant Health, Keynote Speaker of the Italian Society of Agricultural Genetics Talk given at a conference Genetic and genomic approaches to improve disease resistance 16.12.2020 online, Italy Keller Beat;
Borlaug Global Rust Initiative Workshop, Invited Speaker Talk given at a conference Use of a high-quality wheat genome assembly allows cloning of a novel non-NLR leaf rust resistance gene 07.10.2020 online, Great Britain and Northern Ireland Keller Beat;
8th Plant genomics and gene editing congress, Europe Talk given at a conference Advances in wheat genomics: implications for powdery mildew and rust disease control 05.03.2020 Rotterdam, Netherlands Keller Beat;
Plant and Animal Genome Meeting 2020 Talk given at a conference Use of a high quality wheat genome assembly allows cloning of a novel non NLR leaf rust resistance gene 12.01.2020 San Diego, United States of America Kolodziej Markus; Keller Beat;
Plant Science Center Symposium Poster The wheat disease resistance gene Lr34 alters the distribution of abscisic acid 11.12.2019 Zürich, Switzerland Bräunlich Stephanie;
International Symposium on Advances in Phytopathology Talk given at a conference Molecular determinants of host specialization in grass powdery mildews 04.11.2019 IPK Leibniz Institute, Gatersleben, Germany Keller Beat;
Invited Institute Seminar Individual talk Molecular determinants of host specialization in grass powdery mildews 24.10.2019 University of Sydney, Cobbitty, Plant Breeding Institute, Australia Keller Beat;
Invited institute seminar Individual talk Molecular determinants of host specialization in grass powdery mildews 22.10.2019 CSIRO Canberra, Australia Keller Beat;
Host-microbe Genomics meeting Talk given at a conference Identification and validation of a qualitative seedling stage leaf rust resistance gene in wheat 24.09.2019 Zürich, Switzerland Kolodziej Markus;
International Society for Molecular Plant-Microbe Interactions Congress (IS-MPMI) Talk given at a conference Dissecting the molecular basis of the cell death response of new allelic wheat NLR PM2 variants to powdery mildew effectors 15.07.2019 Scottish Event Campus, Glasgow, Great Britain and Northern Ireland Manser Beatrice Verena;
XVIII Congress of the International Society of Molecular Plant Microbe Interactions, Session Host - microbe co-evolution Talk given at a conference Molecular determinants of host specialization in grass powdery mildews 14.07.2019 Glasgow, Great Britain and Northern Ireland Keller Beat;
Powdery mildew satellite symposium Poster Unravelling the molecular basis of the cell death response of new allelic wheat NLR PM2 variants to powdery mildew effectors 14.07.2019 Scottish Event Campus, Glasgow, Great Britain and Northern Ireland Manser Beatrice Verena;
VII Congress of Vavilov Society of Geneticists and Breeder (VSG&B), International Conference "Breads of the future: genomics, genetics, breeding, 125 years of Federal research center VIR" Talk given at a conference Molecular analysis of function and diversity of wheat disease resistance in the age of (pan-) genomics 20.06.2019 St. Petersburg, Vavilov Institute, Russia Keller Beat;
1st International Forum on Crop Science, Green crops for sustainable agriculture Talk given at a conference Molecular analysis of wheat -fungal pathogen interactions in the age of (pan-) genomics 03.06.2019 Huazhong Agricultural University, Wuhan, China Keller Beat;
Institute Seminar Academia Sinica Taiwan Individual talk Substrate of the ABC transporter encoded by the wheat disease resistance gene Lr34 23.05.2019 Taipeh, Taiwan Bräunlich Stephanie;
XXVII Plant and Animal Genome Conference PAG 2019 Talk given at a conference Evolution of novelty in wheat disease resistance occurs at very different time scales 17.01.2019 San Diego , United States of America Keller Beat;


Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
Neue Züchtungsmethoden in der Pflanzenzüchtung - was bringen diese der Schweiz? Vorstand Berner Bauernverband Talk 17.05.2021 online, Switzerland Keller Beat;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions Pizza, Philosophy and Science im Park: Gentechnisch veränderte Pflanzen, organisiert durch reatch German-speaking Switzerland 2021

Awards

Title Year
Poster Award of the Zurich-Basel Plant Science Center Symposium 2021 (for the poster "Unravelling the molecular basis of wheat powdery mildew virulence patterns through ultraviolet mutagenesis") 2021

Associated projects

Number Title Start Funding scheme
192526 Field studies of transgenic cereal crops containing heterologous, modified or combined resistance genes against fungal pathogens 01.04.2020 Project funding (Div. I-III)
163260 Molecular analysis of three different types of fungal disease resistance mechanisms in cereals 01.01.2016 Project funding (Div. I-III)
204165 Functional analysis of host-specific disease resistance in wheat 01.01.2022 Project funding (Div. I-III)
160877 Improvement of broad-spectrum disease resistance in rice: how a comprehensive study of natural rice diversity can help to reduce crop losses in developing countries 01.08.2016 r4d (Swiss Programme for Research on Global Issues for Development)

Abstract

The focus of our work is on the molecular determinants of resistance interactions between the wheat (Triticum aestivum) host plant and the obligate biotrophic, fungal pathogens powdery mildew (Blumeria graminis, Bgt) and leaf rust. In the last three years, the genomic tools both for wheat and its pathogens (particularly powdery mildew) have been greatly improved, allowing efficient map-based cloning of genes as well as genome-wide association studies (GWAS). The new resources have allowed us to identify the first avirulence as well as avirulence suppressor genes from powdery mildew three years ago (AvrPm3a2f2, SvrPm3). This work on the pathogen side was complemented by the development of more efficient approaches for resistance gene isolation from wheat, e.g. MutChromSeq which was used for the identification of the Pm2 mildew resistance gene. In the last two years we have isolated a number of novel molecular determinants of the race-specific resistance interaction of mildew and wheat. The AvrPm2, AvrPm3b2c2, AvrPm3d and AvrPm17 genes specifically recognized by the immune receptors Pm2, Pm3b, Pm3c, Pm3d and Pm17, respectively, have been identified and found to encode small effector-like proteins. Each of them belongs to a gene family with close relatives that are not recognized by the respective immune receptor. On the host side we have recently isolated genes for two new immune receptors. In wheat, at total of 77 Pm (powdery mildew resistance) genes/alleles have been genetically described at 53 loci. Each of them confers resistance to a specific set of mildew isolates. In the past, we have cloned a number of these genes which encode immune receptors, and we want to understand the immune network of host and pathogen factors contributing to agricultural resistance which is highly diverse and specific, depending on host-genotype and pathogen race. Thus, the overall goal of the first proposal part is to understand the molecular basis of disease resistance specificity in the agriculturally important wheat-mildew pathosystem. This will help to understand the evolution of pathogen adaptation as well as contribute to strategies for improved resistance gene management in plant breeding. We will analyze the interactions at the molecular level in a transient system to identify by mutagenesis the AVR and host protein domains involved in resistance. Furthermore, we will perform domain swaps between active AVR proteins and the highly similar proteins encoded by closely related gene family members which exist for all our cloned AVR genes. Such domain swaps will give further insight into the protein recognition surfaces and the sub-domains involved in the recognition. We will also study these interactions at the biochemical level, using yeast-2-hybrid systems, co-immunoprecipitation experiments, bimolecular fluorescence complementation assays and a split-LUC complementation assay. At the protein structural level, we want to purify some of the AVR proteins for protein structure determination. As these proteins have relatively small sizes of around 100 amino acids, structure determinations should be feasible once crystals are obtained. Structural information will then be combined with functional and biochemical studies. This should result in a detailed mechanistic understanding of the specificity of the interactions. Finally, we will continue our genetic approaches on both the host and the pathogen to identify novel factors involved in the determination of specificity of interactions within one host as well as of adaptation to new host species. Building on ongoing work, we will perform a molecular analysis of wheat Lr34 and maize Htn1 gene functions which are both contributing to quantitative disease resistance against fungal diseases in cereals. We want to study allelic and functional diversity of the maize Htn1 resistance gene and possibly related genes. Furthermore, the durable, quantitatively acting wheat resistance gene Lr34 will be functionally analyzed in heterologous cereal species such as barley, rice and maize for its role in conferring a unique, partial resistance phenotype. The work should also allow us to generate hypotheses on additional components involved in durable pathogen resistance.
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