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2. Global genomic analyses of wheat powdery mildew reveal association of pathogen spread with historical human migration and trade

Author

Sotiropoulos, Alexandros G., Arango-Isaza, Epifanía, Ban, Tomohiro, Barbieri, Chiara, Bourras, Salim, Cowger, Christina, Czembor, Paweł C., Ben-David, Roi, Dinoor, Amos, Ellwood, Simon R., Graf, Johannes, Hatta, Koichi, Helguera, Marcelo, Sánchez-Martín, Javier, McDonald, Bruce A., Morgounov, Alexey I., Müller, Marion C., Shamanin, Vladimir, Shimizu, Kentaro K., Yoshihira, Taiki, Zbinden, Helen, Keller, Beat, and Wicker, Thomas

Published
2022
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7. Wheat zinc finger protein TaZF interacts with both the powdery mildew AvrPm2 protein and the corresponding wheat Pm2a immune receptor

Author

Manser, Beatrice; https://orcid.org/0000-0002-7592-5089, Zbinden, Helen; https://orcid.org/0000-0001-9812-923X, Herren, Gerhard; https://orcid.org/0000-0002-3963-4815, Steger, Joel, Isaksson, Jonatan; https://orcid.org/0000-0003-3934-4241, Bräunlich, Stephanie, Wicker, Thomas; https://orcid.org/0000-0002-6777-7135, Keller, Beat; https://orcid.org/0000-0003-2379-9225, Manser, Beatrice; https://orcid.org/0000-0002-7592-5089, Zbinden, Helen; https://orcid.org/0000-0001-9812-923X, Herren, Gerhard; https://orcid.org/0000-0002-3963-4815, Steger, Joel, Isaksson, Jonatan; https://orcid.org/0000-0003-3934-4241, Bräunlich, Stephanie, Wicker, Thomas; https://orcid.org/0000-0002-6777-7135, and Keller, Beat; https://orcid.org/0000-0003-2379-9225

Abstract

Plant defense responses to pathogens are induced after direct or indirect perception of effector proteins or their activity on host proteins. In fungal-plant interactions, relatively little is known about whether, in addition to avirulence effectors and immune receptors, other proteins contribute to specific recognition. The nucleotide-binding leucine-rich repeat (NLR) immune receptor Pm2a in wheat recognizes the fungal powdery mildew effector AvrPm2. We found that the predicted wheat zinc finger TaZF interacts with both the fungal avirulence protein AvrPm2 and the wheat NLR Pm2a. We further demonstrated that the virulent AvrPm2-H2 variant does not interact with TaZF. TaZF silencing in wheat resulted in a reduction but not a loss of Pm2a-mediated powdery mildew resistance. Interaction studies showed that the leucine-rich repeat domain of Pm2a is the mediator of the interaction with TaZF. TaZF recruits both Pm2a and AvrPm2 from the cytosol to the nucleus, resulting in nuclear localization of Pm2a, TaZF, and AvrPm2 in wheat. We propose that TaZF acts as a facilitator of Pm2a-dependent AvrPm2 effector recognition. Our findings highlight the importance of identifying effector host targets for characterization of NLR-mediated effector recognition.

Published
2023

8. Global genomic analyses of wheat powdery mildew reveal association of pathogen spread with historical human migration and trade

Author

Sotiropoulos, Alexandros G, Arango-Isaza, Epifanía, Ban, Tomohiro, Barbieri, Chiara, Bourras, Salim, Cowger, Christina, Czembor, Paweł C, Ben-David, Roi, Dinoor, Amos, Ellwood, Simon R, Graf, Johannes, Hatta, Koichi, Helguera, Marcelo, Sánchez-Martín, Javier, McDonald, Bruce A, Morgounov, Alexey I, Müller, Marion C, Shamanin, Vladimir, Shimizu, Kentaro K, Yoshihira, Taiki, Zbinden, Helen, Keller, Beat, Wicker, Thomas, University of Zurich, Sotiropoulos, Alexandros G, and Wicker, Thomas

Subjects
1000 Multidisciplinary, Multidisciplinary, Human Migration, General Physics and Astronomy, 1600 General Chemistry, Genetics and Molecular Biology, Genomics, General Chemistry, Poaceae, 3100 General Physics and Astronomy, UFSP13-7 Evolution in Action: From Genomes to Ecosystems, 10127 Institute of Evolutionary Biology and Environmental Studies, 10126 Department of Plant and Microbial Biology, 1300 General Biochemistry, Genetics and Molecular Biology, General Biochemistry, Humans, 570 Life sciences, biology, 590 Animals (Zoology), 10211 Zurich-Basel Plant Science Center, Triticum, Plant Diseases
Abstract

The fungus Blumeria graminis f. sp. tritici causes wheat powdery mildew disease. Here, we study its spread and evolution by analyzing a global sample of 172 mildew genomes. Our analyses show that B.g. tritici emerged in the Fertile Crescent during wheat domestication. After it spread throughout Eurasia, colonization brought it to America, where it hybridized with unknown grass mildew species. Recent trade brought USA strains to Japan, and European strains to China. In both places, they hybridized with local ancestral strains. Thus, although mildew spreads by wind regionally, our results indicate that humans drove its global spread throughout history and that mildew rapidly evolved through hybridization.

Published
2022

9. Global genomic analyses of wheat powdery mildew reveal association of pathogen spread with historical human migration and trade

Author

Sotiropoulos, Alexandros G; https://orcid.org/0000-0002-3591-0851, Arango-Isaza, Epifanía; https://orcid.org/0000-0002-8871-7027, Ban, Tomohiro, Barbieri, Chiara; https://orcid.org/0000-0001-8827-5655, Bourras, Salim; https://orcid.org/0000-0003-0855-5433, Cowger, Christina, Czembor, Paweł C; https://orcid.org/0000-0003-2076-7586, Ben-David, Roi; https://orcid.org/0000-0003-2576-2063, Dinoor, Amos, Ellwood, Simon R; https://orcid.org/0000-0002-2673-0816, Graf, Johannes; https://orcid.org/0000-0001-5419-9842, Hatta, Koichi, Helguera, Marcelo; https://orcid.org/0000-0003-4401-8731, Sánchez-Martín, Javier; https://orcid.org/0000-0002-0284-7219, McDonald, Bruce A; https://orcid.org/0000-0002-5332-2172, Morgounov, Alexey I; https://orcid.org/0000-0001-7082-5655, Müller, Marion C; https://orcid.org/0000-0001-5594-2319, Shamanin, Vladimir, Shimizu, Kentaro K; https://orcid.org/0000-0002-6483-1781, Yoshihira, Taiki, Zbinden, Helen; https://orcid.org/0000-0001-9812-923X, Keller, Beat; https://orcid.org/0000-0003-2379-9225, Wicker, Thomas; https://orcid.org/0000-0002-6777-7135, Sotiropoulos, Alexandros G; https://orcid.org/0000-0002-3591-0851, Arango-Isaza, Epifanía; https://orcid.org/0000-0002-8871-7027, Ban, Tomohiro, Barbieri, Chiara; https://orcid.org/0000-0001-8827-5655, Bourras, Salim; https://orcid.org/0000-0003-0855-5433, Cowger, Christina, Czembor, Paweł C; https://orcid.org/0000-0003-2076-7586, Ben-David, Roi; https://orcid.org/0000-0003-2576-2063, Dinoor, Amos, Ellwood, Simon R; https://orcid.org/0000-0002-2673-0816, Graf, Johannes; https://orcid.org/0000-0001-5419-9842, Hatta, Koichi, Helguera, Marcelo; https://orcid.org/0000-0003-4401-8731, Sánchez-Martín, Javier; https://orcid.org/0000-0002-0284-7219, McDonald, Bruce A; https://orcid.org/0000-0002-5332-2172, Morgounov, Alexey I; https://orcid.org/0000-0001-7082-5655, Müller, Marion C; https://orcid.org/0000-0001-5594-2319, Shamanin, Vladimir, Shimizu, Kentaro K; https://orcid.org/0000-0002-6483-1781, Yoshihira, Taiki, Zbinden, Helen; https://orcid.org/0000-0001-9812-923X, Keller, Beat; https://orcid.org/0000-0003-2379-9225, and Wicker, Thomas; https://orcid.org/0000-0002-6777-7135

Abstract

The fungus Blumeria graminis f. sp. tritici causes wheat powdery mildew disease. Here, we study its spread and evolution by analyzing a global sample of 172 mildew genomes. Our analyses show that B.g. tritici emerged in the Fertile Crescent during wheat domestication. After it spread throughout Eurasia, colonization brought it to America, where it hybridized with unknown grass mildew species. Recent trade brought USA strains to Japan, and European strains to China. In both places, they hybridized with local ancestral strains. Thus, although mildew spreads by wind regionally, our results indicate that humans drove its global spread throughout history and that mildew rapidly evolved through hybridization.

Published
2022

10. A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat

Author

Kolodziej, Markus C; https://orcid.org/0000-0003-3155-2935, Singla, Jyoti, Sánchez-Martín, Javier; https://orcid.org/0000-0002-0284-7219, Zbinden, Helen, Šimková, Hana; https://orcid.org/0000-0003-4159-7619, Karafiátová, Miroslava; https://orcid.org/0000-0003-1177-6472, Doležel, Jaroslav; https://orcid.org/0000-0002-6263-0492, Gronnier, Julien; https://orcid.org/0000-0002-1429-0542, Poretti, Manuel; https://orcid.org/0000-0001-6915-2238, Glauser, Gaétan, Zhu, Wangsheng; https://orcid.org/0000-0001-7773-3438, Köster, Philipp; https://orcid.org/0000-0002-1359-822X, Zipfel, Cyril; https://orcid.org/0000-0003-4935-8583, Wicker, Thomas; https://orcid.org/0000-0002-6777-7135, Krattinger, Simon G; https://orcid.org/0000-0001-6912-7411, Keller, Beat; https://orcid.org/0000-0003-2379-9225, Kolodziej, Markus C; https://orcid.org/0000-0003-3155-2935, Singla, Jyoti, Sánchez-Martín, Javier; https://orcid.org/0000-0002-0284-7219, Zbinden, Helen, Šimková, Hana; https://orcid.org/0000-0003-4159-7619, Karafiátová, Miroslava; https://orcid.org/0000-0003-1177-6472, Doležel, Jaroslav; https://orcid.org/0000-0002-6263-0492, Gronnier, Julien; https://orcid.org/0000-0002-1429-0542, Poretti, Manuel; https://orcid.org/0000-0001-6915-2238, Glauser, Gaétan, Zhu, Wangsheng; https://orcid.org/0000-0001-7773-3438, Köster, Philipp; https://orcid.org/0000-0002-1359-822X, Zipfel, Cyril; https://orcid.org/0000-0003-4935-8583, Wicker, Thomas; https://orcid.org/0000-0002-6777-7135, Krattinger, Simon G; https://orcid.org/0000-0001-6912-7411, and Keller, Beat; https://orcid.org/0000-0003-2379-9225

Abstract

Plasma membrane-associated and intracellular proteins and protein complexes play a pivotal role in pathogen recognition and disease resistance signaling in plants and animals. The two predominant protein families perceiving plant pathogens are receptor-like kinases and nucleotide binding-leucine-rich repeat receptors (NLR), which often confer race-specific resistance. Leaf rust is one of the most prevalent and most devastating wheat diseases. Here, we clone the race-specific leaf rust resistance gene Lr14a from hexaploid wheat. The cloning of Lr14a is aided by the recently published genome assembly of ArinaLrFor, an Lr14a-containing wheat line. Lr14a encodes a membrane-localized protein containing twelve ankyrin (ANK) repeats and structural similarities to Ca2+-permeable non-selective cation channels. Transcriptome analyses reveal an induction of genes associated with calcium ion binding in the presence of Lr14a. Haplotype analyses indicate that Lr14a-containing chromosome segments were introgressed multiple times into the bread wheat gene pool, but we find no variation in the Lr14a coding sequence itself. Our work demonstrates the involvement of an ANK-transmembrane (TM)-like type of gene family in race-specific disease resistance in wheat. This forms the basis to explore ANK-TM-like genes in disease resistance breeding.

Published
2021

11. Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2

Author

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, University of Zurich, Keller, Beat, and Sánchez‐Martín, Javier

Subjects
0106 biological sciences, 0301 basic medicine, Aegilops, Blumeria graminis, Nicotiana benthamiana, NLR Proteins, Plant Science, Immune receptor, 580 Plants (Botany), 01 natural sciences, Epitope, UFSP13-7 Evolution in Action: From Genomes to Ecosystems, 1307 Cell Biology, Fungal Proteins, 03 medical and health sciences, Immune system, 10126 Department of Plant and Microbial Biology, 1311 Genetics, Ascomycota, 1110 Plant Science, Tobacco, Genetics, Aegilops tauschii, Plant Immunity, 10211 Zurich-Basel Plant Science Center, Amino Acids, Alleles, Triticum, Disease Resistance, Plant Diseases, Plant Proteins, 2. Zero hunger, chemistry.chemical_classification, biology, Effector, food and beverages, Genetic Variation, Cell Biology, biology.organism_classification, Amino acid, 030104 developmental biology, chemistry, Host-Pathogen Interactions, Mutation, 010606 plant biology & botany
Abstract

Plant nucleotide-binding leucine-rich repeat receptors (NLRs) act as intracellular sensors for pathogen-derived effector proteins and trigger an immune response, frequently resulting in the hypersensitive cell death response (HR) of the infected host cell. The wheat (Triticum aestivum) NLR Pm2 confers resistance against the fungal pathogen Blumeria graminis f. sp. tritici (Bgt) if the isolate contains the specific RNase-like effector AvrPm2. We identified and isolated seven new Pm2 alleles (Pm2e-i) in the wheat D-genome ancestor Aegilops tauschii and two new natural AvrPm2 haplotypes from Bgt. Upon transient co-expression in Nicotiana benthamiana, we observed a variant-specific HR of the Pm2 variants Pm2a and Pm2i towards AvrPm2 or its homolog from the AvrPm2 effector family, BgtE-5843, respectively. Through the introduction of naturally occurring non-synonymous single nucleotide polymorphisms and structure-guided mutations, we identified single amino acids in both the wheat NLR Pm2 and the fungal effector proteins AvrPm2 and BgtE-5843 responsible for the variant-specific HR of the Pm2 variants. Exchanging these amino acids led to a modified HR of the Pm2-AvrPm2 interaction and allowed the identification of the effector head epitope, a 20-amino-acid long unit of AvrPm2 involved in the HR. Swapping of the AvrPm2 head epitope to the non-HR-triggering AvrPm2 family member BgtE-5846 led to gain of a HR by Pm2a. Our study presents a molecular approach to identify crucial effector surface structures involved in the HR and demonstrates that natural and induced diversity in an immune receptor and its corresponding effectors can provide the basis for understanding and modifying NLR-effector specificity.

Published
2021

12. Wheat Pm4resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins

Author

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, and Keller, Beat

Abstract

Crop breeding for resistance to pathogens largely relies on genes encoding receptors that confer race-specific immunity. Here, we report the identification of the wheat Pm4race-specific resistance gene to powdery mildew. Pm4encodes a putative chimeric protein of a serine/threonine kinase and multiple C2 domains and transmembrane regions, a unique domain architecture among known resistance proteins. Pm4undergoes constitutive alternative splicing, generating two isoforms with different protein domain topologies that are both essential for resistance function. Both isoforms interact and localize to the endoplasmatic reticulum when co-expressed. Pm4reveals additional diversity of immune receptor architecture to be explored for breeding and suggests an endoplasmatic reticulum-based molecular mechanism of Pm4-mediated race-specific resistance.

Published
2021
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13. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species

Author

Menardo, Fabrizio, Praz, Coraline R, Wyder, Stefan, Ben-David, Roi, Bourras, Salim, Matsumae, Hiromi, McNally, Kaitlin E, Parlange, Francis, Riba, Andrea, Roffler, Stefan, Schaefer, Luisa K, Shimizu, Kentaro K; https://orcid.org/0000-0002-6483-1781, Valenti, Luca, Zbinden, Helen, Wicker, Thomas, Keller, Beat, Menardo, Fabrizio, Praz, Coraline R, Wyder, Stefan, Ben-David, Roi, Bourras, Salim, Matsumae, Hiromi, McNally, Kaitlin E, Parlange, Francis, Riba, Andrea, Roffler, Stefan, Schaefer, Luisa K, Shimizu, Kentaro K; https://orcid.org/0000-0002-6483-1781, Valenti, Luca, Zbinden, Helen, Wicker, Thomas, and Keller, Beat

Abstract

Throughout the history of agriculture, many new crop species (polyploids or artificial hybrids) have been introduced to diversify products or to increase yield. However, little is known about how these new crops influence the evolution of new pathogens and diseases. Triticale is an artificial hybrid of wheat and rye, and it was resistant to the fungal pathogen powdery mildew (Blumeria graminis) until 2001 (refs. 1,2,3). We sequenced and compared the genomes of 46 powdery mildew isolates covering several formae speciales. We found that B. graminis f. sp. triticale, which grows on triticale and wheat, is a hybrid between wheat powdery mildew (B. graminis f. sp. tritici) and mildew specialized on rye (B. graminis f. sp. secalis). Our data show that the hybrid of the two mildews specialized on two different hosts can infect the hybrid plant species originating from those two hosts. We conclude that hybridization between mildews specialized on different species is a mechanism of adaptation to new crops introduced by agriculture.

Published
2016

14. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species

Author

Menardo, Fabrizio, primary, Praz, Coraline R, additional, Wyder, Stefan, additional, Ben-David, Roi, additional, Bourras, Salim, additional, Matsumae, Hiromi, additional, McNally, Kaitlin E, additional, Parlange, Francis, additional, Riba, Andrea, additional, Roffler, Stefan, additional, Schaefer, Luisa K, additional, Shimizu, Kentaro K, additional, Valenti, Luca, additional, Zbinden, Helen, additional, Wicker, Thomas, additional, and Keller, Beat, additional

Published
2016
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