Nucleotide-binding leucine-rich repeat (NLR) disease resistance genes typically confer resistance against races of a single pathogen. Here, we report that Yr87/Lr85, an NLR gene from Aegilops sharonensis and Aegilops longissima, confers resistance against both P. striiformis tritici (Pst) and Puccinia triticina (Pt) that cause stripe and leaf rust, respectively. Yr87/Lr85 confers resistance against Pst and Pt in wheat introgression as well as transgenic lines. Comparative analysis of Yr87/Lr85 and the cloned Triticeae NLR disease resistance genes shows that Yr87/Lr85 contains two distinct LRR domains and that the gene is only found in Ae. sharonensis and Ae. longissima. Allele mining and phylogenetic analysis indicate multiple events of Yr87/Lr85 gene flow between the two species and presence/absence variation explaining the majority of resistance to wheat leaf rust in both species. The confinement of Yr87/Lr85 to Ae. sharonensis and Ae. longissima and the resistance in wheat against Pst and Pt highlight the potential of these species as valuable sources of disease resistance genes for wheat improvement.

Agricultural Institute Centre for Agricultural Research ELKH Martonvásár Hungary

Blades Evanston IL USA

Departamento de Biología Molecular Universidad de León León Spain

Department of Agronomy and Plant Genetics University of Minnesota St Paul MN USA

Department of Plant Pathology University of Minnesota St Paul MN USA

Field Crops Research Institute Agricultural Research Centre Cairo Egypt

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig Germany

Institute of Evolution University of Haifa Haifa Israel

Institute of Experimental Botany of the Czech Academy of Sciences Centre of Plant Structural and Functional Genomics Olomouc Czechia

John Innes Centre Norwich Research Park Norwich UK

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Seeland Germany

Plant Science Program Biological and Environmental Science and Engineering Division Thuwal Saudi Arabia

School of Plant Sciences and Food Security Tel Aviv University Tel Aviv Israel

The Institute for Cereal Crops Research Tel Aviv University Tel Aviv Israel

The Sainsbury Laboratory Norwich Research Park Norwich UK

USDA ARS Cereal Disease Laboratory University of Minnesota St Paul MN USA

USDA ARS Western Regional Research Center Crop Improvement and Genetics Research Unit Albany CA USA

Zobrazit více v PubMed

Khan, M. H., Bukhari, A., Dar, Z. A. & Rizvi, S. M. Status and strategies in breeding for rust resistance in wheat.

Savary, S. et al. The global burden of pathogens and pests on major food crops. PubMed DOI

Periyannan, S., Milne, R. J., Figueroa, M., Lagudah, E. S. & Dodds, P. N. An overview of genetic rust resistance: From broad to specific mechanisms. PubMed DOI PMC

Dinh, H. X., Singh, D., Periyannan, S., Park, R. F. & Pourkheirandish, M. Molecular genetics of leaf rust resistance in wheat and barley. PubMed DOI

Ali, S. et al. Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici. PubMed DOI PMC

Hovmøller, M. S. et al. Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. DOI

McDonald, B. A. & Stukenbrock, E. H. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. PubMed DOI PMC

Prank, M., Kenaley, S. C., Bergstrom, G. C., Acevedo, M. & Mahowald, N. M. Climate change impacts the spread potential of wheat stem rust, a significant crop disease. DOI

Hafeez, A. N. et al. Creation and judicious application of a wheat resistance gene atlas. PubMed DOI

Cavalet-Giorsa, E. et al. Origin and evolution of the bread wheat D genome. PubMed DOI PMC

Knight, E. et al. Mapping the ‘breaker’ element of the gametocidal locus proximal to a block of sub-telomeric heterochromatin on the long arm of chromosome 4Ssh of Aegilops sharonensis. PubMed DOI PMC

Pont, C. et al. Tracing the ancestry of modern bread wheats. PubMed DOI

Tsujimoto, H. & Tsunewaki, K. Gametocidal genes in wheat and its relatives. I. Genetic analyses in common wheat of a gametocidal gene derived from Aegilops speltoides. DOI

Sánchez-Martín, J. et al. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. PubMed DOI PMC

Steuernagel, B. et al. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. PubMed DOI

Arora, S. et al. Resistance gene cloning from a wild crop relative by sequence capture and association genetics. PubMed DOI

Gaurav, K. et al. Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement. PubMed DOI PMC

Thind, A. K. et al. Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. PubMed DOI

Wang, Y. & Koo, D. An unusual tandem kinase fusion protein confers leaf rust resistance in wheat. PubMed DOI PMC

Walkowiak, S. et al. Multiple wheat genomes reveal global variation in modern breeding. PubMed DOI PMC

Athiyannan, N., Aouini, L., Wang, Y. & Krattinger, S. G. Unconventional R proteins in the botanical tribe Triticeae. PubMed DOI

Mapuranga, J. et al. Harnessing genetic resistance to rusts in wheat and integrated rust management methods to develop more durable resistant cultivars. PubMed DOI PMC

Lolle, S., Stevens, D. & Coaker, G. Plant NLR-triggered immunity: from receptor activation to downstream signaling. PubMed DOI PMC

Yu, G. et al. Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62. PubMed DOI PMC

Klymiuk, V., Coaker, G., Fahima, T. & Pozniak, C. J. Tandem protein kinases emerge as new regulators of plant immunity. PubMed DOI PMC

Li, H. et al. Wheat powdery mildew resistance gene Pm13 encodes a mixed lineage kinase domain-like protein. PubMed DOI PMC

Debernardi, J. M. et al. A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. PubMed DOI PMC

Hayta, S., Smedley, M. A., Clarke, M., Forner, M. & Harwood, W. A. An efficient agrobacterium-mediated transformation protocol for hexaploid and tetraploid wheat. PubMed DOI

Wang, K. et al. The gene TaWOX5 overcomes genotype dependency in wheat genetic transformation. PubMed DOI

Kishii, M. An update of recent use of Aegilops species in wheat breeding. PubMed DOI PMC

Millet, E. Exploitation of Aegilops species of section Sitopsis for wheat improvement. DOI

Scott, J. C., Manisterski, J., Sela, H., Ben-Yehuda, P. & Steffenson, B. J. Resistance of Aegilops species from Israel to widely virulent African and Israeli races of the wheat stem rust pathogen. PubMed DOI

Anikster, Y., Manisterski, J., Long, D. L. & Leonard, K. J. Resistance to leaf rust, stripe rust, and stem rust in Aegilops spp. in Israel. PubMed DOI

Huang, L. et al. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. PubMed DOI PMC

Olivera, P. D., Kolmer, J. A., Anikster, Y. & Steffenson, B. J. Resistance of Sharon goatgrass (Aegilops sharonensis) to fungal diseases of wheat. PubMed DOI

Millet, E. et al. Introgression of leaf rust and stripe rust resistance from Sharon goatgrass (Aegilops sharonensis Eig) into bread wheat (Triticum aestivum L.). PubMed DOI

Khazan, S. et al. Reducing the size of an alien segment carrying leaf rust and stripe rust resistance in wheat. PubMed DOI PMC

Steuernagel, B., Vrána, J., Karafiátová, M., Wulff, B. B. H. & Doležel, J. Rapid gene isolation using MutChromSeq. PubMed DOI

Ni, F. et al. Sequencing trait-associated mutations to clone wheat rust-resistance gene YrNAM. PubMed DOI PMC

Lee, W. S., Rudd, J. J. & Kanyuka, K. Virus induced gene silencing (VIGS) for functional analysis of wheat genes involved in Zymoseptoria tritici susceptibility and resistance. PubMed DOI PMC

Sela, H. et al. Ancient diversity of splicing motifs and protein surfaces in the wild emmer wheat (Triticum dicoccoides) LR10 coiled-coil (CC) and leucine-rich repeat (LRR) domains. PubMed DOI PMC

Sukarta, O. C. A., Slootweg, E. J. & Goverse, A. Structure-informed insights for NLR functioning in plant immunity. PubMed DOI

Rhoads, A. & Au, K. F. PacBio sequencing and its applications. PubMed DOI PMC

Sedlazeck, F. J. et al. Accurate detection of complex structural variations using single-molecule sequencing. PubMed DOI PMC

Kiselev, K. V. et al. Influence of the 135 bp intron on stilbene synthase VaSTS11 transgene expression in cell cultures of grapevine and different plant generations of Arabidopsis thaliana. DOI

Meyberg, M. Selective staining of fungal hyphae in parasitic and symbiotic plant-fungus associations. PubMed DOI

Bailey, P. C. et al. Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions. PubMed DOI PMC

Zhou, Y. et al. Allele mining for blast-resistance gene at Pi5 locus in rice. Plant.

Akpinar, B. et al. The complete genome sequence of elite bread wheat cultivar, ‘Sonmez’. PubMed DOI PMC

Sato, K. et al. Chromosome-scale genome assembly of the transformation-amenable common wheat cultivar ’Fielder. PubMed DOI PMC

Zhou, Y. et al. Introgressing the Aegilops tauschii genome into wheat as a basis for cereal improvement. PubMed DOI

Li, L. F. et al. Genome sequences of five Sitopsis species of Aegilops and the origin of polyploid wheat B subgenome. PubMed DOI

Page, R. et al. Genome-wide association mapping of rust resistance in Aegilops longissima. PubMed DOI PMC

Olivera, P. D., Anikster, Y. & Steffenson, B. J. Genetic diversity and population structure in Aegilops sharonensis. DOI

Fukuoka, S. et al. Loss of function of a proline-containing protein confers durable disease resistance in rice. PubMed DOI

Zhao, H. et al. The rice blast resistance gene Ptr encodes an atypical protein required for broad-spectrum disease resistance. PubMed DOI PMC

Krattinger, S. G. et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. PubMed DOI

Moore, J. W. et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. PubMed DOI

Narusaka, M., Hatakeyama, K., Shirasu, K. & Narusaka, Y. Arabidopsis dual resistance proteins, both RPS4 and RRS1, are required for resistance to bacterial wilt in transgenic Brassica crops. PubMed DOI PMC

Milligan, S. B. et al. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. PubMed DOI PMC

Rossi, M. et al. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. PubMed DOI PMC

Nombela, G., Williamson, V. M. & Muñiz, M. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. PubMed DOI

Schultink, A., Qi, T., Lee, A., Steinbrenner, A. D. & Staskawicz, B. Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. PubMed DOI

Li, W., Deng, Y., Ning, Y., He, Z. & Wang, G. L. Exploiting broad-spectrum disease resistance in crops: from molecular dissection to breeding. PubMed DOI

Brabham, H. J. et al. Barley MLA3 recognizes the host-specificity effector Pwl2 from Magnaporthe oryzae. PubMed DOI PMC

Bettgenhaeuser, J. et al. The barley immune receptor Mla recognizes multiple pathogens and contributes to host range dynamics. PubMed DOI PMC

Brabham, H. J. et al. Rapid discovery of functional NLRs using the signature of high expression, high-throughput transformation, and large-scale phenotyping.

McIntosh, R. A. Nature of induced mutations affecting disease reaction in wheat.

Marais, G. F., McCallum, B. & Marais, A. S. Leaf rust and stripe rust resistance genes derived from Aegilops sharonensis. DOI

Sánchez-Martín, J. & Keller, B. NLR immune receptors and diverse types of non-NLR proteins control race-specific resistance in Triticeae. PubMed DOI

Dinglasan, E., Periyannan, S. & Hickey, L. T. Harnessing adult-plant resistance genes to deploy durable disease resistance in crops. PubMed DOI PMC

Ellis, J. G., Lagudah, E. S., Spielmeyer, W. & Dodds, P. N. The past, present and future of breeding rust resistant wheat. PubMed DOI PMC

Chen, S., Zhang, W., Bolus, S., Rouse, M. N. & Dubcovsky, J. Identification and characterization of wheat stem rust resistance gene Sr21 effective against the Ug99 race group at high temperature. PubMed DOI PMC

McIntosh, R. A. & Luig, N. H. Linkage of genes for reaction to Puccinia graminis f. sp. tritici and P. recondita in selkirk wheat and related cultivars. DOI

Zhang, W. et al. Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. PubMed DOI PMC

Nakano, M. & Mukaihara, T. The type III effector RipB from Ralstonia solanacearum RS1000 acts as a major avirulence factor in Nicotiana benthamiana and other Nicotiana species. PubMed DOI PMC

Faris, J. D. et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. PubMed DOI PMC

Avni, R. et al. Genome sequences of three Aegilops species of the section Sitopsis reveal phylogenetic relationships and provide resources for wheat improvement. PubMed DOI PMC

Kovaka, S., Ou, S., Jenike, K. M. & Schatz, M. C. Approaching complete genomes, transcriptomes and epi-omes with accurate long-read sequencing. PubMed DOI PMC

Long, D. & Kolmer, J. A North American system of nomenclature for Puccinia triticina. DOI

Roelfs, A. P. An international system of nomenclature for Puccinia graminis f. sp. tritici. DOI

Wan, A. & Chen, X. Virulence characterization of Puccinia striiformis f. sp. tritici using a new set of Yr single-gene line differentials in the United States in 2010. PubMed DOI

Ben-David, R. et al. Differentiation among Blumeria graminis f. sp. tritici isolates originating from wild versus domesticated Triticum species in Israel. PubMed DOI

Huang, S., Steffenson, B. J., Sela, H. & Stinebaugh, K. Resistance of PubMed DOI

Zadoks, J. C., Chang, T. T. & Konzak, C. F. A decimal code for the growth stages of cereals. DOI

Šimková, H., Číhalíková, J., Vrána, J., Lysák, M. & Doležel, J. Preparation of HMW DNA from plant nuclei and chromosomes isolated from root tips. DOI

Giorgi, D. et al. FISHIS: fluorescence In Situ Hybridization in suspension and chromosome flow sorting made easy. PubMed DOI PMC

Molnár, I. et al. Dissecting the U, M, S and C genomes of wild relatives of bread wheat (Aegilops spp.) into chromosomes and exploring their synteny with wheat. PubMed DOI

Zhang, Y., Zhu, M. L. & Dai, S. L. Analysis of karyotype diversity of 40 Chinese chrysanthemum cultivars. DOI

Badaeva, E. D., Friebe, B. & Gill, B. S. Genome differentiation in Aegilops. 1. Distribution of highly repetitive DNA sequences on chromosomes of diploid species. PubMed DOI

Šimková, H. et al. Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley. PubMed DOI PMC

Hummel, A. W. et al. Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. PubMed DOI PMC

Zimin, A. V. et al. The MaSuRCA genome assembler. PubMed DOI PMC

Jackman, S. D. et al. ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. PubMed DOI PMC

Wicker, T., Matthews, D. E. & Keller, B. TREP: a database for Triticeae repetitive elements. DOI

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. PubMed DOI PMC

Li, H. et al. The Sequence Alignment/Map format and SAMtools. PubMed DOI PMC

Robinson, J. T. et al. Integrative genomics viewer. PubMed DOI PMC

Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. PubMed DOI

Camacho, C. et al. BLAST+: architecture and applications. PubMed DOI PMC

Appels, R. et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome. PubMed DOI

Doyle, J. J. & Doyle, J. L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue.

Sharma, D. et al. An efficient method for extracting next-generation sequencing quality RNA from liver tissue of recalcitrant animal species. PubMed DOI

Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. PubMed DOI PMC

Collier, R. et al. Accurate measurement of transgene copy number in crop plants using droplet digital PCR. PubMed DOI

Giroux, M. J. & Morris, C. F. A glycine to serine change in puroindoline b is associated with wheat grain hardness and low levels of starch-surface friabilin. DOI

Li, Z., Hansen, J. L., Liu, Y., Zemetra, R. S. & Berger, P. H. Using real-time PCR to determine transgene copy number in wheat. DOI

Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. PubMed DOI PMC

Andrews, S. et al.

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. PubMed DOI PMC

Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. PubMed DOI PMC

Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. PubMed DOI PMC

RcoreTeam. R.: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

Bateman, A. et al. UniProt: the universal protein knowledgebase in 2021. PubMed DOI PMC

Steuernagel, B. et al. The NLR-annotator tool enables annotation of the intracellular immune receptor repertoire. PubMed DOI PMC

Bailey, T. L. & Gribskov, M. Combining evidence using p-values: application to sequence homology searches. PubMed DOI

Martin, E. C. et al. NLRscape: an atlas of plant NLR proteins. PubMed DOI PMC

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. Europe PMC Funders Group The Phyre2 web portal for protein modelling, prediction and analysis. PubMed DOI PMC

Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. PubMed DOI PMC

van Kempen, M. et al. Fast and accurate protein structure search with Foldseek. PubMed DOI PMC

De Beukelaer, H., Davenport, G. F. & Fack, V. Core Hunter 3: flexible core subset selection. PubMed DOI PMC

Edgar, R. C. M. U. S. C. L. E. Multiple sequence alignment with high accuracy and high throughput. PubMed DOI PMC

Martin, D. P. et al. RDP5: a computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. PubMed DOI PMC

Yuan, C. et al. A high throughput barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PubMed DOI PMC

Zhang, R. et al. Generation of herbicide tolerance traits and a new selectable marker in wheat using base editing. PubMed DOI

Liu, Z. & Friesen, T. DAB staining and visualization of hydrogen peroxide in wheat leaves. PubMed DOI PMC

Wenger, A. M. et al. Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome. PubMed DOI PMC

Eid, J. et al. Real-time DNA sequencing from single polymerase molecules. PubMed DOI

Marone, M. P., Singh, H. C., Pozniak, C. J. & Mascher, M. A technical guide to TRITEX, a computational pipeline for chromosome-scale sequence assembly of plant genomes. PubMed DOI PMC

Discovery of functional NLRs using expression level, high-throughput transformation and large-scale phenotyping

Progress and innovations of gene cloning in wheat and its close relatives