Crop losses caused by plant pathogens are a primary threat to stable food production. Stripe rust (Puccinia striiformis) is a fungal pathogen of cereal crops that causes significant, persistent yield loss. Stripe rust exhibits host species specificity, with lineages that have adapted to infect wheat and barley. While wheat stripe rust and barley stripe rust are commonly restricted to their corresponding hosts, the genes underlying this host specificity remain unknown. Here, we show that three resistance genes, Rps6, Rps7, and Rps8, contribute to immunity in barley to wheat stripe rust. Rps7 cosegregates with barley powdery mildew resistance at the Mla locus. Using transgenic complementation of different Mla alleles, we confirm allele-specific recognition of wheat stripe rust by Mla. Our results show that major resistance genes contribute to the host species specificity of wheat stripe rust on barley and that a shared genetic architecture underlies resistance to the adapted pathogen barley powdery mildew and non-adapted pathogen wheat stripe rust.

AgBiome Research Triangle Park NC 27709 USA

Center for Desert Agriculture Biological and Environmental Science and Engineering Division King Abdullah University of Science and Technology Thuwal 23955 6900 Saudi Arabia

Department of Integrated Plant Protection Agrotest Fyto Ltd Havlíčkova 2787 CZ 767 01 Kroměříž Czech Republic

Department of Plant Pathology University of Minnesota St Paul MN 55108 USA

Department of Plant Sciences University of Cambridge Downing Street Cambridge CB2 3EA UK

John Innes Centre Norwich Research Park Norwich NR4 7UH UK

KWS SAAT SE and Co KGaA 37574 Einbeck Germany

NIAB 93 Lawrence Weaver Road Cambridge CB3 0LE England UK

The James Hutton Institute Invergowrie Dundee DD2 5DA Scotland UK

The Sainsbury Laboratory University of East Anglia Norwich Research Park Norwich NR4 7UK England UK

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Nat Plants. 2022 Feb;8(2):100-101. doi: 10.1038/s41477-022-01097-y. PubMed

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Panstruga R, Moscou MJ. What is the molecular basis of nonhost resistance? Mol. Plant-Microbe Interact. 2020;33:1253–1264. PubMed

Heath MC. A comparative study of non-host interactions with rust fungi. Physiol. Plant Pathol. 1977;10:73–88.

Eriksson, J. Ueber die Specialisirung des Parasitismus bei den Getreiderostpilzen. Berichte der Deutschen Botanischen Gesellschaft 12 (1894).

Marchal, É. De la spécialisation du parasitisme chez l’Erysiphe graminis. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences CXXXV, 210–212 (1902).

Nielsen J. Host range of the smut species Ustilago nuda and Ustilago tritici in the tribe Triticeae. Can. J. Bot. /Rev. Can. Bot. 1978;56:901–915.

Edel-Hermann V, Lecomte C. Current status of Fusarium oxysporum formae speciales and races. Phytopathology. 2019;109:512–530. PubMed

Kato, H. Biological and genetical aspects in the perfect state of rice blast fungus Pyricularia oryzae Cav. and its allies. In: Gamma Field Symposia No. 17. Mutation Breeding for Disease Resistance, 1–22 (1978).

Crute, I. in The Downy Mildews (ed Spenser, D. M.) 237–255 (Academic Press, 1981).

Saharan, G. S. & Verma, P. R. White Rusts: a Review of Economically Important Species (International Development Research Centre, 1992).

Riley R, Macer RCF. The chromosomal distribution of the genetic resistance of rye to wheat pathogens. Can. J. Genet. Cytol. 1966;8:640–653.

Tosa Y. Genetic analysis of the avirulence of wheatgrass powdery mildew fungus on common wheat. Genome. 1989;32:913–917.

Thordal-Christensen H. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 2003;6:351–357. PubMed

Jones JD, Dangl JL. The plant immune system. Nature. 2006;444:323–329. PubMed

Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009;60:379–406. PubMed

Boutrot F, Zipfel C. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 2017;55:257–286. PubMed

Jacob F, Vernaldi S, Maekawa T. Evolution and conservation of plant NLR functions. Front. Immunol. 2013;4:297. PubMed PMC

Wilson RA, Talbot NJ. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat. Rev. Microbiol. 2009;7:185–195. PubMed

de Jonge R, et al. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science. 2010;329:953–955. PubMed

Toruno TY, Stergiopoulos I, Coaker G. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal Manners. Annu. Rev. Phytopathol. 2016;54:419–441. PubMed PMC

Michelmore RW, Meyers BC. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998;8:1113–1130. PubMed

Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 2010;11:539–548. PubMed

Gassmann W, Hinsch ME, Staskawicz BJ. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J. 1999;20:265–277. PubMed

Deslandes L, et al. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl Acad. Sci. USA. 2003;100:8024–8029. PubMed PMC

Narusaka M, et al. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 2009;60:218–226. PubMed

Birker D, et al. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 2009;60:602–613. PubMed

Nombela G, Williamson VM, Muniz M. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant-Microbe Interact. 2003;16:645–649. PubMed

Atamian HS, Eulgem T, Kaloshian I. SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta. 2012;235:299–309. PubMed

Briggs FN, Stanford EH. Linkage of factors for resistance to mildew in barley. J. Genet. 1938;37:107–117. PubMed PMC

Zhou F, et al. Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell. 2001;13:337–350. PubMed PMC

Wei F, Wing RA, Wise RP. Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell. 2002;14:1903–1917. PubMed PMC

Seeholzer S, et al. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol. Plant-Microbe Interact. 2010;23:497–509. PubMed

Brabham, H. J., Hernández-Pinzón, I., Holden, S., Lorang, J. & Moscou, M. J. An ancient integration in a plant NLR is maintained as a trans-species polymorphism. bioRxiv10.1101/239541 (2018).

Jørgensen JH. Genetics of powdery mildew resistance in barley. Crit. Rev. Plant Sci. 1994;13:97–119.

Kinizios S, Jahoor A, Fischbeck G. Powdery-mildew-resistance genes Mla29 and Mla32 in H. spontaneum derived winter-barley lines. Plant Breed. /Z. Pflanzenzucht. 1995;114:265–266.

Periyannan S, et al. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science. 2013;341:786–788. PubMed

Jordan T, et al. The wheat Mla homologue TmMla1 exhibits an evolutionarily conserved function against powdery mildew in both wheat and barley. Plant J. 2011;65:610–621. PubMed

Mago R, et al. The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat. Plants. 2015;1:15186. PubMed

Lu X, et al. Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proc. Natl Acad. Sci. USA. 2016;113:E6486–E6495. PubMed PMC

Chen J, et al. Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science. 2017;358:1607. PubMed

Saur IM, et al. Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. eLife. 2019;8:e44471. PubMed PMC

Savary S, et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evolution. 2019;3:430–439. PubMed

Derevnina L, Zhou M, Singh D, Wellings CR, Park RF. The genetic basis of resistance to barley grass yellow rust (Puccinia striiformis f. sp. pseudo-hordei) in Australian barley cultivars. Theor. Appl. Genet. 2015;128:187–197. PubMed

Dracatos PM, Haghdoust R, Singh D, Park RF. Exploring and exploiting the boundaries of host specificity using the cereal rust and mildew models. N. Phytol. 2018;218:453–462. PubMed

Haghdoust R, Singh D, Garnica DP, Park RF, Dracatos PM. Isolate specificity and polygenic inheritance of resistance in barley to diverse heterologous Puccinia striiformis isolates. Phytopathology. 2018;108:617–626. PubMed

Niks RE, Alemu SK, Marcel TC, van Heyzen S. Mapping genes in barley for resistance to Puccinia coronata from couch grass and to P. striiformis from brome, wheat and barley. Euphytica. 2015;206:487–499.

Straib W. Untersuchungen über das Vorkommen physiologischer Rassen des Gelbrostes (Puccinia glumarum) in den Jaren 1935/36 und über die Aggressivität einiger neuer Formen auf Getreide und Gräsern. Arb. biol. Abt. (Anst. -Reichsanst.), Berl. 1937;22:91–119.

Dawson AM, et al. The development of quick, robust, quantitative phenotypic assays for describing the host-nonhost landscape to stripe rust. Front. Plant Sci. 2015;6:876. PubMed PMC

Close TJ, et al. Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics. 2009;10:582. PubMed PMC

Hovmøller MS, Sørensen CK, Walter S, Justesen AF. Diversity of Puccinia striiformis on cereals and grasses. Annu. Rev. Phytopathol. 2011;49:197–217. PubMed

Thomas, W. et al. HGCA Project Report 528: Association Genetics of UK Elite Barley (AGOUEB) (Agriculture and Horticulture Development Board, 2014).

Steffenson BJ, et al. A walk on the wild side: mining wild wheat and barley collections for rust resistance genes. Aust. J. Agric. Res. 2007;58:532–544.

Atienza SG, Jafary H, Niks RE. Accumulation of genes for susceptibility to rust fungi for which barley is nearly a nonhost results in two barley lines with extreme multiple susceptibility. Planta. 2004;220:71–79. PubMed

Yeo FK, et al. Golden SusPtrit: a genetically well transformable barley line for studies on the resistance to rust fungi. Theor. Appl. Genet. 2014;127:325–337. PubMed

Li K, et al. Fine mapping of barley locus Rps6 conferring resistance to wheat stripe rust. Theor. Appl. Genet. 2016;129:845–859. PubMed PMC

Dawson AM, et al. Isolation and fine mapping of Rps6: an intermediate host resistance gene in barley to wheat stripe rust. Theor. Appl. Genet. 2016;129:831–843. PubMed PMC

Büschges R, et al. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell. 1997;88:695–705. PubMed

Wei F, et al. The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics. 1999;153:1929–1948. PubMed PMC

Moseman JG. Isogenic barley lines for reaction to Erysiphe graminis f. sp. hordei. Crop Sci. 1972;12:681–682.

Kølster P, Munk L, Stølen O, Løhde J. Near-isogenic barley lines with genes for resistance to powdery mildew. Crop Sci. 1986;26:903–907.

Kølster P, Stølen O. Barley isolines with genes for resistance to Erysiphe graminis f. sp. hordei in the recurrent parent ‘Siri’. Plant Breed. /Z. Pflanzenzucht. 1987;98:79–82.

Maekawa T, et al. Subfamily-specific specialization of RGH1/MLA immune receptors in wild barley. Mol. Plant-Microbe Interact. 2019;32:107–119. PubMed

Halterman DA, Wise RP. A single-amino acid substitution in the sixth leucine-rich repeat of barley MLA6 and MLA13 alleviates dependence on RAR1 for disease resistance signaling. Plant J. 2004;38:215–226. PubMed

Schreiber M, et al. A genome assembly of the barley ‘Transformation Reference’ cultivar Golden Promise. G3 (Bethesda) 2020;10:1823–1827. PubMed PMC

Bauer S, et al. The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold. PLoS Path. 2021;17:e1009223. PubMed PMC

Inukai T, Vales MI, Hori K, Sato K, Hayes PM. RMo1 confers blast resistance in barley and is located within the complex of resistance genes containing Mla, a powdery mildew resistance gene. Mol. Plant-Microbe Interact. 2006;19:1034–1041. PubMed

Leng Y, et al. The gene conferring susceptibility to spot blotch caused by Cochliobolus sativus is located at the Mla locus in barley cultivar Bowman. Theor. Appl. Genet. 2018;131:1531–1539. PubMed

Wiesner-Hanks T, Nelson R. Multiple disease resistance in plants. Annu. Rev. Phytopathol. 2016;54:229–252. PubMed

Milligan SB, 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. Plant Cell. 1998;10:1307–1319. PubMed PMC

Debieu M, Huard-Chauveau C, Genissel A, Roux F, Roby D. Quantitative disease resistance to the bacterial pathogen Xanthomonas campestris involves an Arabidopsis immune receptor pair and a gene of unknown function. Mol. Plant Pathol. 2016;17:510–520. PubMed PMC

Le Roux C, et al. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell. 2015;161:1074–1088. PubMed

Sarris PF, et al. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell. 2015;161:1089–1100. PubMed

Maekawa T, Kracher B, Vernaldi S, Ver Loren van Themaat E, Schulze-Lefert P. Conservation of NLR-triggered immunity across plant lineages. Proc. Natl Acad. Sci. USA. 2012;109:20119–20123. PubMed PMC

Ames N, Dreiseitl A, Steffenson BJ, Muehlbauer GJ. Mining wild barley for powdery mildew resistance. Plant Pathol. 2015;64:1396–1406.

Collard BC, Mackill DJ. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008;363:557–572. PubMed PMC

Meehan F, Murphy HC. A new Helminthosporium blight of oats. Science. 1946;104:413–414. PubMed

Inoue Y, et al. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science. 2017;357:80–83. PubMed

Ullrich, S. E. Barley, Production, Improvement, and Uses. Vol. 1 (Wiley-Blackwell, 2011).

Wellings CR. Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006. Aust. J. Agric. Res. 2007;58:567–575.

Chen XM, Line RF, Leung H. Virulence and polymorphic DNA relationships of Puccinia striiformis f. sp. hordei to other rusts. Phytopathology. 1995;85:1335–1342.

Bettgenhaeuser J, et al. The genetic architecture of colonization resistance in Brachypodium distachyon to non-adapted stripe rust (Puccinia striiformis) isolates. PLoS Genet. 2018;14:e1007637. PubMed PMC

Hubbard A, et al. Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol. 2015;16:23. PubMed PMC

Niks RE, van Heyzen S, Szabo LJ, Alemu SK. Host status of barley to Puccinia coronata from couch grass and P. striiformis from wheat and brome. Eur. J. Plant Pathol. 2013;136:393–405.

Brown JK, Tellier A. Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 2011;49:345–367. PubMed

Horsley RD, et al. Identification of QTLs associated with Fusarium head blight resistance in barley accession CIho 4196. Crop Sci. 2006;46:145–156.

Sato K, Nankaku N, Takeda K. A high-density transcript linkage map of barley derived from a single population. Heredity. 2009;103:110–117. PubMed

Dreiseitl A. A novel resistance against powdery mildew found in winter barley cultivars. Plant Breed. 2019;138:840–845.

Stewart CN, Jr, Via LE. A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. BioTechniques. 1993;14:748–750. PubMed

Dreiseitl A. Pathogenic divergence of Central European and Australian populations of Blumeria graminis f. sp. hordei. Ann. Appl. Biol. 2014;165:364–372.

Torp, J., Jensen, H. P. & Jørgensen, J. H. Powdery mildew resistance genes in 106 Northwest European spring barley cultivars. Kongelige Veterinaer- Og Landbohoejskole, 75–102 (1978).

McNeal FH, Konzak CF, Smith EP, Tate WS, Russell TS. A uniform system for recording and processing cereal research data. U. S. Dep. Agriculture-Agric. Res. Serv. ARS. 1971;34–121:42.

Ayliffe M, et al. Nonhost resistance of rice to rust pathogens. Mol. Plant-Microbe Interact. 2011;24:1143–1155. PubMed

Kota R, et al. EST-derived single nucleotide polymorphism markers for assembling genetic and physical maps of the barley genome. Funct. Integr. Genomics. 2008;8:223–233. PubMed

Muñoz-Amatriaín M, et al. An improved consensus linkage map of barley based on flow-sorted chromosomes and single nucleotide polymorphism markers. Plant Genome. 2011;4:238–249.

Mascher M, et al. Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ) Plant J. 2013;76:718–727. PubMed PMC

Poland JA, Brown PJ, Sorrells ME, Jannink JL. Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE. 2012;7:e32253. PubMed PMC

Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 2003;19:889–890. PubMed

Basten, C. J., Weir, B. S. & Zeng, Z.-B. In: Proc. 5th World Congress on Genetics Applied to Livestock Production: Computing Strategies and Software (eds C. Smith et al.) 65-66 (Organizing Committee, 5th World Congress on Genetics Applied to Livestock Production, Guelph, Ontario, Canada).

Basten, C. J., Weir, B. S. & Zeng, Z.-B. QTL Cartographer Version 1.16 (Department of Statistics, North Carolina State University, 2002).

Lauter N, Moscou MJ, Habiger J, Moose SP. Quantitative genetic dissection of shoot architecture traits in maize: towards a functional genomics approach. Plant. Genome. 2008;1:99–110.

Grabherr MG, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011;29:644–652. PubMed PMC

Witek K, et al. Accelerated cloning of a potato late blight-resistance gene using RenSeq and SMRT sequencing. Nat. Biotechnol. 2016;34:656–660. PubMed

IBGSC. A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491:711–716. PubMed

Halterman D, Zhou F, Wei F, Wise RP, Schulze-Lefert P. The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J. 2001;25:335–348. PubMed

Gibson DG. Programming biological operating systems: genome design, assembly and activation. Nat. Methods. 2014;11:521. PubMed

Hensel G, Kastner C, Oleszczuk S, Riechen J, Kumlehn J. Agrobacterium-mediated gene transfer to cereal crop plants: Current protocols for barley, wheat, triticale, and maize. Int. J. Plant Genomics. 2009;2009:9. PubMed PMC

Bartlett JG, Alves SC, Smedley M, Snape JW, Harwood WA. High-throughput Agrobacterium-mediated barley transformation. Plant Methods. 2008;4:22. PubMed PMC

Moscou, M. J. Source data for all figures in the manuscript entitled ‘The barley immune receptor Mla recognizes multiple pathogens and contr ibutes to host range dynamics’. Figshare, 10.6084/m9.figshare.16918774 (2021).

Moscou, M. J. Genotypic and phenotypic analysis of 31 barley populations inoculated with wheat stripe rust. Figshare, 10.6084/m9.figshare.7763018.v1 (2021).

Moscou, M. J. QKcartographer: a set of scripts for processing QTL Cartographer output. Figshare, 10.6084/m9.figshare.16912210.v1 (2021).

Moscou, M. J. QKdomain: a set of scripts that can be used for domain analysis. Figshare, 10.6084/m9.figshare.16923799 (2021).

Moscou, M. J. Q. Kgenome. A set of scripts for converting genomes based on resequencing information. Figshare, 10.6084/m9.figshare.16923802 (2021).

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