{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T16:46:31Z","timestamp":1791996391771,"version":"4.4.0"},"reference-count":72,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T00:00:00Z","timestamp":1788998400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T00:00:00Z","timestamp":1791849600000},"content-version":"vor","delay-in-days":33,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Tan spot is an economically important fungal disease of wheat that occurs globally. In this necrotrophic pathosystem, pathogen effectors are recognized by wheat genes in an inverse gene-for-gene manner, leading to the hijacking of host defense mechanisms and ultimately disease susceptibility. Here, we identified the tan spot susceptibility gene\n                    <jats:italic>Tsc2<\/jats:italic>\n                    through positional cloning, mutagenesis, and transgenic complementation.\n                    <jats:italic>Tsc2<\/jats:italic>\n                    encodes a diverged form of the exocyst subunit Exo70FX15 that localizes to the nucleus and cytoplasm and does not interact directly with the fungal effector. A 21\u2011nucleotide deletion in\n                    <jats:italic>Tsc2<\/jats:italic>\n                    occurred in durum wheat more than a century ago and subsequently spread to common wheat through breeding practices, which allowed recognition of the pathogen effector and subsequent hijacking of the host immune system. We demonstrate that elimination of\n                    <jats:italic>Tsc2<\/jats:italic>\n                    through conventional breeding using a diagnostic marker or disruption of\n                    <jats:italic>Tsc2<\/jats:italic>\n                    by gene editing can be used to improve tan spot resistance in wheat.\n                  <\/jats:p>","DOI":"10.1038\/s41467-026-77720-9","type":"journal-article","created":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T18:23:20Z","timestamp":1789064600000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["The hijacking of a wheat Exo70-like protein by a fungal pathogen triggers disease"],"prefix":"10.1038","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2637-7282","authenticated-orcid":false,"given":"Gurminder","family":"Singh","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7577-1123","authenticated-orcid":false,"given":"Katherine L. D.","family":"Running","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0831-4069","authenticated-orcid":false,"given":"Zengcui","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9747-2618","authenticated-orcid":false,"given":"Sudeshi","family":"Seneviratne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0538-1028","authenticated-orcid":false,"given":"Krishna","family":"Acharya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6350-4543","authenticated-orcid":false,"given":"Tiana M.","family":"Roth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8762-0688","authenticated-orcid":false,"given":"Amanda R.","family":"Peters Haugrud","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3392-6646","authenticated-orcid":false,"given":"Agnes","family":"Szabo-Hever","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pooja","family":"Kumari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4809-0864","authenticated-orcid":false,"given":"Phillip E.","family":"McClean","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8106-9186","authenticated-orcid":false,"given":"Zhaohui","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4558-8448","authenticated-orcid":false,"given":"Shengming","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9653-3287","authenticated-orcid":false,"given":"Justin D.","family":"Faris","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,9,10]]},"reference":[{"key":"77720_CR1","doi-asserted-by":"publisher","first-page":"100558","DOI":"10.1016\/j.gfs.2021.100558","volume":"30","author":"O Erenstein","year":"2021","unstructured":"Erenstein, O. et al. Estimating the global number and distribution of maize and wheat farms. Glob. Food Secur. 30, 100558 (2021).","journal-title":"Glob. Food Secur."},{"key":"77720_CR2","doi-asserted-by":"publisher","first-page":"102310","DOI":"10.1016\/j.mib.2023.102310","volume":"73","author":"F Minter","year":"2023","unstructured":"Minter, F. & Saunders, D. G. Safeguarding wheat yields from cereal fungal invaders in the postgenomic era. Curr. Opin. Microbiol. 73, 102310 (2023).","journal-title":"Curr. Opin. Microbiol."},{"key":"77720_CR3","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1080\/07060669809500404","volume":"20","author":"ED De Wolf","year":"1998","unstructured":"De Wolf, E. D. et al. Vistas of tan spot research. Can. J. Plant Pathol. 20, 349\u2013370 (1998).","journal-title":"Can. J. Plant Pathol."},{"key":"77720_CR4","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1080\/07060660309507089","volume":"25","author":"SE Strelkov","year":"2003","unstructured":"Strelkov, S. E. & Lamari, L. Host\u2013parasite interactions in tan spot [Pyrenophora tritici-repentis] of wheat. Can. J. Plant Pathol. 25, 339\u2013349 (2003).","journal-title":"Can. J. Plant Pathol."},{"key":"77720_CR5","doi-asserted-by":"publisher","first-page":"2197","DOI":"10.1007\/s00122-013-2157-y","volume":"126","author":"JD Faris","year":"2013","unstructured":"Faris, J. D. et al. Genetics of tan spot resistance in wheat. Theor. Appl. Genet. 126, 2197\u20132217 (2013).","journal-title":"Theor. Appl. Genet."},{"key":"77720_CR6","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1038\/s41559-018-0793-y","volume":"3","author":"S Savary","year":"2019","unstructured":"Savary, S. et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430\u2013439 (2019).","journal-title":"Nat. Ecol. Evol."},{"key":"77720_CR7","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1016\/j.copbio.2021.09.002","volume":"73","author":"BB Wulff","year":"2022","unstructured":"Wulff, B. B. & Krattinger, S. G. The long road to engineering durable disease resistance in wheat. Curr. Opin. Biotechnol. 73, 270\u2013275 (2022).","journal-title":"Curr. Opin. Biotechnol."},{"key":"77720_CR8","unstructured":"Hosford, R. M. Jr. Tan spot-developing knowledge 1902\u20131981, virulent races and differentials, methodology, rating systems, other leaf diseases, literature. In Tan Spot of Wheat and Related Diseases Workshop 1\u201324 (North Dakota Agricultural Experiment Station, Fargo, ND, 1982)."},{"key":"77720_CR9","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1094\/PDIS.1999.83.3.269","volume":"83","author":"CK Evans","year":"1999","unstructured":"Evans, C. K. et al. Comparison of greenhouse and field testing to identify wheat resistant to tan spot. Plant Dis. 83, 269\u2013273 (1999).","journal-title":"Plant Dis."},{"key":"77720_CR10","doi-asserted-by":"publisher","first-page":"696","DOI":"10.1016\/j.cropro.2009.04.003","volume":"28","author":"SN Wegulo","year":"2009","unstructured":"Wegulo, S. N. et al. Effect of growth stage on the relationship between tan spot and spot blotch severity and yield in winter wheat. Crop Prot. 28, 696\u2013702 (2009).","journal-title":"Crop Prot."},{"key":"77720_CR11","doi-asserted-by":"publisher","unstructured":"Ciuffetti, L. M. et al. Pyrenophora tritici-repentis: a plant pathogenic fungus with global impact. In Genomics of Plant-Associated Fungi: Monocot Pathogens (eds Dean, R. A. et al.) 1\u201339 https:\/\/doi.org\/10.1007\/978-3-662-44053-7_1 (Springer, Berlin, 2014).","DOI":"10.1007\/978-3-662-44053-7_1"},{"key":"77720_CR12","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1071\/AR9820899","volume":"33","author":"R Rees","year":"1982","unstructured":"Rees, R. et al. Yield losses in wheat from yellow spot: comparison of estimates derived from single tillers and plots. Aust. J. Agric. Res. 33, 899\u2013908 (1982).","journal-title":"Aust. J. Agric. Res."},{"key":"77720_CR13","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1080\/07060669009500975","volume":"12","author":"JC Sutton","year":"1990","unstructured":"Sutton, J. C. & Vyn, T. J. Crop sequences and tillage practices in relation to diseases of winter wheat in Ontario. Can. J. Plant Pathol. 12, 358\u2013368 (1990).","journal-title":"Can. J. Plant Pathol."},{"key":"77720_CR14","doi-asserted-by":"publisher","first-page":"1606","DOI":"10.1016\/j.cropro.2007.01.009","volume":"26","author":"LN J\u00f8rgensen","year":"2007","unstructured":"J\u00f8rgensen, L. N. & Olsen, L. V. Control of tan spot (Drechslera tritici-repentis) using cultivar resistance, tillage methods and fungicides. Crop Prot. 26, 1606\u20131616 (2007).","journal-title":"Crop Prot."},{"key":"77720_CR15","unstructured":"Lamey, H. A. & McMullen, M. P. Crop Rotations for Managing Plant Disease http:\/\/hdl.handle.net\/10365\/17693 (2011)."},{"key":"77720_CR16","doi-asserted-by":"publisher","unstructured":"Singh, P. K. et al. Resistance breeding for tan spot (Pyrenophora tritici-repentis) of wheat. In Disease resistance in wheat (ed. Sharma, I.) 136\u2013150 https:\/\/doi.org\/10.1079\/9781845938185.0136 (CABI, UK, 2012).","DOI":"10.1079\/9781845938185.0136"},{"key":"77720_CR17","doi-asserted-by":"publisher","first-page":"13544","DOI":"10.1073\/pnas.1004090107","volume":"107","author":"JD Faris","year":"2010","unstructured":"Faris, J. D. et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. USA 107, 13544\u201313549 (2010).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"77720_CR18","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1111\/j.1469-8137.2010.03362.x","volume":"187","author":"LM Ciuffetti","year":"2010","unstructured":"Ciuffetti, L. M. et al. Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis\u2013 wheat interaction. N. Phytol. 187, 911\u2013919 (2010).","journal-title":"N. Phytol."},{"key":"77720_CR19","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1080\/07060660109506967","volume":"24","author":"SE Strelkov","year":"2002","unstructured":"Strelkov, S. E. et al. Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis. Can. J. Plant Pathol. 24, 29\u201335 (2002).","journal-title":"Can. J. Plant Pathol."},{"key":"77720_CR20","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1094\/MPMI-12-21-0299-R","volume":"35","author":"G Shi","year":"2022","unstructured":"Shi, G. et al. A conserved hypothetical gene is required but not sufficient for Ptr ToxC production in Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 35, 336\u2013348 (2022).","journal-title":"Mol. Plant Microbe Interact."},{"key":"77720_CR21","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1016\/j.pbi.2020.04.003","volume":"56","author":"JD Faris","year":"2020","unstructured":"Faris, J. D. & Friesen, T. L. Plant genes hijacked by necrotrophic fungal pathogens. Curr. Opin. Plant Biol. 56, 74\u201380 (2020).","journal-title":"Curr. Opin. Plant Biol."},{"key":"77720_CR22","unstructured":"Running, K. L. D. Genomic Characterization of Necrotrophic Effector Sensitivity Genes in Wheat (North Dakota State University, Fargo, ND, USA, 2022)."},{"key":"77720_CR23","doi-asserted-by":"publisher","first-page":"793925","DOI":"10.3389\/fpls.2022.793925","volume":"13","author":"KLD Running","year":"2022","unstructured":"Running, K. L. D. et al. Genomic analysis and delineation of the tan spot susceptibility locus Tsc1 in wheat. Front. Plant Sci. 13, 793925 (2022).","journal-title":"Front. Plant Sci."},{"key":"77720_CR24","doi-asserted-by":"publisher","first-page":"464","DOI":"10.1007\/s00122-004-1678-9","volume":"109","author":"TL Friesen","year":"2004","unstructured":"Friesen, T. L. & Faris, J. D. Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor. Appl. Genet. 109, 464\u2013471 (2004).","journal-title":"Theor. Appl. Genet."},{"key":"77720_CR25","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1094\/PHYTO-95-0144","volume":"95","author":"L Lamari","year":"2005","unstructured":"Lamari, L. et al. Forensic pathology of Canadian bread wheat: the case of tan spot. Phytopathology 95, 144\u2013152 (2005).","journal-title":"Phytopathology"},{"key":"77720_CR26","doi-asserted-by":"publisher","first-page":"179","DOI":"10.3835\/plantgenome2010.07.0017","volume":"3","author":"NS Abeysekara","year":"2010","unstructured":"Abeysekara, N. S. et al. Marker development and saturation mapping of the tan spot Ptr ToxB sensitivity locus Tsc2 in hexaploid wheat. Plant Genome 3, 179\u2013189 (2010).","journal-title":"Plant Genome"},{"key":"77720_CR27","doi-asserted-by":"publisher","first-page":"935","DOI":"10.1007\/s00122-019-03517-8","volume":"133","author":"B Corsi","year":"2020","unstructured":"Corsi, B. et al. Genetic analysis of wheat sensitivity to the ToxB fungal effector from Pyrenophora tritici-repentis, the causal agent of tan spot. Theor. Appl. Genet. 133, 935\u2013950 (2020).","journal-title":"Theor. Appl. Genet."},{"key":"77720_CR28","doi-asserted-by":"publisher","first-page":"4139","DOI":"10.1534\/g3.116.036525","volume":"6","author":"SK Virdi","year":"2016","unstructured":"Virdi, S. K. et al. New insights into the roles of host gene-necrotrophic effector interactions in governing susceptibility of durum wheat to tan spot and septoria nodorum blotch. G3 Genes Genomes Genet. 6, 4139\u20134150 (2016).","journal-title":"G3 Genes Genomes Genet."},{"key":"77720_CR29","doi-asserted-by":"publisher","first-page":"2227","DOI":"10.1007\/s00122-020-03593-1","volume":"133","author":"N Galagedara","year":"2020","unstructured":"Galagedara, N. et al. Genome-wide association mapping of tan spot resistance in a worldwide collection of durum wheat. Theor. Appl. Genet. 133, 2227\u20132237 (2020).","journal-title":"Theor. Appl. Genet."},{"key":"77720_CR30","first-page":"1967","volume":"113","author":"A Szabo-Hever","year":"2023","unstructured":"Szabo-Hever, A. et al. Association mapping of resistance to tan spot in the global durum panel. Phytopathology 113, 1967\u20131978 (2023).","journal-title":"Phytopathology"},{"key":"77720_CR31","doi-asserted-by":"publisher","DOI":"10.1186\/s12915-022-01433-w","volume":"20","author":"R Gourlie","year":"2022","unstructured":"Gourlie, R. et al. The pangenome of the wheat pathogen Pyrenophora tritici-repentis reveals novel transposons associated with necrotrophic effectors ToxA and ToxB. BMC Biol. 20, 239 (2022).","journal-title":"BMC Biol."},{"key":"77720_CR32","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1016\/j.pmpp.2005.12.004","volume":"67","author":"SE Strelkov","year":"2005","unstructured":"Strelkov, S. E. et al. Characterization of the ToxB gene from North African and Canadian isolates of Pyrenophora tritici-repentis. Physiol. Mol. Plant Pathol. 67, 164\u2013170 (2005).","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"77720_CR33","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1094\/MPMI-08-23-0114-FI","volume":"37","author":"M Hafez","year":"2024","unstructured":"Hafez, M. et al. Evolution of the ToxB gene in Pyrenophora tritici-repentis and related species. Mol. Plant Microbe Interact. 37, 327\u2013337 (2024).","journal-title":"Mol. Plant Microbe Interact."},{"key":"77720_CR34","doi-asserted-by":"publisher","first-page":"1082","DOI":"10.1094\/MPMI-05-15-0097-R","volume":"28","author":"M Figueroa","year":"2015","unstructured":"Figueroa, M. et al. Persistence of the host-selective toxin Ptr ToxB in the apoplast. Mol. Plant Microbe Interact. 28, 1082\u20131090 (2015).","journal-title":"Mol. Plant Microbe Interact."},{"key":"77720_CR35","doi-asserted-by":"publisher","first-page":"182","DOI":"10.3389\/fmicb.2019.00182","volume":"10","author":"PT See","year":"2019","unstructured":"See, P. T. et al. Heterologous expression of the Pyrenophora tritici-repentis effector proteins ToxA and ToxB, and the prevalence of effector sensitivity in Australian cereal crops. Front. Microbiol. 10, 182 (2019).","journal-title":"Front. Microbiol."},{"key":"77720_CR36","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1094\/MPMI.2001.14.5.675","volume":"14","author":"JP Martinez","year":"2001","unstructured":"Martinez, J. P. et al. Characterization of the ToxB gene from Pyrenophora tritici-repentis. Mol. Plant Microbe Interact. 14, 675\u2013677 (2001).","journal-title":"Mol. Plant Microbe Interact."},{"key":"77720_CR37","doi-asserted-by":"publisher","unstructured":"Seong, K. et al. Chromosome-level genome assembly of Triticum turgidum var \u2018Kronos\u2019. Zenodo https:\/\/doi.org\/10.5281\/ZENODO.11106422 (2024).","DOI":"10.5281\/ZENODO.11106422"},{"key":"77720_CR38","doi-asserted-by":"publisher","first-page":"E913","DOI":"10.1073\/pnas.1619268114","volume":"114","author":"KV Krasileva","year":"2017","unstructured":"Krasileva, K. V. et al. Uncovering hidden variation in polyploid wheat. Proc. Natl. Acad. Sci. USA 114, E913\u2013E921 (2017).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"77720_CR39","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1038\/s41594-017-0016-2","volume":"25","author":"K Mei","year":"2018","unstructured":"Mei, K. et al. Cryo-EM structure of the exocyst complex. Nat. Struct. Mol. Biol. 25, 139\u2013146 (2018).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"77720_CR40","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abn7258","volume":"8","author":"S Holden","year":"2022","unstructured":"Holden, S. et al. A lineage-specific Exo70 is required for receptor kinase\u2013mediated immunity in barley. Sci. Adv. 8, eabn7258 (2022).","journal-title":"Sci. Adv."},{"key":"77720_CR41","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2105287118","volume":"118","author":"L Synek","year":"2021","unstructured":"Synek, L. et al. Plasma membrane phospholipid signature recruits the plant exocyst complex via the EXO70A1 subunit. Proc. Natl. Acad. Sci. USA 118, e2105287118 (2021).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"77720_CR42","doi-asserted-by":"publisher","DOI":"10.21769\/BioProtoc.5633","volume":"16","author":"KLD Running","year":"2026","unstructured":"Running, K. L. D. et al. Fluorescence-based absent allele-specific amplification (FAASA) for high-throughput detection of absent alleles. Bio Protoc. 16, e5633 (2026).","journal-title":"Bio Protoc."},{"key":"77720_CR43","doi-asserted-by":"publisher","first-page":"569905","DOI":"10.3389\/fpls.2020.569905","volume":"11","author":"E Mazzucotelli","year":"2020","unstructured":"Mazzucotelli, E. et al. The global durum wheat panel (GDP): an international platform to identify and exchange beneficial alleles. Front. Plant Sci. 11, 569905 (2020).","journal-title":"Front. Plant Sci."},{"key":"77720_CR44","doi-asserted-by":"publisher","DOI":"10.1007\/s11032-023-01400-5","volume":"43","author":"AR Peters Haugrud","year":"2023","unstructured":"Peters Haugrud, A. R. et al. Genome-wide association mapping of resistance to the foliar diseases septoria nodorum blotch and tan spot in a global winter wheat collection. Mol. Breed. 43, 54 (2023).","journal-title":"Mol. Breed."},{"key":"77720_CR45","doi-asserted-by":"publisher","first-page":"851","DOI":"10.1094\/PDIS-05-24-0990-RE","volume":"109","author":"A Szabo-Hever","year":"2025","unstructured":"Szabo-Hever, A. et al. Evaluation of durum and hard red spring wheat panels for sensitivity to necrotrophic effectors produced by Parastagonospora nodorum. Plant Dis. 109, 851\u2013861 (2025).","journal-title":"Plant Dis."},{"key":"77720_CR46","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.1600822","volume":"2","author":"G Shi","year":"2016","unstructured":"Shi, G. et al. The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci. Adv. 2, e1600822 (2016).","journal-title":"Sci. Adv."},{"key":"77720_CR47","doi-asserted-by":"publisher","first-page":"1720","DOI":"10.1111\/tpj.16879","volume":"119","author":"S Seneviratne","year":"2024","unstructured":"Seneviratne, S. et al. Evolution, diversity, and function of the disease susceptibility gene Snn1 in wheat. Plant J. 119, 1720\u20131736 (2024).","journal-title":"Plant J."},{"key":"77720_CR48","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1111\/tpj.15194","volume":"106","author":"Z Zhang","year":"2021","unstructured":"Zhang, Z. et al. A protein kinase\u2013major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat. Plant J. 106, 720\u2013732 (2021).","journal-title":"Plant J."},{"key":"77720_CR49","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1094\/MPMI-10-24-0125-FI","volume":"38","author":"Z Zhang","year":"2025","unstructured":"Zhang, Z. et al. Protein kinase-major sperm protein (PK-MSP) genes mediate recognition of the fungal necrotrophic effector SnTox3 to cause septoria nodorum blotch in wheat. Mol. Plant Microbe Interact. 38, 315\u2013327 (2025).","journal-title":"Mol. Plant Microbe Interact."},{"key":"77720_CR50","first-page":"49","volume":"71","author":"V \u017d\u00e1rsk\u00fd","year":"2020","unstructured":"\u017d\u00e1rsk\u00fd, V. et al. Three subfamilies of exocyst EXO70 family subunits in land plants: early divergence and ongoing functional specialization. J. Exp. Bot. 71, 49\u201362 (2020).","journal-title":"J. Exp. Bot."},{"key":"77720_CR51","doi-asserted-by":"publisher","unstructured":"Bergum, M. et al. Putative neofunctionalization of a Poales-specific EXO70 clade. Preprint at bioRxiv https:\/\/doi.org\/10.1101\/2024.12.13.628418 (2024).","DOI":"10.1101\/2024.12.13.628418"},{"key":"77720_CR52","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-018-1392-6","volume":"19","author":"PC Bailey","year":"2018","unstructured":"Bailey, P. C. et al. Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions. Genome Biol. 19, 23 (2018).","journal-title":"Genome Biol."},{"key":"77720_CR53","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1111\/j.1365-313X.2006.02854.x","volume":"48","author":"L Synek","year":"2006","unstructured":"Synek, L. et al. AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. 48, 54\u201372 (2006).","journal-title":"Plant J."},{"key":"77720_CR54","first-page":"E41","volume":"113","author":"C Zhang","year":"2016","unstructured":"Zhang, C. et al. Endosidin2 targets conserved exocyst complex subunit EXO70 to inhibit exocytosis. Proc. Natl. Acad. Sci. USA 113, E41\u2013E50 (2016).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"77720_CR55","unstructured":"Hayes, H. K. et al. Thatcher Wheat. Bulletin 325 (University of Minnesota Agricultural Experiment Station, Saint Paul, MN, USA). https:\/\/hdl.handle.net\/11299\/163794 (1936)."},{"key":"77720_CR56","doi-asserted-by":"crossref","unstructured":"Rouse, M. N. et al. Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.). Theor. Appl. Genet. 127, 1549\u20131559 (2014).","DOI":"10.1007\/s00122-014-2319-6"},{"key":"77720_CR57","doi-asserted-by":"publisher","first-page":"581214","DOI":"10.3389\/fgene.2020.581214","volume":"11","author":"A Kokhmetova","year":"2021","unstructured":"Kokhmetova, A. et al. Genome-wide association study of tan spot resistance in a hexaploid wheat collection from Kazakhstan. Front. Genet. 11, 581214 (2021).","journal-title":"Front. Genet."},{"key":"77720_CR58","doi-asserted-by":"publisher","first-page":"582","DOI":"10.1080\/07060661.2020.1870002","volume":"43","author":"B Wei","year":"2021","unstructured":"Wei, B. et al. Race distribution of Pyrenophora tritici-repentis in relation to ploidy level and susceptibility of durum and winter bread wheat. Can. J. Plant Pathol. 43, 582\u2013598 (2021).","journal-title":"Can. J. Plant Pathol."},{"key":"77720_CR59","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1007\/s00122-025-04952-6","volume":"138","author":"KLD Running","year":"2025","unstructured":"Running, K. L. D. et al. Development of diagnostic markers for the disease susceptibility gene Tsn1 in wheat reveals novel resistance alleles and a new locus required for ToxA sensitivity. Theor. Appl. Genet. 138, 164 (2025).","journal-title":"Theor. Appl. Genet."},{"key":"77720_CR60","doi-asserted-by":"publisher","first-page":"787","DOI":"10.1111\/pbi.12183","volume":"12","author":"S Wang","year":"2014","unstructured":"Wang, S. et al. Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol. J. 12, 787\u2013796 (2014).","journal-title":"Plant Biotechnol. J."},{"key":"77720_CR61","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1007\/s00122-024-04767-x","volume":"137","author":"K Acharya","year":"2024","unstructured":"Acharya, K. et al. Genetic mapping of QTLs for resistance to bacterial leaf streak in hexaploid wheat. Theor. Appl. Genet. 137, 265 (2024).","journal-title":"Theor. Appl. Genet."},{"key":"77720_CR62","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-015-0582-8","volume":"16","author":"JA Chapman","year":"2015","unstructured":"Chapman, J. A. et al. A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biol. 16, 26 (2015).","journal-title":"Genome Biol."},{"key":"77720_CR63","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1093\/bioinformatics\/btx665","volume":"34","author":"L Du","year":"2018","unstructured":"Du, L. et al. Krait: an ultrafast tool for genome-wide survey of microsatellites and primer design. Bioinformatics 34, 681\u2013683 (2018).","journal-title":"Bioinformatics"},{"key":"77720_CR64","doi-asserted-by":"publisher","first-page":"2038","DOI":"10.1093\/bioinformatics\/btv069","volume":"31","author":"RH Ramirez-Gonzalez","year":"2015","unstructured":"Ramirez-Gonzalez, R. H. et al. PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31, 2038\u20132039 (2015).","journal-title":"Bioinformatics"},{"key":"77720_CR65","doi-asserted-by":"publisher","first-page":"3812","DOI":"10.1093\/nar\/gkg509","volume":"31","author":"PC Ng","year":"2003","unstructured":"Ng, P. C. & Henikoff, S. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res. 31, 3812\u20133814 (2003).","journal-title":"Nucleic Acids Res."},{"key":"77720_CR66","doi-asserted-by":"publisher","first-page":"1274","DOI":"10.1038\/s41587-020-0703-0","volume":"38","author":"JM Debernardi","year":"2020","unstructured":"Debernardi, J. M. et al. A GRF\u2013GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nat. Biotechnol. 38, 1274\u20131279 (2020).","journal-title":"Nat. Biotechnol."},{"key":"77720_CR67","doi-asserted-by":"publisher","first-page":"1916","DOI":"10.1111\/pbi.13872","volume":"20","author":"E Aliu","year":"2022","unstructured":"Aliu, E. et al. CRISPR RNA-guided integrase enables high-efficiency targeted genome engineering in Agrobacterium tumefaciens. Plant Biotechnol. J. 20, 1916\u20131927 (2022).","journal-title":"Plant Biotechnol. J."},{"key":"77720_CR68","doi-asserted-by":"publisher","DOI":"10.1186\/s13007-019-0503-z","volume":"15","author":"S Hayta","year":"2019","unstructured":"Hayta, S. et al. An efficient and reproducible Agrobacterium-mediated transformation method for hexaploid wheat (Triticum aestivum L.). Plant Methods 15, 121 (2019).","journal-title":"Plant Methods"},{"key":"77720_CR69","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1038\/s41592-022-01488-1","volume":"19","author":"M Mirdita","year":"2022","unstructured":"Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679\u2013682 (2022).","journal-title":"Nat. Methods"},{"key":"77720_CR70","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","volume":"596","author":"J Jumper","year":"2021","unstructured":"Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583\u2013589 (2021).","journal-title":"Nature"},{"key":"77720_CR71","doi-asserted-by":"publisher","DOI":"10.1186\/s12870-014-0327-y","volume":"14","author":"H-L Xing","year":"2014","unstructured":"Xing, H.-L. et al. A CRISPR\/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327 (2014).","journal-title":"BMC Plant Biol."},{"key":"77720_CR72","doi-asserted-by":"crossref","unstructured":"Engler, C. et al. A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3, e3647 (2008).","DOI":"10.1371\/journal.pone.0003647"}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41467-026-77720-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-026-77720-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-026-77720-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T16:03:30Z","timestamp":1791993810000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41467-026-77720-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,10]]},"references-count":72,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["77720"],"URL":"https:\/\/doi.org\/10.1038\/s41467-026-77720-9","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-8788414\/v1","asserted-by":"object"}]},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,10]]},"assertion":[{"value":"4 February 2026","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 September 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 September 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","label":"Competing interests","group":{"name":"EthicsHeading","label":"Ethics"}}],"article-number":"10713"}}