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Identification of a major dominant gene for race-nonspecific tan spot resistance in wild emmer wheat

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Abstract

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A single dominant gene found in tetraploid and hexaploid wheat controls broad-spectrum race-nonspecific resistance to the foliar disease tan spot caused by Pyrenophora tritici-repentis.

Abstract

Tan spot is an important foliar disease of durum and common wheat caused by the necrotrophic fungal pathogen Pyrenophora tritici-repentis. Genetic studies in common wheat have shown that pathogen-produced necrotrophic effectors interact with host genes in an inverse gene-for-gene manner to cause disease, but quantitative trait loci (QTLs) with broad race-nonspecific resistance also exist. Less work has been done to understand the genetics of tan spot interactions in durum wheat. Here, we evaluated a set of Langdon durum—wild emmer (Triticum turgidum ssp. dicoccoides) disomic chromosome substitution lines for reaction to four P. tritici-repentis isolates representing races 1, 2, 3, and 5 to identify wild emmer chromosomes potentially containing tan spot resistance genes. Chromosome 3B from the wild emmer accession IsraelA rendered the tan spot-susceptible durum cultivar Langdon resistant to all four fungal isolates. Genetic analysis indicated that a single dominant gene, designated Tsr7, governed resistance. Detailed mapping experiments showed that the Tsr7 locus is likely the same as the race-nonspecific QTL previously identified in the hexaploid wheat cultivars BR34 and Penawawa. Four user-friendly SNP-based semi-thermal asymmetric reverse PCR (STARP) markers cosegregated with Tsr7 and should be useful for marker-assisted selection of resistance. In addition to 3B, other wild emmer chromosomes contributed moderate levels of tan spot resistance, and, as has been shown previously for tetraploid wheat, the Tsn1-Ptr ToxA interaction was not associated with susceptibility. This is the first report of a major dominant gene governing resistance to tan spot in tetraploid wheat.

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References

  • Abeysekara NS, Friesen TL, Liu ZH, McClean PE, Faris JD (2010) Marker development and saturation mapping of the tan spot Ptr ToxB sensitivity locus Tsc2 in hexaploid wheat. Plant Genome 3:179–189

    CAS  Google Scholar 

  • Cantrell RG, Joppa LR (1991) Genetic analysis of quantitative traits in wild emmer (Triticum turgidum L. var. dicoccoides). Crop Sci 31:645–649

    Google Scholar 

  • Chu CG, Friesen TL, Xu SS, Faris JD (2008) Identification of novel tan spot resistance loci beyond the known host-selective toxin insensitivity loci in wheat. Theor Appl Genet 117:873–881

    CAS  PubMed  Google Scholar 

  • Chu CG, Chao S, Friesen TL, Faris JD, Zhong S, Xu SS (2010) Identification of novel tan spot resistance QTLs using an SSR-based linkage map of tetraploid wheat. Mol Breeding 25:327–338

    CAS  Google Scholar 

  • Faris JD, Friesen TL (2005) Identification of quantitative trait loci for race-nonspecific resistance to tan spot of wheat. Theor Appl Genet 111:386–392

    CAS  PubMed  Google Scholar 

  • Faris JD, Friesen TL (2009) Reevaluation of a tetraploid wheat population indicates that the Tsn1-ToxA interaction is the only factor governing susceptibility to Stagonospora nodorum blotch. Phytopathology 99:906–912

    CAS  PubMed  Google Scholar 

  • Faris JD, Anderson JA, Francl LJ, Jordahl JG (1997) RFLP mapping of resistance to chlorosis induction by Pyrenophora tritici-repentis in wheat. Theor Appl Genet 94:98–103

    CAS  PubMed  Google Scholar 

  • Faris JD, Haen KM, Gill BS (2000) Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics 154:823–835

    CAS  PubMed  PubMed Central  Google Scholar 

  • Faris JD, Zhang Z, Lu HJ, Lu SW, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci USA 107:13544–13549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Faris JD, Abeysekara NS, McClean PE, Xu SS, Friesen TL (2012) Tan spot susceptibility governed by the Tsn1 locus and non race-specific resistance QTL in a population derived from wheat lines Salamouni and Katepwa. Mol Breeding 30:1669–1678

    Google Scholar 

  • Faris JD, Liu ZH, Xu SS (2013) Genetics of tan spot resistance in wheat. Theor Appl Genet 126:2197–2217

    CAS  PubMed  Google Scholar 

  • Faris JD, Zhang QJ, Chao S, Zhang ZC, Xu SS (2014a) Analysis of agronomic and domestication traits in a durum x cultivated emmer wheat population using a high-density single nucleotide polymorphism-based linkage map. Theor Appl Genet 127:2333–2348

    PubMed  Google Scholar 

  • Faris JD, Zhang ZC, Garvin DF (2014b) Molecular and comparative mapping of genes governing spike compactness from wild emmer wheat. Mol Genet Genomics 289:641–651

    CAS  PubMed  Google Scholar 

  • Friesen TL, Faris JD (2004) Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor Appl Genet 109:464–471

    CAS  PubMed  Google Scholar 

  • Friesen TL, Ali S, Klein KK, Rasmussen JB (2005) Population genetic analysis of a global collection of Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Phytopathology 95:1144–1150

    CAS  PubMed  Google Scholar 

  • Garvin DF, Stack RW, Hansen JM (2009) Quantitative trait locus mapping of increased Fusarium head blight susceptibility associated with a wild emmer wheat chromosome. Phytopathology 99:447–452

    CAS  PubMed  Google Scholar 

  • Gonzalez-Hernadez JL, Elias EM, Kianian SF (2004) Mapping genes for grain protein concentration and grain yield on chromosome 5B of Triticum turgidum (L.) var. dicoccoides. Euphytica 139:217–225

    Google Scholar 

  • Gonzalez-Hernandez JL, Singh PK, Mergoum M, Adhikari TB, Kianian SF, Simsek S, Elias EM (2009) A quantitative trait locus on chromosome 5B controls resistance of Triticum turgidum (L.) var. dicoccoides to Stagonospora nodorum blotch. Euphytica 166:199–206

    CAS  Google Scholar 

  • He F, Pasam R, Shi F, Kant S, Keeble-Gagnere G, Kay P, Forrest K, Fritz A, Hucl P, Wiebe K, Knox R, Cuthbert R, Pozniak C, Akhunova A, Morrell PL, Davies JP, Webb SR, Spangenberg G, Hayes B, Daetwyler H, Tibbits J, Hayden M, Akhunov E (2019) Exome sequencing highlights the role of wild-relative introgression in shaping the adaptive landscape of the wheat genome. Nat Genet 51:896–904

    CAS  PubMed  Google Scholar 

  • Joehanes R, Nelson JC (2008) QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics 24:2788–2789

    CAS  PubMed  Google Scholar 

  • Joppa LR (1993) Chromosome engineering in tetraploid wheat. Crop Sci 33:908–913

    Google Scholar 

  • Joppa LR, Cantrell RG (1990) Chromosomal location of genes for grain protein content of wild tetraploid wheat. Crop Sci 30:1059–1064

    CAS  Google Scholar 

  • Joppa LR, Hareland GA, Cantrell RG (1991) Quality characteristics of the Langdon durum-dicoccoides chromosome substitution lines. Crop Sci 31:1513–1517

    Google Scholar 

  • Joppa LR, Du C, Hart GE, Hareland GA (1997) Mapping gene(s) for grain protein in tetraploid wheat (Triticum turgidum L.) using a population of recombinant inbred chromosome lines. Crop Sci 37:1586–1589

    CAS  Google Scholar 

  • Kariyawasam GK, Carter AH, Rasmussen JB, Faris JD, Xu SS, Mergoum M, Liu ZH (2016) Genetic relationships between race-nonspecific and race specific interactions in the wheat-Pyrenophora tritici-repentis pathosystem. Theor Appl Genet 129:897–908

    CAS  PubMed  Google Scholar 

  • Koladia VM, Faris JD, Richards JK, Brueggeman RS, Chao S, Friesen TL (2017) Genetic analysis of net form net blotch resistance in barley lines CIho 5791 and Tifang against a global collection of P. teres f. teres isolates. Theor Appl Genet 130:163–173

    CAS  PubMed  Google Scholar 

  • Kumar S, Gill BS, Faris JD (2007a) Identification and characterization of segregation distortion loci along chromosome 5B in tetraploid wheat. Mol Genet Genomics 278:1870196

    Google Scholar 

  • Kumar S, Stack RW, Friesen TL, Faris JD (2007b) Identification of a novel Fusarium head blight resistance quantitative trail locus on chromosome 7A in tetraploid wheat. Phytopathology 97:592–597

    CAS  PubMed  Google Scholar 

  • Lamari L, Bernier CC (1989) Evaluation of wheat lines and cultivars to tan spot Pyrenophora tritici-repentis based on lesion type. Can J Plant Pathol 11:49–56

    Google Scholar 

  • Lamari L, Sayoud R, Boulif M, Bernier CC (1995) Identification of a new race in Pyrenophora tritici-repentis: implications for the current pathotype classification system. Can J Plant Pathol 17:312–318

    Google Scholar 

  • Liu ZH, Zurn JD, Kariyawasam G, Faris JD, Shi GJ, Hansen J, Rasmussen JB, Acevedo M (2017) Inverse gene-for-gene interactions contribute additively to tan spot susceptibility in wheat. Theor Appl Genet 130:1267–1276

    CAS  PubMed  Google Scholar 

  • Long Y, Chao WS, Ma G, Xu SS, Qi L (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607. https://doi.org/10.1007/s00122-016-2838-4

    Article  CAS  PubMed  Google Scholar 

  • Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breed 30:1231–1235

    CAS  Google Scholar 

  • Nalam VJ, Vales MI, Watson CJW, Kianian SF, Riera-Lizarazu O (2006) Map-based analysis of genes affecting the brittle rachis character in tetraploid wheat (Triticum turgidum L.). Theor Appl Genet 112:373–381

    CAS  PubMed  Google Scholar 

  • Otto CD, Kianian SF, Elias EM, Stack RW, Joppa LR (2002) Genetic dissection of a major Fusarium head blight QTL in tetraploid wheat. Plant Mol Biol 48:625–632

    CAS  PubMed  Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier M-H, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed  PubMed Central  Google Scholar 

  • Sánchez-Martin J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, Vrána J, Kubalákaová M, Krattinger SG, Wicker T, Doležel J, Keller B, Wulff BB (2016) Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol 17:221

    PubMed  PubMed Central  Google Scholar 

  • Singh PK, Gonzalez-Hernandez JL, Mergoum M, Ali S, Adhikari TB, Kianian SF, Elias E, Hughes GR (2006) Identification and molecular mapping of a gene conferring resistance to Pyrenophora tritici-repentis race 3 in tetraploid wheat. Phytopathology 96:885–889

    CAS  PubMed  Google Scholar 

  • Singh PK, Mergoum M, Adhikari TB, Kianian SF, Elias EM (2007) Chromosomal location of genes for seeding resistance to tan spot and Stagonospora nodorum blotch in tetraploid wheat. Euphytica 155:27–34

    Google Scholar 

  • Singh PK, Mergoum M, Gonzalez-Hernandez JL, Ali S, Adhikari TB, Kianian SF, Elias EM, Hughes GR (2008a) Genetics and molecular mapping of resistance to necrosis-inducing race 5 of Pyrenophora tritici-repentis in tetraploid wheat. Mol Breeding 21:293–304

    CAS  Google Scholar 

  • Singh S, Bockus WW, Sharma I, Bowden RL (2008b) A novel source of resistance in wheat to Pyrenophora tritici-repentis race 1. Plant Dis 92:91–95

    PubMed  Google Scholar 

  • Singh PK, Singh RP, Duveiller E, Mergoum M, Adhikari TB, Elias EM (2010) Genetics of wheat-Pyrenophora tritici-repentis interactions. Euphytica 171:1–13

    Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    CAS  PubMed  Google Scholar 

  • Song QJ, Shi JR, Singh S, Fickus EW, Costa JM, Lewis J, Gill BS, Ward R, Cregan PB (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110:550–560

    CAS  PubMed  Google Scholar 

  • Sourdille P, Cadalen T, Guyomarc’h H, Snape JW, Perretant MR, Charmet G, Boeuf C, Bernard S, Bernard M (2003) An update of the Courtot x Chinese Spring intervarietal molecular marker linkage map for the QTL detection of agronomic traits in wheat. Theor Appl Genet 106:530–538

    CAS  PubMed  Google Scholar 

  • Stack RW, Elias EM, Mitchell Fetch J, Miller JD, Joppa LR (2002) Fusarium head blight reaction of Langdon durum-Triticum dicoccoides chromosome substitution lines. Crop Sci 42:637–642

    Google Scholar 

  • Tadesse W, Hsam SLK, Zeller FJ (2006) Evaluation of common wheat cultivars for tan spot resistance and chromosomal location of a resistance gene in the cultivar ‘Salamouni’. Plant Breeding 125:318–322

    Google Scholar 

  • Tadesse W, Reents HJ, Hsam SLK, Zeller FJ (2010) Monosomic analysis of tan spot resistance gene in the winter wheat cultivar ‘Arina’. Plant Breeding 129:477–479

    CAS  Google Scholar 

  • Torada A, Koike M, Mochida K, Ogihara Y (2006) SSR-based linkage map with new markers using a population of common wheat. Theor Appl Genet 112:1042–1051

    CAS  PubMed  Google Scholar 

  • Virdi SK, Liu ZH, Overlander ME, Zhang ZC, Xu SS, Friesen TL, Faris JD (2016) New insights into the roles of host gene-necrotrophic effector interactions in governing susceptibility of durum wheat to tan spot and Septoria nodorum blotch. Genes Genomes Genetics 6:1. https://doi.org/10.1534/g3.116.036525

    Article  CAS  Google Scholar 

  • Zhang ZC, Friesen TL, Simons KJ, Xu SS, Faris JD (2009) Development, identification, and validation of markers for marker-assisted selection against Stagonospora nodorum toxin sensitivity genes Tsn1 and Snn2 in wheat. Mol Breed 23:35–49

    Google Scholar 

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Acknowledgements

The authors thank Shirley Zhong for technical assistance. This work was supported by USDA-Agricultural Research Service CRIS project 3060-21000-038-00D. This material is based upon work supported, in part, by the National Institute of Food and Agriculture, United States Department of Agriculture (USDA), under Hatch project number ND02224.

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Authors and Affiliations

  1. Northern Crop Science Laboratory, Cereal Crops Research Unit, Edward T. Schafer Agricultural Research Center, USDA-Agricultural Research Service, 1616 Albrecht Blvd. North, Fargo, ND, 58102-2765, USA

    Justin D. Faris, Megan E. Overlander & Steven S. Xu

  2. Department of Plant Pathology, North Dakota State University, 306 Walster Hall, Fargo, ND, 58105, USA

    Gayan K. Kariyawasam & Zhaohui Liu

  3. Department of Crop and Soil Sciences, Washington State University, Pullman, WA, 99164, USA

    Arron Carter

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  1. Justin D. Faris
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  2. Megan E. Overlander
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  3. Gayan K. Kariyawasam
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  4. Arron Carter
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  5. Steven S. Xu
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  6. Zhaohui Liu
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Contributions

JF and ZL initiated the study and designed the experiment. JF, SX and AC developed and/or maintained the mapping populations and genetic stocks. JF, MO, GK, and AC conducted mapping studies and/or contributed marker information and marker analysis. MO developed STARP markers. JF, MO, and GK conducted linkage analysis. ZH, MO, and GK conducted tan spot inoculations and analysis. JF and ZH wrote the manuscript and all authors contributed to the final version.

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Correspondence to Justin D. Faris or Zhaohui Liu.

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Communicated by Thomas Miedaner.

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Faris, J.D., Overlander, M.E., Kariyawasam, G.K. et al. Identification of a major dominant gene for race-nonspecific tan spot resistance in wild emmer wheat. Theor Appl Genet 133, 829–841 (2020). https://doi.org/10.1007/s00122-019-03509-8

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