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Identification of quantitative trait loci conferring resistance to tan spot in a biparental population derived from two Nebraska hard red winter wheat cultivars

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Abstract

Tan spot, caused by Pyrenophora tritici-repentis (Ptr), is a destructive foliar disease in all types of cultivated wheat worldwide. Genetics of tan spot resistance in wheat is complex, involving insensitivity to fungal-produced necrotrophic effectors (NEs), major resistance genes, and quantitative trait loci (QTL) conferring race-nonspecific and race-specific resistance. The Nebraska hard red winter wheat (HRWW) cultivar ‘Wesley’ is insensitive to Ptr ToxA and highly resistant to multiple Ptr races, but the genetics of resistance in this cultivar is unknown. In this study, we used a recombinant inbred line (RIL) population derived from a cross between Wesley and another Nebraska cultivar ‘Harry’ (Ptr ToxA sensitive and highly susceptible) to identify QTL associated with reaction to tan spot caused by multiple races/isolates. Sensitivity to Ptr ToxA conferred by the Tsn1 gene was mapped to chromosome 5B as expected. The Tsn1 locus was a major susceptibility QTL for the race 1 and race 2 isolates, but not for the race 2 isolate with the ToxA gene deleted. A second major susceptibility QTL was identified for all the Ptr ToxC-producing isolates and located to the distal end of the chromosome 1A, which likely corresponds to the Tsc1 locus. Three additional QTL with minor effects were identified on chromosomes 7A, 7B, and 7D. This work indicates that both Ptr ToxA-Tsn1 and Ptr ToxC-Tsc1 interactions are important for tan spot development in winter wheat, and Wesley is highly resistant largely due to the absence of the two tan spot sensitivity genes.

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Abbreviations

LOD:

Log of odds ratio

QTL:

Quantitative trait locus

MAS:

Marker-assisted selection

NE:

Necrotrophic effector

RIL:

Recombinant inbred line

Ptr :

Pyrenophora tritici-repentis

S :

Sensitivity gene

SNP:

Single-nucleotide polymorphism

Tsn :

Tan spot necrosis

Tsc :

Tan spot chlorosis

References

  • Abeysekara NS, Friesen TL, Keller B, Faris JD (2009) Identification and characterization of a novel host–toxin interaction in the wheat–Stagonospora nodorum pathosystem. Theor Appl Genet 120:117–126

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ali S, Gurung S, Adhikari TB (2010) Identification and characterization of novel isolates of Pyrenophora tritici-repentis from Arkansas. Plant Dis 94:229–235

    Article  CAS  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 genes in wheat. Theor Appl Genet 117:873–881

    Article  CAS  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 Breed 25:327–338

    Article  CAS  Google Scholar 

  • Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP (2010) Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction. New Phytol 187:911–919

    Article  CAS  Google Scholar 

  • Dinglasan EG, Godwin ID, Phan HT, Tan KC, Platz GJ, Hickey LT (2018) Vavilov wheat accessions provide useful sources of resistance to tan spot (syn. Yellow spot) of wheat. Plant Pathol 67:1076–1087

    Article  Google Scholar 

  • Effertz RJ, Anderson JA, Francl LJ (2001) Restriction fragment length polymorphism mapping of resistance to two races of Pyrenophora tritici-repentis in adult and seedling wheat. Phytopathology 91:572–578

    Article  CAS  Google Scholar 

  • Effertz RJ, Meinhardt SW, Anderson JA, Jordahl JG, Francl LJ (2002) Identification of a chlorosis-inducing toxin from Pyrenophora tritici-repentis and the chromosomal location of an insensitivity locus in wheat. Phytopathology 92:527–533

    Article  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

    Article  CAS  Google Scholar 

  • Faris JD, Anderson JA, Francl LJ, Jordahl JG (1996) Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture filtrate from Pyrenophora tritici-repentis. Phytopathology 86:459–463

    Article  CAS  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

    Article  CAS  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 U S A 107:13544–13549

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Friesen TL, Faris JD (2010) Characterization of the wheat-Stagonospora nodorum disease system: what is the molecular basis of this quantitative necrotrophic disease interaction? Can J Plant Pathol 32:20–28

    Article  CAS  Google Scholar 

  • Friesen TL, Rasmussen JB, Kwon CY, Francl LJ, Meinhardt SW (2002) Reaction of Ptr ToxA-insensitive wheat mutants to Pyrenophora tritici-repentis race. Phytopathol 92:38–42

    Article  CAS  Google Scholar 

  • Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956

    Article  CAS  Google Scholar 

  • Friskop A, Liu Z (2016) Fungal leaf spot diseases of wheat: tan spot, Stagonospora nodorum blotch and Septoria tritici blotch. NDSU Extension Service, North Dakota State University, Fargo (revised)

  • Hosford RM Jr (1982) Tan spot-developing knowledge 1902–1981, virulent races and differentials, methodology, rating systems, other leaf diseases, literature. In: Hosford RM Jr (ed) Tan spot of wheat and related diseases workshop. ND Agric Exp Stn, Fargo, pp 1–24

    Google Scholar 

  • Hussain W, Baenziger PS, Belamkar V, Guttieri MJ, Venegas JP, Easterly A, Sallam A, Poland J (2017) Genotyping-by-sequencing derived high-density linkage map and its application to QTL mapping of flag leaf traits in bread wheat. Sci Rep 7:16394. https://doi.org/10.1038/s41598-017-16006-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

  • Kollers S, Rodemann B, Ling J, Korzun V, Ebmeyer E, Argillier O, Hinze M, Plieske J, Kulosa D, Ganal MW, Röder MS (2014) Genome-wide association mapping of tan spot resistance (Pyrenophora tritici-repentis) in European winter wheat. Mol Breed 34:363–371

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Levene H (1960) Robust tests for equality of variances. In: Olkin I, Ghurye SH, Hoeffding W, Madow WG, Maan HB (eds) Contributions to probability and statistics: essays in honor of Harold Hotelling. Stanford University Press, Stanford, pp 278–292

    Google Scholar 

  • Liu ZH, Faris JD, Oliver RP, Tan K, Solomon PS, Mcdonald MC, Mcdonald BA, Nunez A, Lu S, Rasmussen JB, Friesen TL (2009) SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathog 5:1–15

    CAS  Google Scholar 

  • Liu ZH, El-Basyoni I, Kariyawasam G, Zhang G, Fritz A, Hansen JM, Marais F, Friskop AJ, Chao S, Akhunov E, Baenziger PS (2015) Evaluation and association mapping of resistance to tan spot and Stagonospora nodorum blotch in adapted winter wheat germplasm. Plant Dis 99:1333–1341

    Article  CAS  Google Scholar 

  • Liu Z, Zurn JD, Kariyawasam G, Faris JD, Shi G, Hansen J, Rasmussen JB, Acevedo M (2017) Inverse gene-for-gene interactions contribute additively to tan spot susceptibility in wheat. Theor Appl Genet 6:1267–1276

    Article  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Manning VA, Ciuffetti LM (2015) Necrotrophic effector epistasis in the Pyrenophora tritici-repentis-wheat interaction. PLoS One 10(4):e0123548. https://doi.org/10.1371/journal.pone.0123548

    Article  Google Scholar 

  • Martinez JP, Oesch NW, Ciuffetti LM (2004) Characterization of the multiple-copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis. Mol Plant-Microbe Interact 17:467–474

    Article  CAS  Google Scholar 

  • Mereno MV, Stenglein S, Perello AE (2015) Distribution of races and Tox genes in Pyrenophora tritici-repentis isolates from wheat in Argentina. Trop Plant Pathol 40:141–146

    Article  Google Scholar 

  • Moffat CS, See PT, Oliver RP (2014) Generation of a ToxA knockout strain of the wheat tan spot pathogen Pyrenophora tritici-repentis. Mol Plant Pathol 15:918–926

    CAS  PubMed  Google Scholar 

  • Murray GM, Brennan JP (2009) Estimating disease losses to the Australian wheat industry. Australas Plant Pathol 38:558–570

    Article  Google Scholar 

  • Noriel AJ, Sun XC, Bockus W, Bai G (2011) Resistance to tan spot and insensitivity to Ptr ToxA in wheat. Crop Sci 51:1059–1067

    Article  Google Scholar 

  • Oliver RP, Friesen TL, Faris JD, Solomon PS (2012) Stagonospora nodorum: from pathology to genomics and host resistance. Annu Rev Phytopathol 50:23–43

    Article  CAS  Google Scholar 

  • Patel JS, Mamidi S, Bonman JM, Adhikari TB (2013) Identification of QTL in spring wheat associated with resistance to a novel isolate of Pyrenophora tritici-repentis. Crop Sci 53:842–852

    Article  CAS  Google Scholar 

  • Peel MD, Anderson JA, Rasmussen JB, Miller JD, Olsen TC, Johnson GW (2004) Registration of ‘Jerry’ wheat. Crop Sci 44:1026–1027

    Article  Google Scholar 

  • Rees RG, Platz GJ, Mayer RJ (1982) Yield losses in wheat from yellow spot: comparison of estimates derived from single tillers and plots. Aust J Agric Res 33:899–908

    Article  Google Scholar 

  • SAS Institute (2016) SAS/IML 9.4 User’s Guide. SAS Institute, Cary

    Google Scholar 

  • Schilder AMC, Bergstrom GC (1994) Infection of wheat seed by Pyrenophora tritici-repentis. Can J Bot 72:510–519

    Article  Google Scholar 

  • See PT, Marathamuthu KA, Iagallo EM, Oliver RP, Moffat CS (2018) Evaluating the importance of the tan spot ToxA–Tsn1 interaction in Australian wheat varieties. Plant Pathol 67:1066–1075

    Article  CAS  Google Scholar 

  • Singh PK, Mergoum M, Ali S, Adhikari TB, Elias EM, Anderson JA, Glover KD, Berzonsky WA (2006a) Evaluation of elite wheat germ plasm for resistance to tan spot. Plant Dis 90:1320–1325

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Snedecor GW, Cochran WG (1989) Statistical methods, 8th edn. Iowa State University Press, Ames

    Google Scholar 

  • Strelkov SE, Lamari L (2003) Host-parasite interactions in tan spot (Pyrenophora tritici-repentis) of wheat. Can J Plant Pathol 25:339–349

    Article  CAS  Google Scholar 

  • Strelkov SE, Lamari L, Ballance GM (1999) Characterization of a host-specific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Mol Plant-Microbe Interact 12:728–732

    Article  CAS  Google Scholar 

  • Sun X-C, Bockus WW, Bai GH (2010) Quantitative trait loci for resistance to Pyrenophora tritici-repentis race 1 in a Chinese wheat. Phytopathology 100:468–473

    Article  Google Scholar 

  • Tadesse W, Hsam SLK, Wenzel G, Zeller FJ (2006a) Identification and monosomic analysis of tan spot resistance genes in synthetic wheat lines (Triticum turgidum L. × Aegilops tauschii Coss.). Crop Sci 46:1212–1217

    Article  Google Scholar 

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

    Article  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. G3 6:4139-4150. https://doi.org/10.1534/g3.116.036525

    Article  CAS  Google Scholar 

Download references

Funding

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. The development and genotyping of the Harry/Wesley population was partially supported by the Nebraska Agricultural Experiment Station with funding from the Hatch Act (Accession Number 0232571) through the USDA National Institute of Food and Agriculture and other USDA-NIFA grants.

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Authors and Affiliations

  1. Department of Plant Pathology, North Dakota State University, Fargo, ND, 58102, USA

    Gayan K. Kariyawasam, Jack B. Rasmussen & Zhaohui Liu

  2. Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE, 68583, USA

    Waseem Hussain, Amanda Easterly, Vikas Belamkar, Jorge Venegas & Stephen Baenziger

  3. Hard Winter Wheat Genetics Research Unit, Center for Grain and Animal Health Research, USDA-ARS, Manhattan, KS, 66502, USA

    Mary Guttieri

  4. Wheat Genetics Resource Center, Department of Plant Pathology, Kansas State University, Manhattan, KS, 66506, USA

    Jesse Poland

  5. Department of Plant Sciences, North Dakota State University, Fargo, ND, 58102, USA

    Francois Marais

Authors
  1. Gayan K. Kariyawasam
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  2. Waseem Hussain
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  3. Amanda Easterly
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  4. Mary Guttieri
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  5. Vikas Belamkar
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  6. Jesse Poland
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  7. Jorge Venegas
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  8. Stephen Baenziger
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  9. Francois Marais
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  10. Jack B. Rasmussen
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  11. Zhaohui Liu
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Correspondence to Zhaohui Liu.

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All experiments complied with the ethical standards of the university.

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Kariyawasam, G.K., Hussain, W., Easterly, A. et al. Identification of quantitative trait loci conferring resistance to tan spot in a biparental population derived from two Nebraska hard red winter wheat cultivars. Mol Breeding 38, 140 (2018). https://doi.org/10.1007/s11032-018-0901-3

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