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Genetic relationships between race-nonspecific and race-specific interactions in the wheat–Pyrenophora tritici-repentis pathosystem

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Abstract

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We identified a major QTL conferring race-nonspecific resistance and revealed its relationships with race-specific interactions in the wheat– Pyrenophora tritici - repentis pathosystem.

Abstract

Tan spot, caused by the fungus Pyrenophora tritici-repentis (Ptr), is a destructive disease of wheat worldwide. The disease system is known to include inverse gene-for-gene, race-specific interactions involving the recognition of fungal-produced necrotrophic effectors (NEs) by corresponding host sensitivity genes. However, quantitative trait loci (QTLs) conferring race-nonspecific resistance have also been identified. In this work, we identified a major race-nonspecific resistance QTL and characterized its genetic relationships with the NE-host gene interactions Ptr ToxA-Tsn1 and Ptr ToxC-Tsc1 in a recombinant inbred wheat population derived from the cross between ‘Louise’ and ‘Penawawa.’ Both parental lines were sensitive to Ptr ToxA, but Penawawa and Louise were highly resistant and susceptible, respectively, to conidial inoculations of all races. Resistance was predominantly governed by a major race-nonspecific QTL on chromosome arm 3BL for resistance to all races. Another significant QTL was detected at the distal end of chromosome arm 1AS for resistance to the Ptr ToxC-producing isolates, which corresponded to the known location of the Tsc1 locus. The effects of the 3B and 1A QTLs were largely additive, and the 3B resistance QTL was epistatic to the Ptr ToxA-Tsn1 interaction. Resistance to race 2 in F1 plants was completely dominant; however, race 3-inoculated F1 plants were only moderately resistant because they developed chlorosis presumably due to the Ptr ToxC-Tsc1 interaction. This work provides further understanding of genetic resistance in the wheat-tan spot system as well as important guidance for tan spot resistance breeding.

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Abbreviations

CIM:

Composite interval mapping

ETI:

Effector-triggered immunity

NETS:

Necrotrophic effector-triggered susceptibility

HST:

Host-selective toxin

ITMI:

International triticeae mapping initiative

LOD:

Log of odds ratio

QTL:

Quantitative trait locus

MAS:

Marker assisted selection

NE:

Necrotrophic effector

RIL:

Recombinant inbred line

Ptr :

Pyrenophora tritici-repentis

SNP:

Single nucleotide polymorphism

SSR:

Simple sequence repeat

SWSW:

Soft white spring wheat

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  PubMed  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 

  • Beecher BS, Carter AH, See DR (2012) Genetic mapping of new seed-expressed polyphenol oxidase genes in wheat (Triticum aestivum L.). Theor Appl Genet 124:1463–1473

    Article  CAS  PubMed  Google Scholar 

  • Carter AH, Chen XM, Garland-Campbell K, Kidwell KK (2009) Identifying QTL for high-temperature adult-plant resistance to stripe rust (Puccinia striiformis f. sp. tritici) in the spring wheat (Triticum aestivum L.) cultivar ‘Louise’. Theor Appl Genet 119:1119–1128

    Article  PubMed  Google Scholar 

  • Cheong J, Wallwork H, Williams KJ (2004) Identification of a major QTL for yellow leaf spot resistance in the wheat varieties Brookton and Cranbook. Aust J Agric Res 55:315–319

    Article  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  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 Breed 25:327–338

    Article  CAS  Google Scholar 

  • Ciuffetti LM, Tuori RP, Gaventa JM (1997) A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9:135–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciuffetti LM, Manning VA, Martinez JP, Pandelova I, Andrie RM (2003) Proteinaceous toxins of Pyrenophora tritici-repentis and investigation of the site-of-action of Ptr ToxA. In: Rasmussen JB, Friesen TL, Ali S (eds) Proceedings of the fourth international wheat tan spot and spot blotch workshop. N D Agric Exp Stn, Fargo, pp 96–102

    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  PubMed  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  PubMed  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  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  PubMed  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

    Article  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 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  PubMed  Google Scholar 

  • Faris JD, Zhang QJ, Chao S, Zhang Z, Xu SS (2014) 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

    Article  PubMed  Google Scholar 

  • Flor HH (1956) The complimentary genetics systems in flax and flax rust. Adv Genet 8:29–54

    Article  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  PubMed  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, Ali S, Kianian S, Francl LJ, Rasmussen JB (2003) Role of host sensitivity to Ptr ToxA in development of tan spot of wheat. Phytopathology 93:397–401

    Article  CAS  PubMed  Google Scholar 

  • Friesen TL, Xu SS, Harris MO (2008) Stem rust, tan spot, Stagonospora nodorum blotch, and hessian fly resistance in Langdon durum-synthetic hexaploid wheat lines. Crop Sci 48:1062–1070

    Article  Google Scholar 

  • 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. N D Agric Exp Stn, Fargo, pp 1–24

    Google Scholar 

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

    Article  CAS  PubMed  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) Evaluation 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 

  • Lamari L, Strelkov SE (2010) The wheat/Pyrenophora tritici-repentis interaction: progress towards an understanding of tan spot disease. Can J Plant Pathol 32:4–10

    Article  CAS  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  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Meinhardt SW, Ali S, Ling H, Francl LJ (2003) A new race of Pyrenophora tritici-repentis that produces a putative host-selective toxin. In: Rasmussen JB, Friesen TL, Ali S (eds) Proceedings of the fourth international wheat tan spot and spot blotch workshop. N D Agric Exp Stn, Fargo, pp 117–119

    Google Scholar 

  • Murray GM, Brennan JP (2009) Estimating disease losses to the Australian wheat industry. Aust 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 

  • 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 

  • 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 (2011) SAS/IML 9.3 User’s Guide. SAS Institute, Cary, NC

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

    Article  Google Scholar 

  • Singh PK, Gonzalez-Hernandez JL, Mergoum M, Ali S, Adhikari TB, Kianian SF, Elias EM, 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

    Article  CAS  PubMed  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, Iowa

  • 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  PubMed  Google Scholar 

  • Tadesse W, Hsam SL, 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 

  • Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Ann Rev Phytopathol 40:251–285

    Article  CAS  Google Scholar 

  • Zeng Z-B (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Dr. Qijun Zhang for helping with statistical test of population homogeneity. 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 to Z. Liu and by the National Research Initiative Competitive Grants CAP project 2011-68002-30029 from the USDA National Institute of Food and Agriculture to A.H. Carter.

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  1. Mohamed Mergoum

    Present address: Department of Crop and Soil Sciences, University of Georgia, 1109 Experiment St, Griffin, GA, 30223, USA

Authors and Affiliations

  1. Department of Plant Pathology, North Dakota State University, Fargo, ND, 58108, USA

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

  2. Department of Crop and Soil Science, Washington State University, Pullman, WA, 99164-6420, USA

    Arron H. Carter

  3. USDA-ARS Cereal Crops Research Unit, Northern Crop Science Laboratory, Fargo, 58102, USA

    Justin Faris & Steven S. Xu

  4. Department of Plant Science, North Dakota State University, Fargo, ND, 58108, USA

    Mohamed Mergoum

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  1. Gayan K. Kariyawasam
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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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Communicated by B. Keller.

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Kariyawasam, G.K., Carter, A.H., Rasmussen, J.B. et al. Genetic relationships between race-nonspecific and race-specific interactions in the wheat–Pyrenophora tritici-repentis pathosystem. Theor Appl Genet 129, 897–908 (2016). https://doi.org/10.1007/s00122-016-2670-x

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