Skip to main content
SpringerLink
Log in

Inverse gene-for-gene interactions contribute additively to tan spot susceptibility in wheat

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Tan spot susceptibility is conferred by multiple interactions of necrotrophic effector and host sensitivity genes.

Abstract

Tan spot of wheat, caused by Pyrenophora tritici-repentis, is an important disease in almost all wheat-growing areas of the world. The disease system is known to involve at least three fungal-produced necrotrophic effectors (NEs) that interact with the corresponding host sensitivity (S) genes in an inverse gene-for-gene manner to induce disease. However, it is unknown if the effects of these NE–S gene interactions contribute additively to the development of tan spot. In this work, we conducted disease evaluations using different races and quantitative trait loci (QTL) analysis in a wheat recombinant inbred line (RIL) population derived from a cross between two susceptible genotypes, LMPG-6 and PI 626573. The two parental lines each harbored a single known NE sensitivity gene with LMPG-6 having the Ptr ToxC sensitivity gene Tsc1 and PI 626573 having the Ptr ToxA sensitivity gene Tsn1. Transgressive segregation was observed in the population for all races. QTL mapping revealed that both loci (Tsn1 and Tsc1) were significantly associated with susceptibility to race 1 isolates, which produce both Ptr ToxA and Ptr ToxC, and the two genes contributed additively to tan spot susceptibility. For isolates of races 2 and 3, which produce only Ptr ToxA and Ptr ToxC, only Tsn1 and Tsc1 were associated with tan spot susceptibility, respectively. This work clearly demonstrates that tan spot susceptibility in this population is due primarily to two NE–S interactions. Breeders should remove both sensitivity genes from wheat lines to obtain high levels of tan spot resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

LOD:

Log of odds ratio

QTL:

Quantitative trait locus

MAS:

Marker-assisted selection

MIM:

Multiple interval mapping

NE:

Necrotrophic effector

RIL:

Recombinant inbred line

Ptr :

Pyrenophora tritici-repentis

S :

Sensitivity gene

SNP:

Single-nucleotide polymorphism

SSR:

Simple sequence repeat

Tsn :

Tan spot necrosis

Tsc :

Tan spot chlorosis

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

    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 

  • 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, 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, Zhang Z, Rasmussen JB, Friesen TL (2011) Variable expression of the Stagonospora nodorum effector SnToxA among isolates is correlated with levels of disease in wheat. Mol Plant Microbe Interact 24:1419–1426

    Article  CAS  PubMed  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 

  • Figueroa M, Manning VA, Pandelova I, Ciuffetti LM (2015) Persistence of the host-selective toxin Ptr ToxB in the apoplast. Mol Plant Microbe Interact 28:1082–1090

    Article  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

    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 

  • 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. North Dakota Agric Exp Station, 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 

  • 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  PubMed  Google Scholar 

  • Knot DR (1990) Near-isogenic lines of wheat carrying genes for stem rust resistance. Crop Sci 30:901–905

    Article  Google Scholar 

  • Lamari L, Bernier CC (1989a) Toxin of Pyrenophora tritici-repentis: host specificity, significance in disease, and inheritance of host reaction. Phytopathology 79:740–744

    Article  CAS  Google Scholar 

  • Lamari L, Bernier CC (1989b) 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 

  • Liu ZH, Friesen TL, Rasmussen JB, Ali S, Meinhardt SW, Faris JD (2004) Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat. Phytopathology 94:1061–1067

    Article  CAS  PubMed  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 

  • 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

    Article  PubMed  PubMed Central  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 

  • 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 

  • Nyarko A, Singarapu KK, Figueroa M, Manning VA, Pandelova I, Wolpert TJ, Ciuffetti LM, Barbar E (2014) Solution NMR structures of Pyrenophora tritici-repentis ToxB and its inactive homolog reveal potential determinants of toxin activity. J Biol Chem 289:25946–25956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Orolaza NP, Lamari L, Ballance GM (1995) Evidence of a host-specific chlorosis toxin from Pyrenophora tritici-repentis, the causal agent of tan spot of wheat. Phytopathology 85:1282–1287

    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 

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

    Article  Google Scholar 

  • Shi G, Friesen TL, Saini J, Xu SS, Rasmussen JB, Faris JD (2015) The wheat Snn7 gene confers susceptibility on recognition of the Parastagonospora nodorum necrotrophic effector SnTox7. Plant Genome 8:2. doi:10.3835/plantgenome2015.02.0007

    Article  Google Scholar 

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

    Article  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  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. G3. doi:10.1534/g3.116.036525

    PubMed  PubMed Central  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 

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

    Article  Google Scholar 

  • Zurn JD, Newcomb M, Rouse MN, Jin Y, Chao S, Sthapit I, See DR, Wanyera R, Bonman JM, Brueggeman RB, Acevedo M (2014) High-density mapping of a resistance gene to Ug99 from the Iranian landrace PI 626573. Mol Breed 34:871–881

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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 LMPG-6/PI 626573 population was funded by the North Dakota Wheat Commission.

Author information

Authors and Affiliations

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

    Zhaohui Liu, Jason D. Zurn, Gayan Kariyawasam, Gongjun Shi, Jana Hansen, Jack B. Rasmussen & Maricelis Acevedo

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

    Justin D. Faris

Authors
  1. Zhaohui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jason D. Zurn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gayan Kariyawasam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Justin D. Faris
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gongjun Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jana Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jack B. Rasmussen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maricelis Acevedo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhaohui Liu.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest for this article.

Ethical standards

All experiments complied with the ethical standards of the university.

Additional information

Communicated by Evans Lagudah.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Z., Zurn, J.D., Kariyawasam, G. et al. Inverse gene-for-gene interactions contribute additively to tan spot susceptibility in wheat. Theor Appl Genet 130, 1267–1276 (2017). https://doi.org/10.1007/s00122-017-2886-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-2886-4

Keywords

Search

Navigation