Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Prevalence and importance of sensitivity to the Stagonospora nodorum necrotrophic effector SnTox3 in current Western Australian wheat cultivars

Ormonde D. C. Waters A , Judith Lichtenzveig A , Kasia Rybak A , Timothy L. Friesen B and Richard P. Oliver A C
+ Author Affiliations
- Author Affiliations

A Australian Centre for Necrotrophic Fungal Pathogens, Department of Agriculture and Environment, Curtin University, Bentley, WA 6102, Australia.

B United States Department of Agriculture – Agricultural Research Service, Cereal Crops Research Unit, Northern Crop Science Lab, 1307 18th Street North, Fargo, ND 58105, USA.

C Corresponding author. Email: Richard.Oliver@curtin.edu.au

Crop and Pasture Science 62(7) 556-562 https://doi.org/10.1071/CP11004
Submitted: 10 January 2011  Accepted: 30 June 2011   Published: 28 July 2011

Abstract

Stagonospora nodorum is a major pathogen of wheat in many parts of the world and particularly in Western Australia. The pathosystem is characterised by interactions of multiple pathogen necrotrophic effectors (NE) (formerly host-specific toxins) with corresponding dominant host sensitivity loci. To date, five NE interactions have been reported in S. nodorum. Two proteinaceous NE (ToxA and SnTox3) have been cloned and expressed in microbial systems. The identification of wheat cultivars lacking sensitivity to one or more NE is a promising way to identify cultivars suitable for use in breeding for increased resistance to this economically important pathogen.

The prevalence of sensitivity to the NE SnTox3 was investigated in 60 current Western Australian-adapted bread wheat (Triticum aestivum L.) cultivars. Infiltration of SnTox3 into seedling leaves caused a moderate or strong necrotic response in 52 cultivars. Six cultivars were insensitive and two cultivars exhibited a weak chlorotic response. Five of the cultivars that were insensitive or weakly sensitive to SnTox3 were noticeably more resistant to the disease. The 60 cultivars gave a very similar reaction to SnTox3 and to the crude S. nodorum SN15 culture filtrate demonstrating that SnTox3 is the dominant NE in this isolate. We conclude that a simple screen using both SnTox3 and ToxA effectors combined with simple greenhouse disease evaluation, will allow breeders to select cultivars that are more resistant to the disease, allowing them to concentrate resources on other still intractable breeding objectives.


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. Theoretical and Applied Genetics 209, 1–10.

Antoni EA, Rybak K, Tucker MP, Hane JK, Solomon PS, Drenth A, Shankar M, Oliver RP (2010) Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis. Australasian Plant Pathology 39, 63–68.
Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFKnsr3I&md5=166f5466393ee7607d285681b013c158CAS |

Bhathal JS, Loughman R, Speijers J (2003) Yield reduction in wheat in relation to leaf disease from yellow (tan) spot and septoria nodorum blotch. European Journal of Plant Pathology 109, 435–443.
Yield reduction in wheat in relation to leaf disease from yellow (tan) spot and septoria nodorum blotch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1OksLs%3D&md5=40e7d57a91805e68149667aa546bc6f8CAS |

Curtis B, Penny S, Zaicou-Kunesch C, Dhammu H, Ellis S, Jorgensen D, Miyan S, Shackley B, Sharma DK (2009) ‘Wheat variety guide 2009 Western Australia. Vol. 4763.’ (DAFWA: Perth)

Faris JD, Friesen TL (2009) Reevaluation of a tetraploid wheat population indicates that the Tsnl-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathology 99, 906–912.
Reevaluation of a tetraploid wheat population indicates that the Tsnl-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvF2iurs%3D&md5=0b54b2123d47dae45602daa7e8c54c3aCAS |

Faris JD, Zhang Z, Lu H, Lu S, 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. Proceedings of the National Academy of Sciences of the United States of America 107, 13544–13549.
A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1GmsLzN&md5=bf104b3591e845ade72e037e5e3f2990CAS |

Friesen TL, Faris JD, Solomon PS, Oliver RP (2008a) Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10, 1421–1428.
Host-specific toxins: effectors of necrotrophic pathogenicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotF2hu7Y%3D&md5=751292883537aec71b386a2213525db7CAS |

Friesen TL, Meinhardt SW, Faris JD (2007) The Stagonospora nodorum-wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. The Plant Journal 51, 681–692.
The Stagonospora nodorum-wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSmtrvE&md5=863c9aab335de0ac94c5d3c278044b15CAS |

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. Nature Genetics 38, 953–956.
Emergence of a new disease as a result of interspecific virulence gene transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVChu7c%3D&md5=7d649e5608451aaa94b6c8f32bf6da78CAS |

Friesen TL, Zhang Z, Solomon PS, Oliver RP, Faris JD (2008b) Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiology 146, 682–693.
Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFCmtLc%3D&md5=9184871ef23c605a96829d164a6a6cd6CAS |

Hane JK, Lowe RGT, Solomon PS, Tan K-C, Schoch CL, Spatafora JW, Crous PW, Kodira C, Birren BW, Galagan JE, Torriani SFF, McDonald BA, Oliver RP (2007) Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. The Plant Cell 19, 3347–3368.
Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1ensA%3D%3D&md5=742c7fe779e3d72e8995f6a44c8215b1CAS |

Liu Z, Faris JD, Oliver RP, Tan K-C, Solomon PS, McDonald BA, Nunez A, Lu S, Rasmussen J, Friesen TL (2009) SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathogens 5, e1000581

Liu Z, Friesen TL, Ling H, Meinhardt SW, Oliver RP, Rasmussen JB, Faris JD (2006) The Tsn1-ToxA interaction in the wheat-Stagonospora nodorum pathosystem parallels that of the wheat-tan spot system. Genome 49, 1265–1273.
The Tsn1-ToxA interaction in the wheat-Stagonospora nodorum pathosystem parallels that of the wheat-tan spot system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVOiu7Y%3D&md5=a4852f397204913ac5bacec0309f3fc9CAS |

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.
Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVCjur0%3D&md5=66c221876dd2a38e20dd385433fbecc4CAS |

Murray GM, Brennan JP (2009) Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology 38, 558–570.
Estimating disease losses to the Australian wheat industry.Crossref | GoogleScholarGoogle Scholar |

Oliver RP (2009) Plant breeding for disease resistance in the age of effectors. Phytoparasitica 37, 1–5.
Plant breeding for disease resistance in the age of effectors.Crossref | GoogleScholarGoogle Scholar |

Oliver RP, Lord M, Rybak K, Faris JD, Solomon PS (2008a) Emergence of tan spot disease caused by toxigenic Pyrenophora tritici-repentis in Australia is not associated with increased deployment of toxin-sensitive cultivars. Phytopathology 98, 488–491.
Emergence of tan spot disease caused by toxigenic Pyrenophora tritici-repentis in Australia is not associated with increased deployment of toxin-sensitive cultivars.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjlslelug%3D%3D&md5=bc9ace6e27b95e8457a56129a12ba7dbCAS |

Oliver RP, Rybak K, Shankar M, Loughman R, Harry N, Solomon PS (2008b) Quantitative disease resistance assessment by real-time PCR using the Stagonospora nodorum-wheat pathosystem as a model. Plant Pathology 57, 527–532.
Quantitative disease resistance assessment by real-time PCR using the Stagonospora nodorum-wheat pathosystem as a model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVOktr8%3D&md5=8dd4e19a786ab3ce007223c2b538bc74CAS |

Oliver RP, Rybak K, Solomon PS, Ferguson-Hunt M (2009) Prevalence of ToxA-sensitive alleles of the wheat gene Tsn1 in Australian and Chinese wheat cultivars Crop & Pasture Science 60, 348–352.
Prevalence of ToxA-sensitive alleles of the wheat gene Tsn1 in Australian and Chinese wheat cultivarsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkslGis7g%3D&md5=d70e0117dff831e85a603a3e1d4d765bCAS |

Oliver RP, Solomon PS (2010) New developments in pathogenicity and virulence of necrotrophs. Current Opinion in Plant Biology 13, 415–419.
New developments in pathogenicity and virulence of necrotrophs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Ojsr0%3D&md5=f30fe835b4dc79d6a3c1b7bf53b1612eCAS |

Shankar M, Walker E, Golzar H, Loughman R, Wilson RE, Francki MG (2008) Quantitative trait loci for seedling and adult plant resistance to Stagonospora nodorum in wheat. Phytopathology 98, 886–893.
Quantitative trait loci for seedling and adult plant resistance to Stagonospora nodorum in wheat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjlslemuw%3D%3D&md5=298c9fe405bb600fc2ad3bd7a391dcdcCAS |

Solomon PS, Lowe RGT, Tan KC, Waters ODC, Oliver RP (2006) Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat. Molecular Plant Pathology 7, 147–156.
Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat.Crossref | GoogleScholarGoogle Scholar |

Solomon PS, Thomas SW, Spanu P, Oliver RP (2003) The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection. Physiological and Molecular Plant Pathology 63, 191–199.
The utilisation of di/tripeptides by Stagonospora nodorum is dispensable for wheat infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivVCqs74%3D&md5=faa1ffacf27560e3791f9587c307c16dCAS |

Stukenbrock EH, McDonald BA (2007) Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Molecular Plant Pathology 8, 321–332.
Geographical variation and positive diversifying selection in the host-specific toxin SnToxA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntFOrtbo%3D&md5=be6728f9c7efe2b158ffefb3644d0697CAS |

Tan KC, Oliver RP, Solomon PS, Moffat CS (2010) Proteinaceous necrotrophic effectors in fungal virulence. Functional Plant Biology 37, 907–912.
Proteinaceous necrotrophic effectors in fungal virulence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFyqt7vO&md5=15a3393c6bef85b8f2edd42129627b2cCAS |

Tuori RP, Wolpert TJ, Ciuffetti LM (2000) Heterologous expression of functional Ptr ToxA. Molecular Plant-Microbe Interactions 13, 456–464.
Heterologous expression of functional Ptr ToxA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFOksbs%3D&md5=940eae743689cdf8850ff912425e868dCAS |

Uphaus J, Walker E, Shankar M, Golzar H, Loughman R, Francki M, Ohm H (2007) Quantitative trait loci identified for resistance to Stagonospora glume blotch in wheat in the USA and Australia. Crop Science 47, 1813–1822.
Quantitative trait loci identified for resistance to Stagonospora glume blotch in wheat in the USA and Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSltbjF&md5=7fd7d5153ab99cca0a74bb6b895cd6b7CAS |

Zaicou-Kunesch C, Penny S, Shackley B, Ellis S, Myian S, Dhammu H, Shankar M, Sharma D (2010) ‘Wheat variety guide 2010 Western Australia.’ (DAFWA: Perth)

Zhang Z, Friesen TL, Xu SS, Shi G, Liu Z, Rasmussen JB, Faris JD (2011) Two putatively homoeologous wheat genes mediate recognition of SnTox3 to confer effector-triggered susceptibility to Stagonospora nodorum. The Plant Journal 65, 27–38.
Two putatively homoeologous wheat genes mediate recognition of SnTox3 to confer effector-triggered susceptibility to Stagonospora nodorum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2rsLc%3D&md5=e1fd544dc2585da2ece408e1745d1fccCAS |