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Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis

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Abstract

Pyrenophora tritici-repentis, the causal organism of the necrotrophic foliar wheat disease tan spot [also known as yellow (leaf) spot in Australia] is an important disease in Australia and in many parts of the world. North American isolates of the pathogen have been shown to produce combinations of three host-specific toxins, ToxA, ToxB and ToxC. Each toxin interacts with a host sensitivity locus, respectively Tsn1, Tsc2 and Tsc1. The virulence of an isolate is partially correlated with the presence of these toxins and resistance in the host is associated with absence of the sensitivity loci. Breeding for resistance to tan spot can, therefore, be aided by knowledge of the prevalence of the toxin-encoding genes in local pathogen populations. Two of the toxins, A and B, are encoded by known genes and molecular tests for the genes have been developed. We screened a diverse collection of 119 tan spot isolates collected between 1984 and 2008 and from all affected regions of Australia (Queensland, New South Wales, Victoria and Western Australia). In all cases, the gene for ToxA was present and the gene for ToxB was absent. The implications for resistance breeding and epidemiology of the disease are discussed. We also define a diagnostic molecular marker for P. tritici-repentis.

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References

  • Andrie RM, Pandelova I, Ciuffetti LM (2007) A combination of phenotypic and genotypic characterization strengthens Pyrenophora tritici-repentis race identification. Phytopathology 97, 694–701. doi: 10.1094/PHYTO-97-6-0694

    Article  CAS  PubMed  Google Scholar 

  • Andrie RM, Schoch CL, Hedges R, Spatafora JW, Ciuffetti LM (2008) Homologs of ToxB, a host-selective toxin gene from Pyrenophora tritici-repentis, are present in the genome of sister-species Pyrenophora bromi and other members of the Ascomycota. Fungal Genetics and Biology 45, 363–377. doi: 10.1016/j.fgb.2007.10.014

    Article  CAS  PubMed  Google Scholar 

  • 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. doi: 10.1023/A:1024277420773

    Article  CAS  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379–406. doi: 10.1146/annurev.arplant.57.032905.105346

    Article  CAS  PubMed  Google Scholar 

  • Brennan JP, Murray GM (1998) ‘Economic importance of wheat diseases in Australia.’ (NSW Agriculture: Wagga Wagga)

    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 Cranbrook. Australian Journal of Agricultural Research 55, 315–319. doi: 10.1071/AR03140

    Article  Google Scholar 

  • Ciuffetti LM, Francl LJ, Ballance GM, Bockus WW, Lamari L, Meinhardt SW, Rasmussen JB (1998) Standardization of toxin nomenclature in the Pyrenophora tritici-repentis/wheat interaction. Canadian Journal of Plant Pathology 20, 421–424.

    Article  Google Scholar 

  • Cuomo CA, Güldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M, Adam G, Antoniw J, Baldwin T, Calvo S, Chang YL, Decaprio D, Gale LR, Gnerre S, Goswami RS, Hammond-Kosack K, Harris LJ, Hilburn K, Kennell JC, Kroken S, Magnuson JK, Mannhaupt G, Mauceli E, Mewes HW, Mitterbauer R, Muehlbauer G, Mü nsterkötter M, Nelson D, O’donnell K, Ouellet T, Qi W, Quesneville H, Roncero MI, Seong KY, Tetko IV, Urban M, Waalwijk C, Ward TJ, Yao J, Birren BW, Kistler HC (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 7, 317, 1400–1402. http://blast.jcvi.org/euk-blast/plantta_blast.cgi (for triticum)

    Article  CAS  PubMed  Google Scholar 

  • Effertz RJ, Meinhardt SW, Anderson JA, Jordahl JG, Francl LJ (2002) Identification of a chlorosis-inducing toxin from Pyrenophora triticirepentis and the chromosomal location of an insensitivity locus in wheat. Phytopathology 92, 527–533. doi: 10.1094/PHYTO.2002.92.5.527

    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 necrosisinducing culture filtrate from Pyrenophora tritici-repentis. Phytopathology 86, 459–463. doi: 10.1094/Phyto-86-459

    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. Theoretical and Applied Genetics 109, 464–471. doi: 10.1007/s00122-004-1678-9

    Article  CAS  PubMed  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. Nature Genetics 38, 953–956. doi: 10.1038/ng1839

    Article  CAS  PubMed  Google Scholar 

  • Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cellular Microbiology 10, 1421–1428. doi: 10.1111/j.1462-5822.2008.01153.x

    Article  CAS  PubMed  Google Scholar 

  • 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. doi: 10.1105/tpc.107.052829

    Article  CAS  PubMed  Google Scholar 

  • Hosford RM (1982) Tan spot — developing knowledge 1902–1981, virulent races and wheat differentials, methodology, rating systems, other leaf diseases, literature. In ‘Tan spot of wheat and related diseases workshop’. (Ed. RM Hosford) pp. 1–24. (North Dakota Agricultural Experiment Station: Fargo)

    Google Scholar 

  • Kim YM, Strelkov SE (2007) Heterologous expression and activity of Ptr ToxB from virulent and avirulent isolates of Pyrenophora triticirepentis. Canadian Journal of Plant Pathology 29, 232–242.

    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. Canadian Journal of Plant Pathology 11, 49–56.

    Article  Google Scholar 

  • Lamari L, McCallum BD, DePauw RM (2005a) Forensic pathology of Canadian bread wheat: the case of tan spot. Phytopathology 95, 144–152. doi: 10.1094/PHYTO-95-0144

    Article  PubMed  Google Scholar 

  • Lamari L, Strelkov SE, Yahyaoui A, Amedov M, Saidov M, Djunusova M, Koichibayev M (2005b) Virulence of Pyrenophora tritici-repentis in the countries of the Silk Road. Canadian Journal of Plant Pathology 27, 383–388.

    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. Molecular Plant-Microbe Interactions 17, 467–474. doi: 10.1094/MPMI.2004.17.5.467

    Article  CAS  PubMed  Google Scholar 

  • Mikhailova LA, Ternuk IG, Mironenko NV (2007) Structure of Pyrenophora tritici-repentis populations from European part of Russia by virulence. Mikologiya I Fitopatologiya 41, 269–275.

    Google Scholar 

  • Oliver R (2009) Plant breeding for disease resistance in the age of effectors. Phytoparasitica 37, 1–5.

    Article  Google Scholar 

  • Oliver RP, Lord M, Rybak K, Faris JD, Solomon PS (2008) Emergence of tan spot disease caused by toxigenic Pyrenophora tritici-repentis in Australia is not associated with increased deployment of toxinsensitive cultivars. Phytopathology 98, 488–491. doi: 10.1094/PHYTO-98-5-0488

    Article  CAS  PubMed  Google Scholar 

  • 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. doi: 10.1071/CP08259

    Article  CAS  Google Scholar 

  • Rees RG, Platz GJ (1979) The occurrence and control of yellow spot of wheat in north-eastern Australia. Australian Journal of Experimental Agriculture 19, 369–372. doi: 10.1071/EA9790369

    Article  Google Scholar 

  • Rees RG, Mayer RJ, Platz GJ (1981) Yield losses in wheat from yellow spot: a disease-loss relationship derived from single tillers. Australian Journal of Agricultural Research 32, 851–859. doi: 10.1071/AR9810851

    Article  Google Scholar 

  • Rotmistrovsky K, Jang W, Schuler G (2004) A web server for performing electronic PCR. Nucleic Acids Research 32, W108-W112. doi: 10.1093/nar/gkh450

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S Krawetz, S. Misener) pp. 365–386. (Humana Press: Totowa, NJ)

    Google Scholar 

  • Sarma GN, Manning VA, Ciuffetti LM, Karplus PA (2005) Structure of Ptr ToxA: an RGD-containing host-selective toxin from Pyrenophora tritici-repentis. The Plant Cell 17, 3190–3202. doi: 10.1105/tpc.105.034918

    Article  CAS  PubMed  Google Scholar 

  • Schilder AM, Bergstrom GC (1995) Seed transmission of Pyrenophora tritici-repentis, causal fungus of tan spot of wheat. European Journal of Plant Pathology 101, 81–91. doi: 10.1007/BF01876096

    Article  Google Scholar 

  • Strelkov SE, Lamari L, Ballance GM (1999) Characterization of a hostspecific protein toxin (Ptr ToxB) from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 12, 728–732. doi: 10.1094/MPMI.1999.12.8.728

    Article  CAS  Google Scholar 

  • Tan K-C, Heazlewood JL, Millar AH, Thomson G, Oliver RP, Solomon PS (2008) A signaling-regulated, short-chain dehydrogenase of Stagonospora nodorum regulates asexual development. Eukaryotic Cell 7, 1916–1929. doi: 10.1128/EC.00237-08

    Article  CAS  PubMed  Google Scholar 

  • Tomas A, Bockus WW (1987) Cultivar-specific toxicity of culture filtrates of Pyrenophora tritici-repentis. Phytopathology 77, 1337–1340. doi: 10.1094/Phyto-77-1337

    Article  Google Scholar 

  • Valder PG, Shaw DE (1953) Yellow spot disease of wheat in Australia. Proceedings of the Linnean Society of New South Wales 77, 323–330.

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR protocols’. (Eds DH Innis, DH Gelfand, JJ Sninsky, TJ White) pp. 315–322. (Academic Press: New York)

    Google Scholar 

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Authors and Affiliations

  1. Australian Centre for Necrotrophic Fungal Pathogens, Murdoch University, 6150, Murdoch, WA, Australia

    Eva A. Antoni, Kasia Rybak, Madeline P. Tucker, James K. Hane & Richard P. Oliver

  2. Plant Cell Biology, Research School of Biology, TheAustralian National University, 0200, Canberra, ACT, Australia

    Peter S. Solomon

  3. The University of Queensland, Tree Pathology Centre, 4072, Brisbane, Qld, Australia

    Andre Drenth

  4. Department of Agriculture and Food, 3 Baron Hay Court, 6151, WA, South Perth, Australia

    Manisha Shankar

Authors
  1. Eva A. Antoni
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  2. Kasia Rybak
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  3. Madeline P. Tucker
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  4. James K. Hane
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  5. Peter S. Solomon
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  8. Richard P. Oliver
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Correspondence to Richard P. Oliver.

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Antoni, E.A., Rybak, K., Tucker, M.P. et al. Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis. Australasian Plant Pathology 39, 63–68 (2010). https://doi.org/10.1071/AP09056

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  • DOI: https://doi.org/10.1071/AP09056

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