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Identification and characterization of a novel host–toxin interaction in the wheat–Stagonospora nodorum pathosystem

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Abstract

Stagonospora nodorum, casual agent of Stagonospora nodorum blotch (SNB) of wheat, produces a number of host-selective toxins (HSTs) known to be important in disease. To date, four HSTs and corresponding host sensitivity genes have been reported, and all four host–toxin interactions are significant factors in the development of disease. Here, we describe the identification and partial characterization of a fifth S. nodorum produced HST designated SnTox4. The toxin, estimated to be 10–30 kDa in size, was found to be proteinaceous in nature. Sensitivity to SnTox4 is governed by a single dominant gene, designated Snn4, which mapped to the short arm of wheat chromosome 1A in a recombinant inbred (RI) population. The compatible Snn4–SnTox4 interaction is light dependent and results in a mottled necrotic reaction, which is different from the severe necrosis that results from other host–toxin interactions in the wheat–S. nodorum pathosystem. QTL analysis in a population of 200 RI lines derived from the Swiss winter wheat varieties Arina and Forno revealed a major QTL for SNB susceptibility that coincided with the Snn4 locus. This QTL, designated QSnb.fcu-1A, explained 41.0% of the variation in disease on leaves of seedlings indicating that a compatible Snn4–SnTox4 interaction plays a major role in the development of SNB in this population. Additional minor QTL detected on the short arms of chromosomes 2A and 3A accounted for 5.4 and 6.0% of the variation, respectively. The effects of the three QTL were largely additive, and together they explained 50% of the total phenotypic variation. These results provide further evidence that host–toxin interactions in the wheat–S. nodorum pathosystem follow an inverse gene-for-gene model.

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References

  • Ballance GM, Lamari L, Bernier CC (1989) Purification of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiol Mol Plant Pathol 35:203–213

    Article  CAS  Google Scholar 

  • Barthe P, Pujade-Renaud V, Breton F, Gargani D, Thai R, Roumestand C, de Lamotte F (2007) Structural analysis of cassiicolin, a host-selective protein toxin from Corynespora cassiicola. J Mol Biol 367:89–101

    Article  CAS  PubMed  Google Scholar 

  • Bostwick DE, Ohm HW, Shaner G (1993) Inheritance of Septoria nodorum blotch resistance in wheat. Crop Sci 33:439–443

    Google Scholar 

  • Du CG, Nelson LR, McDaniel ME (1999) Diallel analysis of gene effects conditioning resistance to Stagonospora nodorum (Berk) in wheat. Crop Sci 39:686–690

    Article  Google Scholar 

  • Effertz RJ, Meinhardt SW, Anderson JA, Jordahl JG, Francl LJ (2002) Identification of 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 

  • Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS (2004) Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res 32:3546–3565

    Article  CAS  PubMed  Google Scholar 

  • Faris JD, Friesen TL (2009) Reevaluation of a tetraploid wheat population indicates that the Tsn1-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathology 99:906–912

    Article  CAS  PubMed  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, Li WL, Liu DJ, Chen PD, Gill BS (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor Appl Genet 98:219–225

    Article  CAS  Google Scholar 

  • Faris JD, Haen KM, Gill BS (2000) Saturation mapping of a gene-rich recombination hotspot region in wheat. Genetics 154:823–835

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fried PM, Meister E (1987) Inheritances of leaf and head resistance of winter wheat to Septoria nodorum in a diallel cross. Phytopathology 86:459–463

    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 38:935–956

    Article  CAS  Google Scholar 

  • 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. Plant J 51:681–692

    Article  CAS  PubMed  Google Scholar 

  • Friesen TL, Faris JD, Solomon PS, Oliver RP (2008a) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10:1421–1428

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 146:682–693

    Article  CAS  PubMed  Google Scholar 

  • Friesen TL, Chu CG, Liu ZH, Xu SS, Halley S, Faris JD (2009) Host-selective toxins produced by Stagonospora nodorum confer disease susceptibility in adult plants under field conditions. Theor Appl Genet 118:1489–1497

    Article  CAS  PubMed  Google Scholar 

  • Haen KM, Lu HJ, Friesen TL, Faris JD (2004) Genomic targeting and high-resolution mapping of the Tsn1 gene in wheat. Crop Sci 44:951–962

    CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Liu ZH, Faris JD, Meinhardt SW, Ali S, Rasmussen JB, Friesen TL (2004a) Genetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum. Phytopathology 94:1056–1060

    Article  CAS  PubMed  Google Scholar 

  • Liu ZH, Friesen TL, Rasmussen JB, Ali S, Meinhardt SW, Faris JD (2004b) 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 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

    Article  CAS  PubMed  Google Scholar 

  • Lu HJ, Faris JD (2006) Macro- and microcolinearity between the genomic region of wheat chromosome 5B containing the Tsn1 gene and the rice genome. Funct Integr Genomics 6:90–103

    Article  CAS  PubMed  Google Scholar 

  • Lu HJ, Fellers JP, Friesen TL, Meinhardt SW, Faris JD (2006) Genomic analysis and marker development for the Tsn1 locus in wheat using bin-mapped ESTs and flanking BAC contigs. Theor Appl Genet 112:1132–1142

    Article  CAS  PubMed  Google Scholar 

  • Manly KK Jr, Cudmore HH, Meer JM (2001) MAP MANAGER QTX, cross platform software for genetic mapping. Mamm Genome 12:930–932

    Article  CAS  PubMed  Google Scholar 

  • Manning VA, Ciuffetti LM (2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17:3203–3212

    Article  CAS  PubMed  Google Scholar 

  • McDonald BA, Linde C (2002) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124:163–180

    Article  CAS  Google Scholar 

  • Paillard S, Schnurbusch T, Winzeler M, Messmer M, Sourdille P, Abderhalden O, Keller B, Schachermayr G (2003) An integrative genetic linkage map of winter wheat (Triticum aestivum L). Theor Appl Genet 107:1235–1242

    Article  CAS  PubMed  Google Scholar 

  • Panaccione DG, Scott-Craig JS, Pocard JA, Walton JD (1992) A cyclic peptide synthetase gene required for pathogenicity of the fungus Cochliobolus carbonum on maize. Proc Natl Acad Sci USA 89:6590–6594

    Article  CAS  PubMed  Google Scholar 

  • Parada RY, Sakuno E, Mori N, Oka K, Egusa M, Kodama M, Otani H (2008) Alternaria bassicae produces a host-specific protein toxin from germinating spores on host leaves. Phytopathology 98:458–463

    Article  CAS  PubMed  Google Scholar 

  • Peng JH, Zadeh H, Lazo GR, Gustafson JP, Chao S, Anderson OD, Qi LL, Echalier B, Gill BS, Dilbirligi M, Sandhu D, Gill KS, Greene RA, Sorrells ME, Akhunov ED, Dvorak J, Linkiewicz AM, Dubcovsky J, Hossain KG, Kalayacharla V, Kianian SF, Mohmoud AA, Miftahudin, Conley EJ, Anderson JA, Pathan MS, Nguyen HT, McGuire PE, Qualset CO, Lapitan NLV (2004) Chromosome bin map of expressed sequence tags in homoeologous group 1 of hexaploid wheat and homoeology with rice and Arabidopsis. Genetics 168:609–623

  • Qi LL, Echalier B, Chao S, Lazo GR, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Eryman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma X-F, Miftahudin, Gustafson JP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharl V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi D-W, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16, 000 EST loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

  • Reddy L, Friesen TL, Meinhardt SW, Chao S, Faris JD (2008) Genomic analysis of the Snn1 locus on wheat chromosome arm 1BS and the identification of candidate genes. Plant Genome 1:55–66

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers Methods. Mol Biol 132:365–386

    CAS  Google Scholar 

  • Sandhu D, Champoux JA, Bondareva SN, Gill KS (2001) Identification and physical localization of useful genes and markers to major gene-rich regions on wheat group 1S chromosomes. Genetics 157:1735–1747

    CAS  PubMed  Google Scholar 

  • Sarpeleh A, Wallwork H, Catcheside DEA, Tate ME, Able AJ (2007) Proteinaceous metabolites from Pyrenophora teres contribute to symptom development of barley net blotch. Phytopathology 97:907–915

    Article  CAS  PubMed  Google Scholar 

  • Schnurbusch T, Paillard S, Fossati D, Messmer M, Schachermayr G, Winzeler M, Keller B (2003) Detection of QTLs for Stagonospora glume blotch resistance in Swiss winter wheat. Theor Appl Genet 107:1226–1234

    Article  CAS  PubMed  Google Scholar 

  • Schnurbusch T, Bossolini E, Messmer M, Keller B (2004) Tagging and validation of a major quantitative trait locus for leaf rust resistance and leaf tip necrosis in winter wheat cultivar Forno. Phytopathology 94:1036–1041

    Article  CAS  PubMed  Google Scholar 

  • Strelkov SE, Lamari L, Balance GM (1998) Induced chlorophyll degradation by a chlorosis toxin from Pyrenophora tritici-repentis. Can J Plant Pathol 20:428–435

    CAS  Google Scholar 

  • Tomas A, Feng GH, Reeck GR, Bockus WW, Leach JE (1990) Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol Plant Microbe Interact 3:221–224

    CAS  Google Scholar 

  • Tommasini L, Schnurbusch T, Fossati D, Mascher F, Keller B (2007) Association mapping of Stagonospora nodorum blotch resistance in modern European winter wheat varieties. Theor Appl Genet 115:697–708

    Article  CAS  PubMed  Google Scholar 

  • Tuori RP, Wolpert TJ, Ciuffetti LM (1995) Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Mol Plant Microbe Interact 8:41–48

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Xu SS, Friesen TL, Cai X (2004) Sources and genetic control of resistance to Stagonospora nodorum blotch in wheat. Recent Res Dev Genet Breed 1:449–469

    Google Scholar 

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Acknowledgments

This research was supported by USDA-ARS CRIS projects 5442-21000-033 and 5442-22000-037, and Swiss SNF grant 105620.

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Correspondence to Justin D. Faris.

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Communicated by M. Sorrells.

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Abeysekara, N.S., Friesen, T.L., Keller, B. et al. Identification and characterization of a novel host–toxin interaction in the wheat–Stagonospora nodorum pathosystem. Theor Appl Genet 120, 117–126 (2009). https://doi.org/10.1007/s00122-009-1163-6

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  • DOI: https://doi.org/10.1007/s00122-009-1163-6

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