Characterization of the wheat-Stagonospora nodorum disease system: what is the molecular basis of this quantitative necrotrophic disease interaction?^†

References

• Abeysekara , N.S. , Friesen , T.L. , Keller , B. and Faris , J.D. 2009 . Identification and characterization of a novel host-toxin interaction in the wheat – Stagonospora nodorum pathosystem . Theor. Appl. Genet. , doi: 10.1007/s00122-009-1163-6
   Google Scholar
• Ballance , G.M. , Lamari , L. and Bernier , C.C. 1989 . Purification and characterization of a host selective toxin from Pyrenophora tritici-repentis . Physiol. Mol. Plant Pathol. , 35 : 203 – 213 .
   Web of Science ®Google Scholar
• Ballance, G.M., Lamari, L., Kowatsch, R., & Bernier, C.C. (1996). Cloning, expression and occurrence of the gene encoding the Ptr necrosis toxin from Pyrenophora tritici-repentis. Mol. Plant Pathol., online http://www.bspp.org.uk/mppol/1996/1209ballance
   Google Scholar
• Barthe , P. , Pujade-Renaud , V. , Breton , F. , Gargani , D. , Thai , R. , Roumestand , C. and de Lamotte , F. 2007 . Structural analysis of cassiicolin, a host-selective protein toxin from Corynespora cassiicola . J. Mol. Biol. , 369 : 89 – 101 .
   Google Scholar
• Bousquet , J.-F. and Skajennikoff , M. 1974 . Isolement et mode d'action d'une phytotoxine produite en culture par Septoria nodorum Berk . Phytopathol. Zeitsch. , 80 : 355 – 360 .
   Google Scholar
• Chisolm , S.T. , Coaker , G. , Day , B. and Staskawicz , B.J. 2006 . Host-microbe interactions: Shaping the evolution of the plant immune response . Cell , 124 : 803 – 814 .
   Google Scholar
• Ciuffetti , L.M. and Touri , R.P. 1999 . Advances in the characterization of the Pyrenophora tritici-repentis–wheat interaction . Phytopathology , 89 : 444 – 449 .
   PubMed Web of Science ®Google Scholar
• Ciuffetti , L.M. , Touri , R.P. and Gaventa , J.M. 1997 . A single gene encodes a selective toxin causal to the development of tan spot of wheat . Plant Cell , 9 : 135 – 144 .
   PubMed Web of Science ®Google Scholar
• Dangl , J.L. and Jones , J.D.G. 2001 . Plant pathogens and integrated defense responses to infection . Nature , 411 : 826 – 833 .
   PubMed Web of Science ®Google Scholar
• Devys , M. , Bousquet , J.-F. , Kollmann , A. and Barbier , M. 1978 . La septorine, nouvelle pyrazine substitiuée, isolée du milieu de culture de Septoria nodorum Berk. Champignon phytopathogéne . Comptes Rendu Hebdomadaires des Séances de L'Académie des Sciences, Série C , 286 : 457 – 458 .
   Google Scholar
• Faris , J.D. , Anderson , J.A. , Francl , L.J. and Jordahl , J.G. 1996 . Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture filtrate from . Pyrenophora tritici-repentis. Phytopathology , 86 : 459 – 463 .
   Web of Science ®Google Scholar
• Faris , J.D. and Friesen , T.L. 2009 . Re-evaluation of a tetraploid wheat population indicates that the Tsn1-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility . Phytopathology , 99 : 906 – 912 .
   Google Scholar
• Flor , H.H. 1956 . The complementary genetic systems in flax and flax rust . Adv. Genet. , 8 : 29 – 54 .
   Web of Science ®Google Scholar
• Fried , P.M. and Meister , E. 1987 . Inheritance of leaf and head resistance of winter wheat to Septoria nodorum in a diallel cross . Phytopathology , 77 : 1371 – 1375 .
   Google Scholar
• Friesen , T.L. , Chu , C.-G. , Liu , Z.H. , Halley , S. and Faris , J.D. 2009 . Host-selective toxins produced by Stagonospora nodorum confer disease susceptibility in adult wheat plants under field conditions . Theor. Appl. Genet. , doi: 10.1007/s00122-009-0997-2
   Google Scholar
• Friesen , T.L. , Meinhardt , S.W. and Faris , J.D. 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 .
   PubMed Web of Science ®Google Scholar
• Friesen , T.L. , Stukenbrock , E.H. , Liu , Z.H. , Meinhardt , S.W. , Ling , H. , Faris , J.D. , Rasmussen , J.B. , Solomon , P.S. , McDonald , B.A. and Oliver , R.P. 2006 . Emergence of a new disease as a result of interspecific virulence gene transfer . Nat. Genet. , 38 : 953 – 956 .
   PubMed Web of Science ®Google Scholar
• Friesen , T.L. , Zhang , Z. , Solomon , P.S. , Oliver , R.P. and Faris , J.D. 2008 . Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene . Plant Physiol. , 146 : 682 – 693 .
   PubMed Web of Science ®Google Scholar
• Gonzalez-Hernandez , J.L. , Singh , P.K. , Mergoum , M. , Adhikari , T.B. , Kianian , S.F. , Simsek , S. and Elias , E. 2008 . A quantitative trait locus on chromosome 5B controls resistance of Triticum turgidum (L.) var. dicoccoides to Stagonospora nodorum blotch . Euphytica , 166 : 199 – 206 .
   Google Scholar
• Haen , K.M. , Lu , H. , Friesen , T.L. and Faris , J.D. 2004 . Genomic targeting and high-resolution mapping of the Tsn1 gene in wheat . Crop Sci. , 44 : 951 – 962 .
   Google Scholar
• Hammond-Kosack , K.E. and Jones , J.D.G. 1996 . Resistance gene-dependent plant defense responses . Plant Cell , 8 : 1773 – 1791 .
   PubMed Web of Science ®Google Scholar
• Jones , J.D.G. and Dangl , J.L. 2006 . The plant immune system . Nature , 444 : 323 – 329 .
   PubMed Web of Science ®Google Scholar
• Keller , B. , Winzeler , H. , Winzeler , M. and Fried , P.M. 1994 . Differential sensitivity of wheat embryos against extracts containing toxins of Septoria nodorum: First steps towards in vitro selection . J. Phytopathol. , 141 : 233 – 240 .
   Google Scholar
• Kent , S.S. and Strobel , G.A. 1976 . Phytotoxin from Septoria nodorum . Trans. Brit. Mycol. Soc. , 67 : 354 – 358 .
   Google Scholar
• King , J.E. , Cook , R.J. and Melville , S.C. 1983 . A review of Septoria diseases of wheat and barley . Ann. Appl. Biol. , 103 : 345 – 373 .
   Web of Science ®Google Scholar
• Kleijer , G. , Bronnimann , A. and Fossati , A. 1977 . Chromosomal location of a dominant gene for resistance at the seedling stage to Septoria nodorum Berk. in the wheat variety Atlas 66 . Z.Pflanzenzeucht , 78 : 170 – 173 .
   Google Scholar
• Lalaoui , F. , Halama , P. , Dumortier , V. and Paul , B. 2000 . Cell wall degrading enzymes produced in vitro by isolates of Phaeosphaeria nodorum differing in aggressiveness . Plant Pathol. , 49 : 727 – 733 .
   Web of Science ®Google Scholar
• Lamari , L. , Strelkov , S.E. , Yahyaoui , A. , Orabi , J. and Smith , R.B. 2003 . The identification of two new races of Pyrenophora tritici-repentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat . Phytopathology , 93 : 391 – 396 .
   PubMed Web of Science ®Google Scholar
• Lehtinen , U. 1993 . Plant cell wall degrading enzymes of Septoria nodorum . Physiol. Mol. Plant Pathol , 43 : 121 – 134 .
   Google Scholar
• Liu , Z.H. , Faris , J.D. , Meinhardt , S.W. , Ali , S. , Rasmussen , J.B. and Friesen , T.L. 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 .
   PubMed Web of Science ®Google Scholar
• Liu , Z.H. , Faris , J.D. , Oliver , R.P. , Tan , K.-C. , Solomon , P.S. , McDonald , M.C. , McDonald , B. A , Nunez , A. , Lu , S. , Rasmussen , J.B. and Friesen , T.L. 2009 . SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene . PLoS Pathog. , e1000581
   Google Scholar
• Liu , Z.H. , Friesen , T.L. , Ling , H. , Meinhardt , S.W. , Oliver , R.P. , Rasmussen , J.B. and Faris , J.D. 2006 . The Tsn1-ToxA interaction in the wheat–Stagonospora nodorum pathosystem parallels that of the wheat-tan spot system . Genome , 49 : 1265 – 1273 .
   PubMed Web of Science ®Google Scholar
• Liu , Z.H. , Friesen , T.L. , Meinhardt , S.W. , Ali , S. , Rasmussen , J.B. and Faris , J.D. 2004b . Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat . Phytopathology , 94 : 1061 – 1067 .
   Google Scholar
• Lu , H.J. and Faris , J.D. 2006 . Macro- and micro-colinearity between the genomic region of wheat chromosome 5B containing the Tsn1 gene and the rice genome . Funct. Integr. Gen. , 6 : 90 – 103 .
   Google Scholar
• Lu , H.J. , Fellers , J.P. , Friesen , T.L. , Meinhardt , S.W. and Faris , J.D. 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 .
   Google Scholar
• Ma , H. and Hughes , G.R. 1995 . Genetic control and chromosomal location of Triticum timopheevii derived resistance to Septoria nodorum blotch in durum wheat . Genome , 38 : 332 – 338 .
   PubMed Web of Science ®Google Scholar
• Magro , P. 1984 . Production of polysaccharide-degrading enzymes by Septoria nodorum in culture and during pathogenesis . Plant Sci. Lett. , 37 : 63 – 68 .
   Google Scholar
• Manning , V.A. and Ciuffetti , L.M. 2005 . Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells . Plant Cell , 17 : 3203 – 3212 .
   Google Scholar
• Manning , V.A. , Pandelova , I. and Ciuffetti , L.M. 2002 . A race for a novel host selective toxin . Phytopathology , 92 : S51
   PubMedGoogle Scholar
• Martinez , J.P. , Ottum , S.A. , Ali , S. , Francl , L.J. and Ciuffetti , L.M. 2001 . Characterization of the ToxB gene from Pyrenophora tritici-repentis . Mol. Plant-Microbe Interact. , 14 : 675 – 677 .
   PubMed Web of Science ®Google Scholar
• Meehan , F. and Murphy , H.C. 1947 . Differential phytotoxicity of metabolic by-products of Helminthosporium victoriae. Science , 106 : 270 – 271 .
   Google Scholar
• Meinhardt , S.W. , Cheng , W.J. , Kwon , C.Y. , Donohue , C.M. and Rasmussen , J.B. 2002 . Role of the arginyl-glycyl-aspartic motif in the action of Ptr ToxA produced by Pyrenophora tritici-repentis. Plant Physiol . 130 : 1545 – 1551 .
   Google Scholar
• Murphy , N.E.A. , Loughman , R. , Wilson , R. , Lagudah , E.S. , Appels , R. and Jones , M.G.K. 2000 . Resistance to Septoria nodorum blotch in the Aegilops tauschii accession RL5271 is controlled by a single gene . Euphytica , 113 : 227 – 233 .
   Google Scholar
• Quayyum , H.A. , Gijzen , M. and Traquair , J.A. 2003 . Purification of a necrosis-inducing, host-specific protein toxin from spore germination fluid of Alternaria panax . Phytopathology , 93 : 323 – 328 .
   Google Scholar
• Reddy , L. , Friesen , T.L. , Meinhardt , S.W. , Chao , S. and Faris , J.D. 2008 . Genomic analysis of the Snn1 locus on wheat chromosome arm 1BS and the identification of candidate genes . Plant Genome , 1 : 55 – 66 .
   Google Scholar
• Sarma , G.N. , Manning , V.A. , Ciuffetti , L.M. and Karplus , P.A. 2005 . Structure of Ptr ToxA: An RGD-containing host-selective toxin from Pyrenophora tritici-repentis . Plant Cell , 17 : 3190 – 3202 .
   PubMed Web of Science ®Google Scholar
• Stukenbrock , E.H. and McDonald , B.A. 2007 . Geographic variation and positive diversifying selection in the host specific toxin SnToxA . Mol. Plant Pathol. , 18 : 321 – 332 .
   Google Scholar
• Tatum , L.A. 1971 . The southern corn leaf blight epidemic . Science , 171 : 1113 – 1116 .
   PubMed Web of Science ®Google Scholar
• Tomás , A. and Bockus , W.W. 1987 . Cultivar specific toxicity of culture filtrate of Pyrenophora tritici-repentis . Phytopathology , 77 : 1337 – 1366 .
   Web of Science ®Google Scholar
• Van Kan , J.A.L. 2006 . Licensed to kill: The lifestyle of a necrotrophic plant pathogen . Trends Plant Sci. , 11 : 247 – 253 .
   PubMed Web of Science ®Google Scholar
• Walton , J.D. 1996 . Host-selective toxins: Agents of compatibility . Plant Cell , 8 : 1723 – 1733 .
   PubMed Web of Science ®Google Scholar
• Wicki , W. , Messmer , M. , Winzeler , M. , Stamp , P. and Schmid , J.E. 1999a . In vitro screening for resistance against Septoria nodorum blotch in wheat . Theor. Appl. Genet. , 99 : 1273 – 1280 .
   Google Scholar
• Wicki , W. , Winzeler , M. , Schmid , J.E. , Stamp , P. and Messmer , M. 1999b . Inheritance of resistance to leaf and glume blotch caused by Septoria nodorum Berk. in winter wheat . Theor. Appl. Genet. , 99 : 1265 – 1272 .
   Google Scholar
• Wolpert , T.J. , Dunkle , L.D. and Ciuffetti , L.M. 2002 . Host-selective toxins and avirulence determinants: What's in a name? . Annu. Rev. Phytopathol. , 40 : 251 – 285 .
   PubMed Web of Science ®Google Scholar
• Xu , S.S. , Friesen , T.L. and Cai , X. 2004 . Sources and genetic control of resistance to Stagonospora nodorum blotch in wheat . Recent Res. Develop. Gen. Breed. , 1 : 449 – 469 .
   Google Scholar
• Zhang , Z. , Friesen , T.L. , Simons , K.J. , Xu , S.S. and Faris , J.D. 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 .
   Web of Science ®Google Scholar