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

Canadian Journal of Plant Pathology

Volumn 32, Issue 1, 2010, Pages 20-28

  Friesen, Timothy L ^a   Faris, Justin D ^a  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Effector proteins; Host selective toxin; Phaeosphaeria nodorum; Triticum aestivum

Indexed keywords

PHAEOSPHAERIA NODORUM; TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

EID: 77955198728     PISSN: 07060661     EISSN: None     Source Type: Journal    
DOI: 10.1080/07060661003620896     Document Type: Conference Paper

References (56)

1. ABEYSEKARA, N.S., FRIESEN, T.L., KELLER, S., & 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.
2. BALLANCE, G.M., LAMARI, L., & BERNIER, C.C. (1989). Purification and characterization of a host selective toxin from Pyrenophora triticirepentis. Physiol. Mol Plant Pathol, 35, 203-213.
3. 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.
4. 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, 369,89-101.
5. BOUSQUET, J.-F., & SKAJENNIKOFF, M. (1974). Isolement et mode d'action d'une Phytotoxine produite en culture par Septoria nodorum Berk. Phytopathol Zeitsch., 80, 355-360.
6. CHISOLM, S.T., COAKER, G., DAY, B., & STASKAWICZ, BJ. (2006). Hostmicrobe interactions: Shaping the evolution of the plant immune response. Cell, 124, 803-814.
7. CIUFFETTI, L.M., & TOURI, R.P. (1999). Advances in the characterization of the Pyrenophora tritici-repentis-v/heat interaction. Phytopathology, 89, 444-449.
8. CIUFFETTI, L.M., TOURI, R.P., & 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.
9. DANGL, J.L., & JONES, J.D.G. (2001). Plant pathogens and integrated defense responses to infection. Nature, 411,826-833. (Pubitemid 32588110)
10. DEVYS, M., BOUSQUET, J.-F., KOLLMANN, A., & 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.
11. FARIS, J.D., ANDERSON, J.A., FRANCL, L.J., & 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.
12. FARIS, J.D., & FRIESEN, T.L. (2009). Re-evaluation of a tetraploid wheat population indicates that the TsnI-ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathology, 99,906-912.
13. FLOR, H.H. (1956). The complementary genetic systems in flax and flax rust. Adv. Genet., 8, 29-54.
14. FRIED, P.M., & MHSTER, E. (1987). Inheritance of leaf and head resistance of winter wheat to Septoria nodorum in a diallel cross. Phytopathology, 77,1371-1375.
15. FRIESEN, T.L., CHU, C.-G., LIU, Z.H., HALLEY, S., & 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.
16. FRIESEN, T.L., MEINHARDT, S.W., & FARIS, J.D. (2007). The Stagonospora nodorum-v/heat pathosystem involves multiple proteinaceous hostselective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. Plant J., 51, 681-692.
17. 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., & OLIVER, R.P. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet., 38,953-956. (Pubitemid 44141666)
18. FRIESEN, T.L., ZHANG, Z., SOLOMON, P.S., OLIVER, R.P., & 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.
19. GONZALEZ-HERNANDEZ, J.L., SINGH, P.K., MERGOUM, M., ADHIKARI, T.B., KIANIAN, S.F., SIMSEK, S., & 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.
20. HAEN, K.M., LU, H., FRIESEN, T.L., & FARIS, J.D. (2004). Genomic targeting and high-resolution mapping of the Tsnl gene in wheat. Crop Sci., 44,951-962.
21. HAMMOND-KOSACK, K.E., & JONES, J.D.G. (1996). Resistance genedependent plant defense responses. Plant Cell, 8,1773-1791.
22. JONES, J.D.G., & DANGL, J.L. (2006). The plant immune system. Nature, 444, 323-329.
23. KELLER, B., WINZELER, H., WINZELER, M., & 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.
24. KENT, S.S., & STROBEL, G.A. (1976). Phytotoxin from Septoria nodorum. Trans. Brit. Mycol. Soc, 67, 354-358.
25. KING, J.E., COOK, R.J., & MELVILLE, S.C. (1983). A review of Septoria diseases of wheat and barley. Ann. Appl. Biol, 103,345-373.
26. KLEIJER, G., BRONNIMANN, A., & 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.
27. LALAOUI, F., HALAMA, P., DUMORTIR, V., & PAUL, B. (2000). Cell wall degrading enzymes produced in vitro by isolates of Phaeosphaeria nodorum differing in aggressiveness. Plant Pathol, 49, 727-733.
28. LAMARI, L., STRELKOV, S.E., YAHYAOUI, A., ORABI, J., & SMITH, R.B. (2003). The identification of two new races of Pyrenophora triticirepentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat. Phytopathology, 93, 391-396.
29. LEHTINEN, U. (1993). Plant cell wall degrading enzymes of Septoria nodorum. Physiol. Mol. Plant Pathol, 43, 121-134.
30. Liu, Z.H., FARIS, J.D., MEINHARDT, S.W., Au, S., RASMUSSEN, J.B., & 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.
31. Liu, Z.H., FARIS, J.D., OUVER, R.P., TAN, K.-C., SOLOMON, P.S., MCDONALD, M.C., MCDONALD, B. A., NUNEZ, A., LU, S., RASMUSSEN, J.B., & FRIESEN, T.L. (2009). SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathog., el000581.
32. Liu, Z.H., FRIESEN, T.L., LING, H., MEINHARDT, S.W., OUVER, R.P., RASMUSSEN, J.B., & FARIS, J.D. (2006). The Tsnl-ToxA interaction in the wheat-Siagonospora nodorum paüiosystem parallels that of die wheat-tan spot system. Genome, 49, 1265-1273.
33. Liu, Z.H., FRIESEN, T.L., MEINHARDT, S.W., ALI, S., RASMUSSEN, J.B., & FARIS, J.D. (2004b). Quantitative trait loci analysis and mapping of seedling resistance to Stagonospora nodorum leaf blotch in wheat. Phytopathology, 94,1061-1067. (Pubitemid 39290278)
34. Lu, H.J., & FARIS, J.D. (2006). Macro- and micro-colinearity between the genomic region of wheat chromosome 5B containing die Tsnl gene and the rice genome. Fund. Integr. Gen., 6, 90-103. (Pubitemid 43298550)
35. Lu, H.J., FELLERS, J.P., FRIESEN, T.L., MEINHARDT, S.W., & FARIS, J.D. (2006). Genomic analysis and marker development for the Tsnl locus in wheat using bin-mapped ESTs and flanking BAC contigs. Theor. Appl. Genet., 112,1132-1142.
36. MA, H., & 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.
37. MAGRO, P. (1984). Production of polysaccharide-degrading enzymes by Septoria nodorum in culture and during pathogenesis. Plant Sci. Lett., 37,63-68.
38. MANNING, V.A., & 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.
39. MANNING, V.A., PANDELOVA, I., & CIUFFETTI, L.M. (2002). A race for a novel host selective toxin. Phytopathology, 92, S51.
40. MARTINEZ, J.P., OTTUM, S.A., ALI, S., FRANCL, L.J., & CIUFFETTI, L.M. (2001). Characterization of the ToxB gene from Pyrenophora triticirepentis. Mol Plant-Microbe Interact, 14, 675-677.
41. MEEHAN, F., & MURPHY, H.C. (1947). Differential phytotoxicity of metabolic by-products of Helminthosporium victoriae. Science, 106, 270-27'1.
42. MEINHARDT, S.W., CHENG, WJ., KWON, C.Y., DONOHUE, C.M., & 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.
43. MURPHY, N.E.A., LOUGHMAN, R., WILSON, R., LAGUDAH, E.S., APPELS, R., & 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.
44. QUAYYUM, H.A., GUZEN, M., & TRAQUAIR, J.A. (2003). Purification of a necrosis-inducing, host-specific protein toxin from spore germination fluid of Alternaria panax. Phytopathology, 93, 323-328.
45. REDDY, L., FRIESEN, T.L., MEINHARDT, S.W., CHAO, S., & FARIS, J.D. (2008). Genomic analysis of the Snnl locus on wheat chromosome arm IBS and the identification of candidate genes. Plant Genome, 1, 55-66.
46. SARMA, G.N., MANNING, V.A., CIUFFETTI, L.M., & KARPLUS, P.A. (2005). Structure of Ptr ToxA: An RGD-containing host-selective toxin from Pyrenophora tritici-repentis. Plant Cell, 17,3190-3202.
47. STUKENBROCK, E.H., & MCDONALD, B.A. (2007). Geographic variation and positive diversifying selection in the host specific toxin SnToxA. Mol Plant Pathol, 18,321-332.
48. TATUM, L.A. (1971). The southern corn leaf blight epidemic. Science, 171, 1113-1116.
49. TOMÁS, A., & BOCKUS, W.W. (1987). Cultivar specific toxicity of culture filtrate of Pyrenophora tritici-repentis. Phytopathology, 77, 1337-1366.
50. VAN KAN, J.A.L. (2006). Licensed to kill: The lifestyle of a necrotrophic plant pathogen. Trends Plant Sci., 11,247-253.
51. WALTON, J.D. (1996). Host-selective toxins: Agents of compatibility. Plant Cell, 8, 1723-1733.
52. WICKI, W., MESSMER, M., WINZELER, M., STAMP, P., & SCHMID, J.E. (1999a). In vitro screening for resistance against Septoria nodorum blotch in wheat. Theor. Appl Genet., 99, 1273-1280.
53. WICKI, W., WINZELER, M., SCHMID, J.E., STAMP, P., & 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.
54. WOLPERT, T.J., DUNKLE, L.D., & CIUFFETTI, L.M. (2002). Host-selective toxins and avirulence determinants: What's in a name? Annu. Rev. Phytopathol, 40, 251-285.
55. Xu, S.S., FRIESEN, T.L., & CAI, X. (2004). Sources and genetic control of resistance to Stagonospora nodorum blotch in wheat. Recent Res. Develop. Gen. Breed., 1,449-469.
56. ZHANG, Z., FRIESEN, T.L., SIMONS, K.J., Xu, S.S., & FARIS, J.D. (2009). Development, identification, and validation of markers for markerassisted selection against die Stagonospora nodorum toxin sensitivity genes Tsnl and Snn2 in wheat. Mol. Breeding, 23, 35-49.