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Title: Novel necrotrophic effectors from stagonospora nodorum and corresponding host genes in winter wheat germplasm in the Southeastern United States

Author
item CROOK, A - North Carolina State University
item Friesen, Timothy
item LIU, Z - North Dakota State University
item OJIAMBO, P - North Carolina State University
item Cowger, Christina

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/1/2012
Publication Date: 4/15/2012
Citation: Crook, A.D., Friesen, T.L., Liu, Z.H., Ojiambo, P.S., Cowger, C. 2012. Novel necrotrophic effectors from stagonospora nodorum and corresponding host genes in winter wheat germplasm in the Southeastern United States. Phytopathology. 102:498-505.

Interpretive Summary: Stagonospora nodorum blotch (SNB), caused by the fungus Stagonospora nodorum, is among the most common diseases of winter wheat in the U.S. Recently, it has been discovered that the fungus produces several necrotrophic effectors (NEs), also known as host-selective toxins. Each NE matches a specific sensitivity (Snn) gene that may be present in the host. In this study, 39 isolates of S. nodorum were obtained from wheat debris or grain from seven states in the southeastern U.S., in order to investigate the production of NEs in the region. Twenty-nine cultivars with varying levels of resistance to SNB, representing 10 eastern-U.S. breeding programs, were tested for potential NE sensitivity. Leaves of the wheat plants were infiltrated with liquid in which the S. nodorum isolates had been grown. Production of NEs was detected in isolates originating in each sampled state except Maryland. A large percentage of isolates (44%) produced NEs different from those previously characterized in the upper Great Plains region. These novel NEs likely correspond to as-yet unidentified Snn genes in Southeastern wheat cultivars. Using a genetic test, lower percentages of previously identified NE genes were found in the southeastern U.S. isolates compared to previously analyzed, larger international samples. Only two of the wheat cultivars appeared to contain known Snn genes, although 50% of the cultivars displayed sensitivity to culture filtrates containing unknown NEs. Sensitivity to the NEs was more frequent in SNB-susceptible cultivars than in moderately resistant (MR) cultivars. Our results suggest that NE sensitivities influence but may not be the only determinant of cultivar resistance to S. nodorum. NEs and Snn genes that have not yet been characterized appear to be more important than the already-studied genes in determining SNB severity in the southeastern U.S.

Technical Abstract: Stagonospora nodorum blotch (SNB), caused by the necrotrophic fungus Stagonospora nodorum (teleomorph: Phaeosphaeria nodorum), is among the most common diseases of winter wheat in the U.S. New opportunities in resistance breeding have arisen from the recent discovery of several necrotrophic effectors (NEs, also known as host-selective toxins) produced by S. nodorum, along with their corresponding host sensitivity (Snn) genes. Thirty-nine isolates of S. nodorum collected from wheat debris or grain from seven states in the southeastern U.S. were used to investigate the production of NEs in the region. Twenty-nine cultivars with varying levels of resistance to SNB, representing 10 eastern-U.S. breeding programs, were infiltrated with culture filtrates from the S. nodorum isolates in a randomized complete block design. Three single-NE Pichia pastoris controls, two S. nodorum isolate controls, and six Snn-differential wheat controls were also used. Cultivar × isolate interactions were visually evaluated for sensitivity at seven days after infiltration. Production of NEs was detected in isolates originating in each sampled state except Maryland. A large percentage of isolates (44%) produced NEs different from those previously characterized in the upper Great Plains region. These novel NEs likely correspond to unidentified Snn genes in Southeastern wheat cultivars, as NEs are thought to arise under selection pressure from genes for resistance to biotrophic pathogens of wheat cultivars that differ by geographic region. Only 3%, 0%, and 23% of isolates produced SnToxA, SnTox1, and SnTox3, respectively, by the culture-filtrate test. A Southern dot-blot test showed that 15%, 74%, and 39% of the isolates carried the genes for those NEs, respectively; those percentages were lower than those found previously in larger international samples. Only two cultivars appeared to contain known Snn genes, although 50% of the cultivars displayed sensitivity to culture filtrates containing unknown NEs. Effector sensitivity was more frequent in SNB-susceptible cultivars than in moderately resistant (MR) cultivars (P = 0.008), although some susceptible cultivars did not exhibit sensitivity to NEs produced by isolates in this study and some MR cultivars were sensitive to NEs of multiple isolates. Our results suggest that NE sensitivities influence but may not be the only determinant of cultivar resistance to S. nodorum. Specific knowledge of NE and Snn gene frequencies in this region can be used by wheat breeding programs to improve SNB resistance.