@article{cowger_meyers_whetten_2022, title={Sensitivity of the US Wheat Powdery Mildew Population to Quinone Outside Inhibitor Fungicides and Determination of the Complete Blumeria graminis f. sp. tritici Cytochrome b Gene}, volume={112}, ISSN={["1943-7684"]}, url={https://doi.org/10.1094/PHYTO-04-21-0132-R}, DOI={10.1094/PHYTO-04-21-0132-R}, abstractNote={ Wheat powdery mildew, caused by Blumeria graminis f. sp. tritici, is managed primarily with cultivar resistance and foliar fungicides. Quinone outside inhibitors (QoIs), which target the mitochondrial cytochrome b (cytb) gene, are one of the two main fungicide classes used on wheat. While European populations of B. graminis f. sp. tritici are widely insensitive to QoIs, largely because of the cytb mutation G143A, the QoI sensitivity of the U.S. B. graminis f. sp. tritici population had never been evaluated despite years of QoI use on U.S. wheat. A total of 381 B. graminis f. sp. tritici isolates from 15 central and eastern U.S. states were screened for sensitivity to QoI fungicides pyraclostrobin and picoxystrobin. A modest range of sensitivities was observed, with maximum resistance factors of 11.2 for pyraclostrobin and 5.3 for picoxystrobin. The F129L, G137R, and G143A cytb mutations were not detected in the U.S. B. graminis f. sp. tritici population, nor were mutations identified in the PEWY loop, a key part of the Qo site. Thus, no genetic basis for the observed quantitative variation in QoI sensitivity of U.S. B. graminis f. sp. tritici was identified. Isolate sporulation was weakly negatively associated with reduced QoI sensitivity, suggesting a fitness cost. In the course of the study, the complete B. graminis f. sp. tritici cytb gene sequence was determined for the first time in the isolate 96224 v. 3.16 reference genome. Contrary to previous reports, the gene has an intron that appears to belong to intron group II, which is unusual in fungi. The study was the first QoI sensitivity screening of a large, geographically diverse set of U.S. B. graminis f. sp. tritici isolates, and while the population as a whole remains relatively sensitive, some quantitative loss of efficacy was observed. }, number={2}, journal={PHYTOPATHOLOGY}, author={Cowger, Christina and Meyers, Emily and Whetten, Rebecca}, year={2022}, month={Feb}, pages={249–260} }
 @article{meyers_arellano_cowger_2019, title={Sensitivity of the US Blumeria graminis f. sp. tritici Population to Demethylation Inhibitor Fungicides}, volume={103}, ISBN={1943-7692}, url={https://doi.org/10.1094/PDIS-04-19-0715-RE}, DOI={10.1094/PDIS-04-19-0715-RE}, abstractNote={ Wheat powdery mildew, caused by Blumeria graminis f. sp. tritici, is managed in the United States with cultivar resistance and foliar fungicides. Despite high levels of fungicide sensitivity in other cereal mildew populations, fungicide sensitivity of U.S. B. graminis f. sp. tritici has never been evaluated. Almost 400 B. graminis f. sp. tritici isolates were collected from 15 U.S. states over 2 years and phenotyped for sensitivity to two widely used demethylation inhibitor (DMI) fungicides, tebuconazole and prothioconazole. A large range of sensitivity to both DMIs was observed, with more insensitive isolates originating from the eastern United States (Great Lakes, Mid-Atlantic, and Southeast regions) and more sensitive isolates from central states (Plains region, Arkansas, and Missouri). Cross-resistance was indicated by a positive although weak association between tebuconazole and prothioconazole sensitivities at all levels of analysis (EC50 values, P < 0.0001). A possible fitness cost was also associated with prothioconazole insensitivity (P = 0.0307) when analyzed at the state population level. This is the first assessment of fungicide sensitivity in the U.S. B. graminis f. sp. tritici population, and it produced evidence of regional selection for reduced DMI efficacy. The observation of reduced sensitivity to DMI fungicides in the eastern United States underlines the importance of rotating between chemistry classes to maintain the effectiveness of DMIs in U.S. wheat production. Although cross-resistance was demonstrated, variability in the relationship of EC50 values for tebuconazole and prothioconazole also suggests that multiple mechanisms influence B. graminis f. sp. tritici isolate responses to these two DMI fungicides. }, number={12}, journal={PLANT DISEASE}, publisher={Scientific Societies}, author={Meyers, Emily and Arellano, Consuelo and Cowger, Christina}, year={2019}, month={Dec}, pages={3108–3116} }
 @article{mcnally_menardo_luthi_praz_mueller_kunz_ben-david_chandrasekhar_dinoor_cowger_et al._2018, title={Distinct domains of the AVRPM3(A2/F2) avirulence protein from wheat powdery mildew are involved in immune receptor recognition and putative effector function}, volume={218}, ISSN={["1469-8137"]}, DOI={10.1111/nph.15026}, abstractNote={Summary}, number={2}, journal={NEW PHYTOLOGIST}, author={McNally, Kaitlin Elyse and Menardo, Fabrizio and Luthi, Linda and Praz, Coraline Rosalie and Mueller, Marion Claudia and Kunz, Lukas and Ben-David, Roi and Chandrasekhar, Kottakota and Dinoor, Amos and Cowger, Christina and et al.}, year={2018}, month={Apr}, pages={681–695} }
 @article{cowger_mehra_arellano_meyers_murphy_2018, title={Virulence Differences in Blumeria graminis f. sp tritici from the Central and Eastern United States}, volume={108}, ISSN={["1943-7684"]}, DOI={10.1094/phyto-06-17-0211-r}, abstractNote={ Wheat powdery mildew is a disease of global importance that occurs across a wide geographic area in the United States. A virulence survey of Blumeria graminis f. sp. tritici, the causal agent, was conducted by sampling 36 wheat fields in 15 U.S. states in the years 2013 and 2014. Using a hierarchical sampling protocol, isolates were derived from three separated plants at each of five separated sites within each field in order to assess the spatial distribution of pathotypes. In total, 1,017 isolates from those fields were tested individually on single-gene differential cultivars containing a total of 21 powdery mildew resistance (Pm) genes. Several recently introgressed mildew resistance genes from wild wheat relatives (Pm37, Pm53, MlAG12, NCAG13, and MlUM15) exhibited complete or nearly complete resistance to all local B. graminis f. sp. tritici populations from across the sampled area. One older gene, Pm4b, also retained at least some efficacy across the sampled area. The B. graminis f. sp. tritici population sampled from Arkansas and Missouri, on the western edge of the eastern soft red winter wheat region, had virulence profiles more similar to other soft wheat mildew populations than to the geographically closer population from hard wheat fields in the Plains states of Oklahoma, Nebraska, and Kansas. The Plains population differed in that it was avirulent to several Pm genes long defeated in the soft-wheat-growing areas. Virulence complexity was greatest east of the Mississippi River, and diminished toward the west. Several recently introgressed Pm genes (Pm25, Pm34, Pm35, and NCA6) that are highly effective against mildew in the field in North Carolina were unexpectedly susceptible to eastern-U.S. B. graminis f. sp. tritici populations in detached-leaf tests. Sampled fields displayed a wide range of pathotype diversity and spatial distribution, suggesting that epidemics are caused by varying numbers of pathotypes in all regions. The research confirmed that most long-used Pm genes are defeated in the eastern United States, and the U.S. B. graminis f. sp. tritici population has different virulence profiles in the hard- and soft-wheat regions, which are likely maintained by host selection, isolation by distance, and west-to-east gene flow. }, number={3}, journal={PHYTOPATHOLOGY}, author={Cowger, Christina and Mehra, Lucky and Arellano, Consuelo and Meyers, Emily and Murphy, J. Paul}, year={2018}, month={Mar}, pages={402–411} }