Sensitivity of Alternaria spp. from potato to pyrimethanil, cyprodinil, and fludioxonil

Highlights

• AP and PP fungicides remain effective on potato early blight/brown spot pathogens.

• Cross-sensitivity between pyrimethanil and cyprodinil in baseline A. alternata.

• Significant loss of disease control seen for some non-baseline A. solani isolates.

• Fludioxonil and cyprodinil are good candidates for addition to a potato IPM program.

Abstract

Early blight, caused by Alternaria solani, and brown leaf spot, caused by a number of small-spored Alternaria spp. including Alternaria alternata sensu stricto, Alternaria arborescens, and Alternaria tenuissima, are observed annually in all midwestern potato production areas. However, Alternaria spp. have developed reduced sensitivity and/or resistance to many single-site mode of action fungicides such as quinone outside inhibitor (QoI; FRAC group 11), succinate dehydrogenase inhibitor (SDHI; FRAC group 7), and anilinopyrimidine (AP; FRAC group 9). Mean in vitro sensitivity EC₅₀ values (effective concentration where fungal growth is inhibited by 50%) of A. alternata (n = 16), A. arborescens (n = 3), A. tenuissima (n = 5), and A. solani (n = 58) in response to the AP fungicides pyrimethanil and cyprodinil and the phenylpyrrole (PP) fungicide fludioxonil were determined via mycelial growth assays. Significant fungicide by isolate interactions were observed for all Alternaria spp. evaluated in vitro, indicating reduced-sensitivity of some isolates to individual fungicides. EC₅₀ values for three non-baseline A. solani isolates collected in 2010, 2011 and 2013 were within the baseline for all three fungicides. A significant correlation was observed between pyrimethanil and cyprodinil EC₅₀ values among A. alternata isolates, but no relationship was observed with the other fungicides or in A. solani. In greenhouse evaluations, a significant loss of disease control was observed for some non-baseline A. solani isolates, and this was more pronounced in the AP fungicides, pyrimethanil and cyprodinil. No significant correlation was observed between in vitro EC₅₀ value and area under the dose response curve based on greenhouse assays, likely due to the limited number of isolates evaluated. Further research is needed to determine if these reductions affect control of early blight and brown leaf spot in potato under field conditions. Results from this study indicate that fludioxonil and cyprodinil are potentially good additions into fungicide rotation programs or as co-pack chemistries for control of leaf spot diseases and fungicide resistance management.

Introduction

Early blight and brown leaf spot are chronic problems in potato production. Alternaria solani Sorauer, which causes early blight, is the dominant pathogen when compared to small-spored Alternaria spp., such as Alternaria alternata (Fr.) Keissler, Alternaria arborescens E.G. Simmons, and Alternaria tenuissima (Kunze) which cause brown leaf spot. Early blight and brown leaf spot can cause potato yield reductions up to 30 and 18%, respectively, if conditions are favorable (Christ and Maczuga, 1989; Droby et al., 1984; Shtienberg et al., 1990).

Specialty fungicides such as quinone outside inhibitors (QoI; FRAC group 11) and succinate dehydrogenase inhibitors (SDHI; FRAC group 7) utilized in rotation with standard protectant fungicides mancozeb or chlorothalonil, can provide early blight disease control and increase potato yield (Yellareddygari et al., 2019). While SDHI and QoI fungicides are useful additions to potato disease management programs, they are regarded as high resistance-risk fungicides due to the single-site modes of action. Specialty fungicides including demethylation inhibitors (DMI; FRAC group 3) and anilinopyrimidines (AP; FRAC group 9) also provide a high level of early blight disease control and are all classified as medium-risk fungicides. The addition of phenylpyrroles (PP; FRAC group 12) also may be useful in the management of early blight and brown leaf spot. PP fungicides are also classified as medium resistance-risk fungicides (FRAC, 2019).

While a low frequency of reduced sensitivity and/or resistance to the AP and PP fungicides has been observed in numerous pathogens, these chemistries remain effective for disease management (Avenot and Michailides, 2015; Fairchild et al., 2013; Fonseka and Gudmestad, 2016; Kanetis et al., 2008). A recent study determined that two DMI fungicides, difenoconazole, and metconazole, demonstrated high intrinsic activity against A. solani and putative A. alternata sensu lato (Fonseka and Gudmestad, 2016). Also in that study, some A. solani isolates exhibited reduced sensitivity to the AP fungicide pyrimethanil under in vitro conditions and were controlled to a significantly lesser degree than sensitive isolates in greenhouse evaluations. Pyrimethanil has been utilized in potato grower management programs for over 16 years and reduced sensitivity has only been detected in a small number of A. solani isolates in Colorado, Idaho, Minnesota, and Texas (Fairchild et al., 2013; Fonseka and Gudmestad, 2016). Other studies have demonstrated the AP fungicide, cyprodinil, and the PP fungicide, fludioxonil, effectively controlled putative A. alternata sensu lato isolates (Avenot and Michailides, 2015). In that study, a few isolates displayed resistance to fludioxonil and/or cyprodinil with no observed fitness penalties.

AP and PP fungicides are frequently used in combination with other fungicide chemistries in pre-packaged mixtures. These mixtures have been highly effective for management of Botrytis cinerea (Chapeland et al., 1999; Hilber and Schüepp, 1996), A. alternata sensu lato (Avenot and Michailides, 2015), and Penicillium digitatum (Kanetis et al., 2008). Fludioxonil is used primarily as a seed treatment fungicide registered on numerous crops, and as a post-harvest fungicide used on several tree fruit crops. Fludioxonil also is used in a pre-packaged mixture with cyprodinil for foliar disease control in pulse crops, and numerous vegetable and fruit crops. In potato, fludioxonil is used as a seed treatment for seed-borne tuber black scurf (Rhizoctonia solani) and, more recently has been mixed with other chemistries to manage potato storage diseases such as Fusarium dry rot (Fusarium spp.), and silver scurf of potato (Helimthosporium solani). The efficacy of cyprodinil and fludioxonil for management of early blight and brown leaf spot has not been studied extensively. Although cyprodinil is not currently registered for foliar use on potato, at the time these studies were initiated it was being considered as a pre-pack partner for recently developed SDHI fungicides. Fludioxonil is used as a pre-packaged mixture partner with the SDHI fungicide adepidyn as a potato foliar fungicide Miravis Prime™ (Syngenta Crop Protection, Greensboro, NC); however, its activity on the Alternaria leaf spot pathogens of potato has not been reported.

Previous studies have determined baseline (isolates collected before fungicide was registered) pyrimethanil sensitivity for both A. solani and putative A. alternata sensu lato (Fonseka and Gudmestad, 2016). A recently published study determined that potato brown spot is caused by four Alternaria spp. (A. alternata, A. arbusti, A. arborescens, and A. tenuissima) (Tymon et al., 2016). In light of this, further examination resulted in reclassification of some isolates of the putative A. alternata sensu lato baseline population tested for sensitivity to pyrimethanil (Fonseka and Gudmestad, 2016) as A. arborescens and A. tenuissima (Budde-Rodriguez, 2020). Given these new findings, reexamination of these isolates is warranted. Additionally, baseline sensitivities of A. alternata, A. arborescens, and A. tenuissima in response to cyprodinil and fludioxonil have not been established. Analyzing isolate response to new or existing fungicides aids in determining the fungicide risk factors and is the only way to effectively monitor for shifts in sensitivity. Alternaria solani and A. alternata sensu lato are classified as medium- and high-risk pathogens, respectively (FRAC, 2019). Risk to develop fungicide resistance has not been reported for A. arborescens and A. tenuissima. Therefore, the objectives of this study were to (i) determine the sensitivity of four Alternaria spp. to anilinopyrimidine and phenylpyrrole fungicides, and to (ii) determine the control of A. solani provided by pyrimethanil, cyprodinil, and fludioxonil.