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Baseline Sensitivity of Ascochyta Rabiei to Azoxystrobin, Pyraclostrobin, and Boscalid

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Baseline Sensitivity of Ascochyta Rabiei to Azoxystrobin, Pyraclostrobin, and Boscalid Baseline Sensitivity of Ascochyta rabiei to Azoxystrobin, Pyraclostrobin, and Boscalid K. A. Wise, C. A. Bradley, J. S. Pasche, and N. C. Gudmestad, Department of Plant Pathology, North Dakota State University, Fargo 58105; and F. M. Dugan and W. Chen, United States Department of Agriculture–Agriculture Re- search Service, Department of Plant Pathology, Washington State University, Pullman 99164 chickpea for control of Ascochyta blight in ABSTRACT the United States, but was not available for Wise, K. A., Bradley, C. A., Pasche, J. S., Gudmestad, N. C., Dugan, F. M., and Chen, W. 2008. use by growers until the 2004 growing Baseline sensitivity of Ascochyta rabiei to azoxystrobin, pyraclostrobin, and boscalid. Plant Dis. season. Boscalid is a novel chemistry in 92:295-300. the carboximide group that acts at succi- nate-ubiquinone reductase (complex II) in Ascochyta rabiei, causal agent of Ascochyta blight on chickpea (Cicer arietinum), can cause the mitochondrial respiration pathway (3). severe yield loss in the United States. Growers rely on applications of fungicides with site- Due to price constraints, this fungicide specific modes of action such as the quinone outside inhibiting (QoI) fungicides azoxystrobin currently has limited use in chickpea pro- and pyraclostrobin, and the carboximide fungicide boscalid, to manage disease. In all, 51 iso- lates collected prior to QoI fungicide registration and 71 isolates collected prior to boscalid reg- duction in the United States; however, the istration in the United States were tested in an in vitro assay to determine the effective fungicide site-specific mode of action increases the likelihood that shifts in fungicide sensitiv- concentration at which 50% of conidial germination was inhibited (EC50) for each isolate– fungicide combination. The effect of salicylhydroxamic acid (SHAM) on conidia of A. rabiei in ity will occur in the pathogen population if the presence and absence of azoxystrobin also was assessed to determine whether the fungus is boscalid use on chickpea becomes more capable of using alternative respiration. Five of nine A. rabiei isolates tested had significantly widespread in the future. The first report of higher (P ≤ 0.05) EC50 values when SHAM was not included in media amended with azox- fungal resistance to boscalid was published ystrobin, indicating that A. rabiei has the potential to use alternative respiration to overcome recently by Avenot and Michailides (1), in fungicide toxicity in vitro. EC50 values of azoxystrobin and pyraclostrobin ranged from 0.0182 which Alternaria alternata isolates from to 0.0338 µg/ml and from 0.0012 to 0.0033 µg/ml, with mean values of 0.0272 and 0.0023 pistachio (Pistacia vera) in California µg/ml, respectively. EC50 values of boscalid ranged from 0.0177 to 0.4960 µg/ml, with a mean of were found to be resistant. 0.1903 µg/ml. Establishment of these baselines is the first step in developing a monitoring pro- Because growers rely heavily on fungi- gram to determine whether shifts in sensitivity to these fungicides are occurring in the A. rabiei cide applications to manage Ascochyta pathogen population. blight, it is important to determine whether Additional keywords: Didymella rabiei, fungicide resistance the fungal population is changing in re- sponse to selection pressure. Isolates of D. bryoniae, a pathogen of cucurbits in the same genus as the teleomorph of As- Ascochyta blight, caused by the fungal Two of the most widely used fungicide cochyta rabiei (D. rabiei), have been re- pathogen Ascochyta rabiei (Pass.) Labr. active ingredients for control of Ascochyta ported to be resistant to the QoI fungicide (teleomorph, Didymella rabiei (Kovatsch.) blight in the United States are azoxystrobin azoxystrobin (20,29). Because of these Arx.), is a limiting disease of chickpea (Ci- (Amistar or Quadris; Syngenta Crop Pro- reports and the history of QoI resistance in cer arietinum L.) production throughout the tection, Greensboro, NC) and pyraclos- other pathogens, a baseline sensitivity level world (18,27). In the United States and trobin (Headline; BASF Corporation, Re- should be established to facilitate a moni- Canada, chickpea production has decreased search Triangle Park, NC). Azoxystrobin toring program to detect shifts in sensitiv- in the last decade due to the devastating became available for use on chickpea in ity. According to Brent and Holloman (4), effects of Ascochyta blight, which is con- the 2002 growing season in areas of the there are three reasons to conduct baseline sidered to be the most important disease United States where section 18 emergency fungicide sensitivity studies: (i) to develop affecting chickpea production in these re- exemptions were approved for control of and test an accurate, rapid, reproducible gions (5,7,30). A. rabiei can spread quickly Ascochyta blight on chickpea. In 2003, method for determining the degree of sen- throughout chickpea fields, causing signifi- both azoxystrobin and pyraclostrobin re- sitivity of large numbers of field samples cant yield losses (5,30). Development of ceived United States Environmental Pro- of major target fungi, so that such a chickpea cultivars with durable resistance tection Agency section 3 registrations prior method is readily available for any future has been complicated by the presence of to the growing season. These fungicides monitoring that may be required; (ii) to different pathotypes of A. rabiei (5,7). are classified as quinone outside inhibitors obtain initial data regarding the range of Therefore, growers rely on fungicide appli- (QoI) and block electron transport at the sensitivity that exists in major target cations to manage the disease (27). quinol-oxidizing site of the cytochrome pathogens and major areas of use, to serve bc1 complex (complex III) in the mito- as a baseline against which any future chondrial respiration chain (2,10). The measurements of sensitivity can be com- Corresponding author: C. A. Bradley site-specific mode of action of this chemis- pared in order to reveal any possible shifts E-mail: [email protected] try increases the potential for fungicide in sensitivity; and (iii) to detect any differ- Current address of C. A. Bradley: Department of resistance to develop in the target fungal ences in sensitivity between samples that Crop Sciences, University of Illinois, 1102 S. populations. Several fungal pathogens are might, through the buildup of the less- Goodwin Ave., Urbana 61801. reported to have reduced levels of sensitiv- sensitive components, lead to future resis- ity to QoI fungicides due to single amino tance problems. Jutsum et al. (12) and Accepted for publication 24 September 2007. acid substitutions in the cytochrome b site Russell (26) stressed the importance of (6,10,15,16,23). determining the range of sensitivities pre- doi:10.1094/ PDIS-92-2-0295 The fungicide boscalid (Endura; BASF sent in target pathogen populations prior to © 2008 The American Phytopathological Society Corporation) was registered in 2003 on commercialization of the product. Estab- Plant Disease / February 2008 295 lishing a baseline for the carboximide fun- from the Ascochyta collection in the plates (60 by 15 mm). Plates were held at gicide, boscalid, is a proactive approach to United States Department of Agriculture– 19°C for 18 h in the dark. Following incu- fungicide resistance management and will Agricultural Research Service collection in bation, 100 conidia per plate were visually allow pathogen sensitivity to be monitored Pullman, WA (Table 1). These A. rabiei assessed microscopically (×100 magnifica- if the chemistry use becomes more wide- isolates were collected prior to the registra- tion) and evaluated for germination. A spread on chickpea in the United States. tions of QoI fungicides and boscalid in the conidium was considered to be germinated Previous research involving in vitro test- United States, and represent a true baseline if the germ tube was at least as long as the ing of fungi in the presence of respiration- group with no possible exposure to any length of the conidium. inhibiting fungicides has indicated that QoI chemistry or boscalid. An additional Effect of SHAM on conidia germina- some fungi are able to use an alternative 20 isolates of A. rabiei were used to estab- tion. The effect of SHAM (Sigma-Aldrich) respiration pathway to bypass complex III lish the baseline for boscalid (Table 1); at a concentration of 100 µg/ml on A. ra- and IV in the mitochondrial respiration these isolates were collected prior to the biei conidial germination was examined in chain, allowing fungal spores to germinate use of boscalid in U.S. chickpea fields. a preliminary experiment. Ten isolates even in the presence of high doses of certain Each isolate was preserved for long-term (AR401, AR402, AR418, AR430, AR477, fungicides (22,31,35). This phenomenon is storage by plating 2 µl of conidial suspen- AR604, AR660, AR666, AR668, and observed only in vitro, and it is hypothe- sion onto individual plates of potato dex- AR721) were selected randomly to test on sized that plant-produced flavones prevent trose agar (PDA) (Difco Laboratories, PDA amended with SHAM at 100 µg/ml the induction of alternative oxidase in na- Detroit) with Whatman no. 1 filter paper and nonamended PDA. Random selection ture, thus inhibiting alternative respiration cut into small strips, sterilized, and placed of the isolates was done using the RAND (22,31). However, alternative respiration is on the agar surface. Each isolate was function in Microsoft Excel 2003 software still important because it may strongly im- grown in a growth chamber for 14 to 21 (Microsoft Corp., Redmond, WA). For this pact results of in vitro assays, leading to days under a diurnal cycle (12 h of light experiment, a stock solution of SHAM was inaccurate assessments of fungicide sensi- and 12 h of dark) at 20 ± 2°C, at which prepared by adding 100 mg of SHAM for tivity in vitro. The chemical salicylhydrox- time the filter paper was covered with each 1 ml of methanol.
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