Effect of the F129L Mutation in Alternaria solani on Fungicides Affecting Mitochondrial Respiration

Alternaria solani Sorauer (Ellis), a foliar pathogen of potato (Solanum tuberosum L.), was considered to be difficult to control, responsible for yield losses of up to 30% (24), until the registration of the first strobilurin fungicide, azoxystrobin (Quadris; Syngenta Crop Protection, Greensboro, NC), in 1999. Strobilurins belong to the group of chemicals classified as Quinone outside inhibitor (QoI) fungicides (Fungicide Resistance Action Committee [FRAC] group 11), which inhibit electron transport in mitochondrial respiration at complex III (13). These fungicides have a specific single-site mode of action but, in spite of this, originally were classified as a medium resistance risk in A. solani (2). The development of reduced-sensitivity to azoxystrobin was first observed in 2000 in Nebraska by one of the authors (N. C. Gudmestad) and in North Dakota and Minnesota in 2001. Isolates of A. solani collected from these fields subsequently were determined to be significantly less sensitive in vitro to azoxystrobin, resulting in decreased disease control in vivo (23). When first registered, azoxystrobin provided significantly improved control of early blight under field conditions compared with protectant fungicides such as chlorothalonil or mancozeb (28). However, more recently, disease control provided by azoxystrobin frequently has been no better than the level of control provided by standard protectant fungicides in the presence of azoxystrobin reduced-sensitive A. solani isolates (29). Resistance to QoI fungicides first was detected in Blumeria graminis (DC) E. O. Sper f. sp. tritici Em. Marchal and was attributed to a mutation in the cytochrome b gene causing an amino acid substitution of glycine with alanine at position 143 (G143A) (26). A second amino acid substitution of phenylalanine with leucine at position 129 (F129L) has since been described in one isolate of Pythium aphanidermatum (Edson) Fitzp. (1) as well as isolates of Pyricularia grisea (Cooke) Sacc., although most isolates of P. grisea have undergone the G143A mutation (12,30). Six previously evaluated A. solani isolates which had reduced-sensitivity to azoxystrobin were determined to contain the F129L mutation (23). Although the G143A mutation has been shown to convey full resistance in other host–pathogen systems, resulting in a total loss of disease control (8,10,12,14,25,26), the F129L mutation in A. solani conveys an approximately 10-fold loss of sensitivity in vitro to fungicides azoxystrobin and pyraclostrobin, resulting in a significant, but not total, loss of disease control under controlled conditions (23). However, reducedsensitive isolates were only twofold less sensitive to trifloxystrobin and this shift in sensitivity did not appreciably affect disease control in these same studies (23). Similar results were observed with isolates of P. grisea in which the F129L mutation was detected (12,30). The G143A mutation has been detected in other Alternaria spp., including isolates of A. alternata (Fr.:Fr.) Keissl., A. tenuissima, (Kunze: Fr.) Wiltshire, and A. arborescens Simmons, which failed to be controlled by azoxystrobin (19). After the registration of azoxystrobin, several other QoI fungicides were labeled for use on potato. Related nonstrobilurin QoI chemistries famoxadone (Tanos; DuPont Crop Protection, Wilmington, DE) and fenamidone (Reason; Bayer Corporation, Agricultural Division, Kansas City, MO), registered for use on potato in 2003 and 2004, respectively, have modes of action similar to those of azoxystrobin and pyraclostrobin (1,11). Although these chemicals all are classified within the QoI group, each is classified by FRAC into different chemical subgroups. Crossresistance among all fungicides in the QoI group, conveyed by the G143A mutation, has been demonstrated in plant-pathogenic fungi such as Podosphaera xanthii (Castagne) U. Braun & N. Shishkoff, Pseudoperonospora cubensis Berk. & M. A. Curtis) Rostovzev (8,10), P. grisea (12,30), Plasmopara viticola (Berk. & M. A. Curtis) Berl. & De Toni in Sacc. (8), B. graminis f. sp. tritici (8,26), MyABSTRACT Pasche, J. S., Piche, L. M., and Gudmestad, N. C. 2005. Effect of the F129L mutation in Alternaria solani on fungicides affecting mitochondrial respiration. Plant Dis. 89:269-278.