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Occurrence of Strobilurin Resistance and Impact on Managing Powdery Mildew of Cucurbits


June 2003

Margaret Tuttle McGrath

Associate Professor, Department of Plant Pathology

Long Island Horticultural Research and Extension Center, Cornell University

3059 Sound Avenue, Riverhead, NY 11901

Resistance to strobilurin fungicides in the cucurbit powdery mildew fungus was detected in the USA in 2002.  This was not surprising because strobilurin resistance had already developed elsewhere in the world.  The cucurbit powdery mildew fungus has demonstrated a high potential for developing resistance. Resistance has developed to each chemical class active for powdery mildew that is at risk for resistance somewhere in the world following repeated use. Strobilurins are in fungicide group 11, quinone outside inhibitors (QoI). Strobilurins have been available for commercial use in the USA beginning in 1998 when azoxystrobin received Section 18 registration in some states for cucurbit powdery mildew. Federal registration was granted in March 1999.

Strobilurin resistance was documented in four fungicide efficacy experiments conducted in research fields in GA, NC, VA, and NY. In these fields, strobilurins, when used alone on a 7-day schedule (use pattern not labeled), did not effectively control cucurbit powdery mildew compared to previous years. Strobilurin efficacy was seen to decline dramatically after the second application in NY. Efficacy also was reduced in commercial fields in KY and research fields in AZ, CA, KY, IL, and MI in 2002 where strobilurins were used predominantly or exclusively.  One resistant isolate was obtained from both the AZ and CA fields; however, this is not considered conclusive because of the small sample size.

Resistance can be detected in research fields more easily than commercial fields, especially when control is not greatly affected.  Reduced control is often the first indication that resistance has developed.  Detecting reduced control is easier in research fields because there are also plants treated with other fungicides not affected by resistance and non-treated plants.  Comparing all the treatments and considering how these treatments have performed in previous experiments reveals whether efficacy is indeed reduced.  Poor application timing is another possible reason for reduced control; however, this would affect efficacy of other treatments as well.  Resistance also can be more difficult to detect in commercial fields because other fungicides used with strobilurins in a program designed for managing resistance might provide enough control of powdery mildew to mask the presence of strobilurin resistant strains, especially if they are at a low frequency. 

The type of resistance detected to strobilurins was qualitative, which means individuals of the cucurbit powdery mildew pathogen were either highly sensitive to strobilurins or highly resistant.  With qualitative resistance, control cannot be regained by applying the fungicide more frequently and/or at a higher rate or by switching to a more active fungicide in the same chemical class, in contrast with quantitative resistance.  All strobilurins will be affected by resistance.

When strobilurins were first introduced, several people involved with their development felt they had a moderate to low resistance risk.  These are site-specific compounds, which has often indicated a high resistance risk; however, they have a new mode of action (inhibition of mitochondrial respiration) that was thought to be difficult for fungi to overcome. Resistance developed much more quickly than expected, but resistance did develop first in a pathogen with a past history of developing resistance to site-specific compounds.  Resistant strains of the cucurbit powdery mildew fungus were found in 1999 after just two years of commercial use in four countries.  Unexplainably, resistance was not detected in North America, despite the size of the pathogen population, until the fifth year of commercial use.  Just as unexpectedly, resistance to strobilurins developed first in the USA in the fungus causing gummy stem blight and black rot in cucurbits.  This was not expected based on past history with benomyl resistance in these pathogens.  In the USA, control failure associated with resistance to benomyl was observed in the cucurbit powdery mildew fungus just 1 year after its registration for use on cucurbits, but it was not observed in the gummy stem blight fungus until 23 years after its registration.

Current general recommendations for managing fungicide resistance include using a diversity of fungicides having different modes of action, within an integrated disease management program that includes non-chemical practices, such as use of resistant cultivars.  Fungicides at risk for resistance should be applied as infrequently as possible.  Using a resistance management program will also minimize yield loss when resistance occurs.  It is extremely important to evaluate disease control when using any fungicide that is at risk for resistance development.  Contact extension staff or the fungicide manufacturer promptly, while the crop is still there, if control is inadequate and there are no other feasible explanations, such as poor application timing.

The fungicide program that has been recommended by extension specialists in the USA for managing powdery mildew and resistance is a strobilurin fungicide (azoxystrobin formulated as Quadris® or trifloxystrobin formulated as Flint®) applied in alternation with the DMI fungicide myclobutanil (formulated as Nova® or Rally®) tank-mixed with a protectant fungicide.  This program uses two strategies for managing resistance: 1. alternation among systemic fungicides in at least two chemical groups and 2. inclusion of protectant fungicides which are not at risk for resistance development because they have multi-site mode of action. Myclobutanil is a triazole fungicide in the DMI activity group, which is fungicide group 3.  Growers need to know what chemical group fungicides are in to avoid alternating among products in the same group.

Although isolates were not tested from commercial production fields, it is prudent for growers to consider improving their resistance management program.  Strobilurin resistance likely occurred in commercial fields as well as research fields in 2002.  Strobilurin resistance appears to be widespread in the USA.  It was confirmed in GA, VA, NC, and NY. It is likely in AZ and CA.  And efficacy of strobilurins was reduced in some mid-western states.  The cucurbit powdery mildew fungus produces spores wind-dispersed over large areas.  Inoculum for powdery mildew developing on cucurbit crops is thought to be wind-dispersed northwards through the eastern and mid-western USA each year.  Occurrence of resistance in commercial fields will reduce the utility of strobilurins, including those not yet registered, and eliminate an important tool for managing DMI resistance. Strobilurins and DMIs are the only systemic fungicides registered for cucurbit powdery mildew in the USA. 

One suggested change to improve resistance management is to apply a contact fungicide with strobilurins as well as with DMIs.  Based on research with Microthiol Disperss® and JMS Stylet-oil®, sulfur and mineral oil are recommended for resistance management because they are more effective than chlorothalonil and other contact fungicides for powdery mildew on the lower leaf surface.  Quadris applied in alternation with Nova and Microthiol Disperss was more effective than Quadris alternated with Nova and Bravo in an experiment conducted in Riverhead, NY, in 2002.  However, chlorothalonil is recommended when other diseases are a concern.  Sulfur is very inexpensive, but can be phytotoxic to melon.  Oil is not compatible with chlorothalonil, captan, sulfur, Kelthane, and possibly foliar nutrients; these materials should not be applied within 2 weeks of an oil application.

Strobilurins should be used as little as possible for managing powdery mildew to delay build up of resistant isolates. This will be challenging because these fungicides are effective against several different plant pathogenic fungi that are often present at the same time as powdery mildew.  This group is unique in that these fungicides are the first synthetic, site-specific compounds to provide significant control of plant diseases caused by pathogens from all three major groups of fungi.  Consequently they have quickly become a very valuable tool for managing diseases.  Early in disease development is the best time to apply strobilurins for powdery mildew because they have outstanding ability to inhibit spore germination, however, other diseases controlled by strobilurins begin to develop later in the growing season than powdery mildew.  No more than half of the applications in a season should include strobilurins.  A limit of one-third is recommended in other areas of the world.

Strobilurins could be used more wisely if the proportion of the powdery mildew pathogen population that is resistant to strobilurins was known before the first application of these fungicides and the impact was known of resistance management programs on the pathogen population.  This information will be obtained in NY in 2003 through work supported by the Friends of Long Island Horticulture Grant Program and the New York State Integrated Pest Management Program.

Managing resistance to DMIs is also extremely important.  Resistance to this group of fungicides is quantitative, in contrast with the qualitative resistance detected to strobilurins in the USA.  With quantitative resistance the pathogen exhibits a continuous range in sensitivity including highly sensitive individuals, moderately insensitive individuals controlled with high but not low rates of the fungicide, and resistant individuals that are not controllable with the fungicide.  Presently in the USA the degree of resistance to DMIs is such that Bayleton, the first DMI fungicide registered, is no longer effective while new DMIs, Nova and Procure, are still highly effective, especially when used at high rates.  These fungicides reportedly are no longer adequately effective in other areas of the world, which indicates the cucurbit powdery mildew pathogen has the genetic potential to develop a higher degree of resistance to the DMIs in the USA.  To manage DMI resistance, apply these fungicides at the manufacturer’s higher label rates and shorter application intervals.

Managing DMI resistance may be challenging. The strobilurin-resistant isolates examined in 2002 also exhibited reduced sensitivity to DMIs.  Most individuals in the powdery mildew fungal population in 2002 that were insensitive to one of these chemical groups must have been insensitive to the other, consequently, applying either a strobilurin or a DMI fungicide shifted the population towards insensitivity to both.

It is important to recognize that the systemic fungicides registered recently for cucurbit powdery mildew are not new chemistry.  Cabrio is a strobilurin while Procure is a DMI fungicide.  Some feel Procure may be sufficiently different from Nova that cross resistance between these may not always occur.

There are no new systemic fungicides in development that could be requested for use in 2003 through Section 18 or 24c registration in the USA. 

The specific directions on fungicide labels must be adhered to -- they supersede these recommendations, if there is a conflict.  Any reference to commercial products, trade or brand names is for information only; no endorsement is intended.

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