» Plant pathogens of vegetable crops can develop resistance to commonly used fungicides.
» Fungicide resistance can result in reduced levels of disease control and reductions in production.
» Fungicide resistance management programs can help slow the development of resistance and prolong the usefulness of fungicides for disease control.
RESISTANCE DEVELOPMENT
Fungicides are the primary means for managing many diseases of vegetable crops. However, pathogens can become resistant to the effects of fungicides. The development of fungicide resistance in plant pathogens can result in the loss of the ability to adequately manage a disease and lead to substantial reductions in production. It is in the grower’s best interest to follow practices that minimize the chances of resistance development and prolong the effectiveness of the fungicides they use.
Two types of resistance have been observed, disruptive resistance and continuous resistance.1 With disruptive resistance, the effectiveness of the fungicide is lost suddenly. A complete loss of effectiveness can occur even at higher application rates, and the resistance tends to be stable even after the fungicide is no longer used. With continuous resistance, reductions of efficacy can occur, but effective control can often be achieved with higher application rates. If the use of the fungicide is discontinued, the pathogen population may revert to being sensitive to the fungicide.
Some classes of fungicides are at higher risk for resistance development. The Fungicide Resistance Action Committee (FRAC) classifies fungicides based on modes of action and chemical/biological makeup. Groups of fungicides with similar modes of action are indicated by their FRAC group codes.2 Estimating a FRAC group’s risk level of resistance development helps companies devise resistance management strategies to protect and prolong the effectiveness of their products.1 When a pathogen develops resistance to one fungicide in a FRAC group, it is often also resistant to other fungicides in the same group. This is known as cross-resistance.1 This occurs in several fungicide classes; however, the degree of crossresistance can vary. Occasionally, negative cross-resistance occurs in fungi between two unrelated fungicides.3
Pathogens also vary in their likelihood of developing resistance to fungicides. Powdery mildew and downy mildew pathogens, and the fungal pathogen Botrytis cinerea have been shown to develop fungicide resistance more frequently than some other groups of pathogens. Species of Rhizoctonia and many rust fungi are less likely to develop resistance to fungicides.1
The risk of developing fungicide resistance is affected by additional factors, including the level of disease pressure, climatic conditions, cropping intensity, cropping diversity, and the rate and frequency of fungicide applications.1
CASE STUDIES
The phenyl amide fungicides (FRAC group 4) include metalaxyl and mefenoxam, which are used to manage oomycete pathogens, including species of Phytophthora and Pythium, and the downy mildews. The phenyl amide fungicides have been classified as high-risk for fungicide resistance.2 Resistance to metalaxyl was first detected in Phytophthora infestans, the pathogen that causes late blight of potato and tomato. Resistance to these fungicides later developed in Phytophthora capsici, the pathogen that causes Phytophthora blight on cucurbits and peppers and buckeye rot on tomatoes, and to the pathogen that causes cucurbit downy mildew (CDM). The presence of resistant strains of these pathogens has resulted in a loss of efficacy of these fungicides for controlling the associated diseases.4,5,6 The CDM pathogen has also developed resistance to other groups of fungicides, such as azoxystrobin (FRAC group 11) and fluopicolide (FRAC group 43).
The fungi that causes powdery mildew in cucurbits (CPM) also have developed resistance to several classes of fungicides, including the MBC fungicides (FRAC group 1), DMI fungicides (FRAC group 3), SDHI fungicides (FRAC group 7), the QoI fungicides (FRAC group 11), quinoxyfen (FRAC group 13), and cyflufenamid (FRAC group U6).4,6 Resistance to MBC fungicides in CPM pathogen isolates can still be detected even though there is now little use of these fungicides for controlling CPM. Resistance to the DMI fungicide triadimefon was detected in the early 1990s; however some newly developed DMI fungicides are still able to effectively control CPM.2
Resistance to the QoI fungicides in the CPM pathogen was detected in the U.S. when there was a sudden reduction of the ability of these fungicides to control CPM, an example of disruptive resistance. QoI fungicides are no longer recommended for CPM control in many areas of the U.S. The CPM pathogen has also developed resistance to the SDHI fungicide boscalid. Cross-resistance to some other SDHI fungicides (benzovindiflupyr, metrafenone, penthiopyrad) has occurred, but resistance to fluopyram has yet to be detected.4
MANAGEMENT
The main strategy used to reduce the development of fungicide resistance is to limit the exposure of target pathogens to at-risk fungicides by limiting the use of these classes of chemicals. Limiting the exposure lowers the selection pressure on the pathogen to develop resistant biotypes.1 Once resistance to a fungicide has occurred in an area, growers should avoid using that FRAC group of fungicides whenever possible.6
The use of integrated pest management programs can reduce the need for fungicide applications by implementing nonchemical methods of disease management. Planting diseaseresistant varieties, when available, can reduce or eliminate the need for fungicide applications. Cultural practices, such as crop rotation and post-harvest sanitation, can lower initial pathogen inoculum levels, and alterations of crop density and irrigation methods can reduce the favorability of conditions for infection and disease spread during the season.
The use of disease-forecast systems, which inform the grower when conditions favor disease development, can reduce the number of fungicide applications as compared to calendarbased spray programs. Crop scouting and regional disease monitoring services can also be used to delay the initiation of spray programs until the disease begins to be observed in or near an area. The primary goal is to delay the development of resistance within the pathogen population, not to manage resistant pathogens once they have developed.1
Exposure to specific fungicides or classes of fungicides can also be reduced by alternating the application of a fungicide with those of fungicides with different modes of action (belonging to different FRAC groups). The idea behind this strategy is that if a few resistant individuals in a pathogen population survive a fungicide application, the next application using a fungicide with a different mode of action will kill the few resistant individuals, eliminating the resistant part of the population. For this strategy to be effective, each of the fungicides in the rotation needs to provide adequate levels of control of the pathogen.1 A fungicide should not be used in the rotation if resistance to that fungicide is already prevalent in the local pathogen population. This approach can be difficult if the number of available (registered), effective fungicides belonging to different FRAC groups is limited.
A similar strategy is to tank-mix higher-risk fungicides with lower-risk fungicides. Again, the idea is that it will be unlikely that an individual pathogenic organism will be resistant to both types of fungicides, so if one fungicide does not kill the individual, the other one will. However, the practice of tankmixing fungicides is somewhat controversial, especially if the mixes are not chosen carefully. There can be problems if the recommendations for the application methods for the two products are different, such as the need to cover the undersides of leaves or if the reentry (REI) or pre-harvest (PHI) intervals are different. A solution to some of these problems is the use of premixed, combination products.1
Resistance management procedures may be mandated on the label of some fungicide products in the form of application restrictions. These restrictions can include the number of allowed sequential applications of a product before an alternate product is applied; the total amount of active ingredient that can be applied in a season; the prohibition of using both soil and foliar applications of the product in the same field; prohibitions of using the product on seedlings or in greenhouse settings; and the requirement to tank-mix the product with another fungicide.
Fungicide products that are no longer effective because of the development of resistant pathogens often continue to be labeled for use on that disease. It can be challenging for growers to know when they should stop using products containing active ingredients that are no longer effective. There is variation in the availability of information on fungicide resistance among growing regions. Regional pest management recommendations often provide general information on the management of fungicide resistance and may mention when certain products are no longer effective. However, this is not always the case, and growers may need to consult several sources of information to be adequately informed about fungicide resistance issues in their area.4
SOURCES
1 Leadbeater, A., McGrath, M., Wyenandt, C., and Stevenson, K. An overview of fungicide resistance and resistance management: history and future trends. In Fungicide Resistance in North America, Second Edition (Stevenson, K., McGrath, M., and Wyenandt, C., editors). American Phytopathological Society. St. Paul, MN.
2 Fungicide Resistance Action Committee (FRAC). https://www.frac.info/.
3 Elad, Y., Shabi, E., and Katan, T. 1988. Negative cross resistance between benzimidazole and N-phenylcarbamate fungicides and control of Botrytis cinerea on grapes. Plant Pathology 37:141-147.
4 McGrath, M., Wyenandt, C., and Stevenson, K. 2019. Fungicide resistance in pathogens of nonsolanaceous vegetable crops. In Fungicide Resistance in North America, Second Edition (Stevenson, K., McGrath, M., and Wyenandt, C., editors). American Phytopathological Society. St. Paul, MN.
5 Gudmestad, N. and Ivors, K. 2019. Development of fungicide resistance in potato and tomato pathogens. In Fungicide Resistance in North America, Second Edition (Stevenson, K., McGrath, M., and Wyenandt, C., editors). American Phytopathological Society. St. Paul, MN.
6 Wyenandt, A. 2021. Cucurbit powdery mildew and downy mildew: A tale of two pathogens. Plant & Pest Advisory. Rutgers Cooperative Extension. June, 5, 2021.
Websites verified: 8/9/2021
ADDITIONAL INFORMATION
For additional agronomic information, please contact your local seed representative.
Performance may vary from location to location and from year to year, as local growing, soil and weather conditions may vary. Growers should evaluate data from multiple locations and years whenever possible and should consider the impacts of these conditions on the grower’s fields. The recommendations in this article are based upon information obtained from the cited sources and should be used as a quick reference for information about vegetable production. The content of this article should not be substituted for the professional opinion of a producer, grower, agronomist, pathologist and similar prSofessional dealing with vegetable crops.
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9050_SE_S13 Published 09/08/2021
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