Written by Gary Grove, Prashant Swamy, and Neusa Guerra, WSU-IAREC, Prosser WA. 28 April 2020.
Summary New research results confirm resistance to Group 11 fungicides. More than half of the powdery mildew isolates had developed various levels of DMI (Group 3) resistance. Group 3 and 11 resistance was found in all production areas. The resistance is widespread but we do not yet know the extent within a production area. Resistance in your orchard will depend on fungicide history in the block. Given our documentation of resistance to Groups 11 and 3 compounds, growers should consider available alternatives.
Powdery mildew of cherry, which is caused by Podosphaera cerasi (formerly P. clandestina), is a perennial problem in PNW cherries. Disease incidence and severity vary from season to season but the economic requirements of intensive fungicide programs are an annual challenge. Our cherry industry is understandably in an “all hands on deck” scenario vis-à-vis the epidemic of Western X that is challenging our industry. However, despite these serious disease challenges we also need to remain cognizant of the epidemiological status of cherry powdery mildew in the region. Given the necessity for a diverse set of fungicide tools for powdery mildew management, we will focus this discussion on that aspect of disease management.
The Fungicide Resistance Action Committee (FRAC) has classified fungicides based on site-of-action. A fungicide’s mode of action refers to specific cellular processes inhibited by a fungicide. A fungicide’s FRAC code refers to the compound’s site of action. For example, group 3, 7, and 11 sites of action are inhibition of C-14 demethylase during membrane biosynthesis, succinate dehydrogenase, and ubiquinol oxidase pathways, respectively. However, both group 7 and 11 fungicides inhibit cellular respiration and therefore have the same mode of action. This information is helpful when designing a fungicide program that conforms to FRAC resistance management guidelines. Resistance management involves the use (via tank mixing, alternation, and/or rotation) of multiple fungicide sites of action. It is important to understand that if a pathogen population develops resistance to fungicides within a FRAC group (i.e. compounds with the same site of action, e.g. FRAC Group 7), it is likely to be resistant to all members of that group. Resistance is more likely to develop if the pathogen is frequently treated with one or multiple fungicides within a given FRAC group. Included in the table (Table 1) are members of the fungicide site of action groups (or FRAC Groups) known as DMI (demethylation inhibitors, Group 3), QoI (quinone outside inhibitors; previously called strobilurins, Group 11), quinolines (quinoxyfen, Group 13), SDHI (succinate dehyrodgenase inhibitors; group 7), sulfur (Group M2), various “biological” fungicides (Group 44), petroleum-derived spray oils, potassium bicarbonate, and various inorganic salts. Petroleum spray oils, inorganic salts, and potassium bicarbonate are listed as “Not Classified” (NC) by FRAC. Several products are formulations or “premixes” of two different fungicide classes (modes of action) of FRAC groups. Consult product labels for appropriate rates and spray intervals. The resistance risk is product-dependent.
The availability of “premix” or combination fungicide formulations are common in agriculture. The cherry toolbox contains several of these product types: Adament (tebuconazole + trifloxystrobin), Pristine (pyraclostrobin + boscalid), and Unicorn (tebuconazole + sulfur). When introduced, both modes of action had activity against the target organism, some level of resistance management was built into the products provided that they were used rationally. Given the resistance issues discussed below, it is no longer safe to assume that resistance management is “built-in” to premix formulation of two fungicide sites-of-action.
Qualitative or quantitative fungicide resistance (molecular mechanism of fungicide resistance)
Fungicides from FRAC Group 11 (QoIs) inhibit respiration by targeting the mitochondrial electron transport chain at protein complex III and block the transfer of electrons from cytochrome b to c1 which results in halting ATP synthesis. Consequently, the pathogen becomes deprived of energy for its growth and development during its most critical stage of spore germination and the establishment of infection. The genetic mutations at one or two key positions in cytochrome b gene disrupt fungicide efficacy and pathogen becomes resistant to Group 11 fungicides. Since these fungicides target the unique site of the pathogen cellular process, the pathogen resistance is qualitative and therefore “all or nothing”.
DMI fungicides (pyrimidines, imidazoles and triazoles) disrupt sterol biosynthesis that is critical to the integrity of the plasma membrane in pathogenic fungi. The compounds become ineffective when the target gene of the pathogen, erg11/ cyp51 is mutated at various key nucleotide positions. Additionally, other genetic changes that include cyp51 promotor disruption and ABC transporters also contribute to the fungicide inefficacies. Furthermore, the activity spectra of DMI fungicides are broad and FRAC warns about the presence of cross-resistance between various DMI compounds. Since various genetic mechanisms of the pathogen may be utilized in response to the DMI fungicide applications, the pathogen resistance to such fungicides is quantitative (rate dependent).
Local Research and Results
Our laboratory in 2017 received multiple reports of control failures in several Washington orchards, some of which had received as many as 12 fungicide applications for mildew control. The PNW cherry industry has long been dependent on various synthetic fungicide classes: FRAC Group 11 (QoI or strobilurin), FRAC Group 3 (DMI or SBI Class-I), FRAC Group 7 (SDHI), and FRAC Group 13 (quinoline, quinoxyfen, Quintec). Many of the 2017 control failures occurred in programs that were significantly reliant on Group 11 fungicides. Given the documentation of widespread resistance of the grapevine powdery mildew pathogen (Erysiphe necator) in Eastern Washington, and the epidemiological similarities between the powdery mildews of grapes and cherries, we suspected a similar scenario in PNW cherries.
We collected isolates of P. cerasi from orchards in all PNW production regions. These isolates were subjected to a bioassay that included treatment of foliar tissue with fungicides followed by inoculation. Powdery mildew grew on foliage were either 1) the fungus was insensitive to the fungicide or 2) the compounds were not designed to be used as protective fungicides and therefore not suited for our bioassay (e.g. Polyoxin-D, an eradicative fungicide). An important result was the growth of some isolates of P. cerasi on foliage treated with Group 11 (QoI or strobilurin) fungicides. These results required additional molecular testing that confirmed the presence of a mutation in P. cerasi that confers resistance to Group 11 fungicides.
Treatment of foliar tissue with Group 3 (DMI) fungicides revealed that several P. cerasi isolates were insensitive to these fungicides when used protectively and the pathogen established colonies under laboratory conditions. Molecular analysis showed a good correlation with some fungicide treatment experiments. By comparing different laboratory experiments, we also found that the P. cerasi resistance to DMI fungicides is quantitative in nature. This suggests that the pathogen has developed a spectrum of resistance (sensitive, intermediate resistance and, resistant) owing to the nature of fungicide compounds that target complex cellular processes. Our results confirmed that more than half of the P. cerasi isolates representing different production areas had developed various levels of DMI resistance. Given the quantitative nature of the resistance to Group 3 compounds, we do not yet completely understand the nature of cross-resistance within the group. The complete loss of DMIs would be devastating since several straight Group 3 and premix formulations containing Group 3 would become obsolete. Therefore, further research is needed to preserve and protect this important class of fungicides through aggressive resistance management in production areas where complete resistance is not observed.
Compounding the problem of resistance in Group 11 is the presence of cross-resistance within the group, meaning that if P. cerasi becomes resistant to one Group 11 compound (e.g. trifloxystrobin) it will be resistant to other compounds within that group (e.g. pyraclostrobin, azoxystrobin). Standalone and premix fungicides containing Group 11 compounds are presented in Table 1. One of the benefits of “premix” fungicide formulations is the presence of two compounds (having two different sites-of-action) active against the target organism. In our situation, this amounts to “built-in” resistance management. Given the cross-resistance issues seen for Group 11 compounds, this is a game-changer. It means that the resistance is not being managed for the remaining effective compound in the premix formulation. For example, the resistance to pyraclostrobin component of Pristine means that the built-in “resistance management” for boscalid is no longer effective. This increases the resistance risk to the remaining effective compound boscalid. Cross-resistance among Group 3 compounds is less obvious due to its quantitative nature, i.e. given cross-resistance between Group 3 compounds, it is unclear how this would translate between compounds given the rate-dependent nature. For example, if an isolate is insensitive to the highest labeled rate of fenarimol, it is unclear whether it is also insensitive to the highest labeled rates of myclobutanil, triflumizole, metconazole, and tebuconazole. However, if there is resistance to the Group 3 component of a premix formulation, the management of resistance to the remaining compound is not accomplished.
We identified resistance to Group 3 and Group 11 in all production areas. Therefore, we are aware of the widespread geographical nature of the problem but do not yet know the extent of the problem within each production area. The actual spectrum of potential fungicide resistance within each orchard is partially a result of the fungicide application histories in that and neighboring orchards.
Table 1. Fungicides containing Group 11 and/or Group 3 compounds. Premix formulations are shaded in gray.
| Trade Name | Common Name | FRAC Group |
Comments |
| Abound | azoxystrobin | 11 | |
| Adament | trifloxystrobin + tebuconazole |
11 3 |
|
| Gem | trifloxystrobin | 11 | |
| Cabrio | pyraclostrobin | 11 | |
| Pristine | pyraclostrobin + boscalid |
11 7 |
|
| Luna Sensation | fluopyram + trifloxystrobin |
7 11 |
|
| Merivon | fluxapyroxad + pyraclostrobin |
7 11 |
|
| Quadris Top | difenoconazole | 3 | |
| azoxystrobin | 11 | ||
| Rally | myclobutanil | 3 | |
| Rubigan | fenarimol | 3 | Generic formulations available |
| Procure | triflumizole | 3 | |
| Orbit | propiconazole | 3 | Generic formulations available |
| Elite | tebuconazole | 3 | Generic formulations available |
| Unicorn | tebunconazole + sulfur |
3 M2 |
|
| Quash | metconazole | 3 | |
| Topguard Specialty Crops |
flutriafol | 3 |
Table 2. Non-group 11 and 3 fungicide options for management of powdery mildew of cherry.
| Trade Name | Common Name | FRAC Group (site of action) |
Resistance Risk |
| Vivando | metrafenone | 50 | moderate |
| Gatten | flutianil | U13 | moderate |
| Torino | cyflufenamid | U06 | moderate |
| Fontelis | penthiopyrad | 7 | moderate |
| Various manufacturers | sulfur | M2 | low |
| Various manufacturers | Horticultural oils (petroleum derived spray oils) | NC** | low |
| Oso* | polyoxin zinc salt | 19 | moderate |
| Polyoxin-D* | polyoxin zinc salt | 19 | moderate |
| Various products available | potassium bicarbonate | M2 | low |
| Sonata | Bacillus pumilus | BM02 | low |
| Serenade Max | Bacillus subtilis | BM02 | low |
| Mpede | Fungicidal soap | NC** | low |
| Neem oil | Extract of Azadirachta indica | NC** | |
| * not for use as a protectant; for use on established mildew colonies; **NC (not classified). |
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Given our documentation of resistance to Groups 11 and 3 compounds, growers should consider available alternatives. Fortunately, some effective fungicides (Table 2) remain and there are also some new synthetic fungicides with unique sites-of-action available.
General resistance management guidelines include the incorporation of cultural practices that lower disease pressure. Cultural practices such as vigor management and effective pruning both serve to lower disease pressure and improve spray penetration. The incorporation of these practices serves to lower selection pressure on pathogen populations. Always use fungicides in a protective, rather than reactive, manner. It is far easier to prevent powdery mildew than to cure it.
Additional guidelines include limiting the number of applications of individual modes of action per season and limiting sequential applications. Do not tank mix or alternate fungicides with the same FRAC number in a spray program. Quinoline compounds (Group 13) should be applied no more than 3 times per season and no more than twice in sequence. High-risk SDHI (FRAC Group 7) compounds or premixed formulations containing them should be preferably alternated 1:1 with other sites of action or groups. It is preferable to make only one application of any resistance-prone compound and then switch to a fungicide from a different class or FRAC group. But, the cost of this approach can be expensive in Eastern Washington. It also helps to tank-mix fungicides from different groups that are both effective against powdery mildew. Sulfur is a relatively inexpensive and effective companion product for mixing with medium- or high-risk compounds. Try to include it in every spray tank aimed at powdery mildew if permitted according to usage instructions on product labels and ensure that applying it is not detrimental to overall IPM objectives.
Always follow label instructions pertaining to application rates and intervals and always use a properly calibrated sprayer and sufficient spray volume to provide good coverage. Always make applications under good conditions.
Use pesticides with care. Apply them only to plants, animals, or sites listed on the labels. When mixing and applying pesticides, follow all label precautions to protect yourself and others around you. It is a violation of the law to disregard label directions. If pesticides are spilled on skin or clothing, remove clothing and wash skin thoroughly. Store pesticides in their original containers and keep them out of the reach of children, pets, and livestock.
YOU ARE REQUIRED BY LAW TO FOLLOW THE LABEL. It is a legal document. Always read the label before using any pesticide. You, the grower, are responsible for safe pesticide use. Trade (brand) names are provided for your reference only. No discrimination is intended, and other pesticides with the same active ingredient may be suitable. No endorsement is implied.
Acknowledgments
The authors appreciate financial support of this research by the Washington Tree Fruit Research Commission, Oregon Sweet Cherry Commission, Washington State Commission on Pesticide Registration, and Northwest Nursery Improvement Institute.
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