Understanding Fungicide Resistance: What You Can Do To Prevent It. Bruce B. Clarke Rutgers University

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1 Understanding Fungicide Resistance: What You Can Do To Prevent It Bruce B. Clarke Rutgers University

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3 Documented Cases of Resistance to Turfgrass Fungicide Pathogen Diseases Fungicides Sclerotinia homoeocarpa Dollar spot anilazine Dyrene iprodione Chipco Benzimidazoles Tersan 1991 Cleary 3336 SBIs Rubigan Banner Bayleton Micrdochium nivale Fusarium Patch Benzimidazoles Tersan 1991 Erysiphe graminis Powdery mildew Benzimidazoles, Tersan 1991 Pythium aphanidermatum Pythium Blight metalaxyl Subdue

4 Documented Cases of Resistance to Turfgrass Fungicide Pathogen Pyricularia grisea Diseases Gray Leaf Spot Fungicides Strobilurins Heritage Compass Colletotrichum cereale Anthracnose (ABR) Strobilurins Heritage Compass Benzimidazoles Cleary 3336

5 What is Fungicide Resistance? The stable, inheritable adjustment by a fungus to a fungicide, resulting in a less than normal sensitivity to that fungicide. (Dekker, 1995) Simply put, resistance is the ability of a fungus to remain relatively unaffected by a fungicide.

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8 Acute Resistance: - A continuing event brought on by alterations in the genetic makeup of the target organism that. - These features are inherited and are permanent in successive generations of the pathogen. - Resistance is persistent as long as the fungal strain is competitive / winter hardy

9 Transient Resistance: - A temporary condition brought on by climatic and/or management conditions that favor unusually severe outbreaks of a disease. - When transient resistance occurs, either the normal dosage levels of the fungicide fail to give satisfactory control or longevity of control is significantly reduced. - When the conditions that heightened the development of the disease no longer exist, the basic control level of the fungicide is restored.

10 Table 1. Chronological Development of Chemical Control Agents. (adapted from Delp, 1988) Date of Use Chemical Control Agent 1802 Lime sulfur 1885 Bordeaux Mixture 1913 Organomercurials 1934 Dithiocarbamates Chloronitrobenzenes Streptomycin*, Cycloheximide* Captan, Organo-tins, Dodine, Anilazine,

11 Table 1. Chronological Development of Chemical Control Agents. (adapted from Delp, 1988) - Cont d Date of Use Chemical Control Agent Chlorothalonil, Polyoxin*, Chloroneb, Organophosphates*, Carboximides*, Benzimidazoles* Sterol Biosynthesis Inhibitors, Phenylamides, Dicarboximides Additional compounds of the classes developed in the period Strobilurins (Heritage, Compass, Insignia, Disarm) Phenylpyrrole (Medallion), Carboximide (Emerald, Velista), ), QiI (Segway), DMIs (Trinity, Triton, Tourney, Torque), Mineral Oil (Civitas), Daconil Action (acibenzolar)

12 Reasons for fungicide non-performance Disease misdiagnosis Fungicide application strategies Fungicide application techniques Post spray irrigation/rainfall Cultural Practices Environment

13 How does a fungus develop resistance to a fungicide? Fungicide Resistance development is dependent upon the following: Fungicide mode of action (see Table 2) Specific Site vs. Multisite Fungicides Monogenic vs. Polygenic Resistance

14 How does a fungus develop resistance to a fungicide? Fungicide Resistance development is dependent upon the following: Fungicide mode of action (see Table 2)

15 Table 2. Fungicides for Turfgrass. Chemical Common Trade Names¹ Comments Family Names Aromatic Chloroneb Teremec SP Protectant Fungicide. Hydrocarbons Ethazole Koban, Terrazole Mode of Action: Quintozene PCNB, Turfcide 400, Interferes with mitosis +lipid metabolism Benzimidazole Benomyl Lebanon Fungicide Acropetal penetrant. Thiophaate- Fungo 50, Mode of Action: methyl Cleary s 3336, Fungicide bind tubulin subunits that result in mitotic arrest. Carboximides Flutolanil Prostar Acropetal penetrant. Boscalid Emerald Mode of Action: Penthiopyrad Velista Blocks activity of respiratory enzymes

16 Table 2. Fungicides for Turfgrass (Cont d) Chemical Common Trade Names¹ Comments Family Names Demethylation Triadimefon Bayleton Inhibitors (DMI) Fenarimol Rubigan Metaconazole Myclobutanil Propiconazole Tebuconazole Triticonazole Tourney Eagle Banner MAXX Torque Trinity Broad -spectrum, acropetal penetrant. Mode of Action: Inhibits sterol synthesis in fungal cell membrane. Dicarboximides Iprodione Chipco 26GT Localized penetrant. Vinclozolin Vorlan, Touché, Curalan Mode of Action: Affect DNA synthesis and lipids Dithiocarbamates Captan Captan Protectant fungicide. and Carbamates Mancozeb (a) Fore, Protect, Pentathlon Mode of Action: Propamocarb (b) Banol (a) Enzyme inactivation. Thiram (c) Spotrete, Defiant (b) Alters cell membrane function (c) Chelates metal ions Nitriles Chlorothalonil Daconil, Chlorostar, Protectant fungicide. Concorde, Echo, Manicure Mode of Action: Cell membrane

17 Table 2. Fungicides for Turfgrass (Cont d) Chemical Common Names Trade Names¹ Comments Family Phenylamides Metalaxyl Subdue, Apron Acropetal penetrant. Mode of Action: Mefanoxam Subdue MAXX,Quell Inhibits RNA synthesis. Phenylpyrrole Fludioxonil Medallion Protectant fungicide. Mode of Action: Causes cell lysis, inhibits amino acid uptake. Phosphonates Fosetyl Al Chipco Signature Systemic fungicide. Phosphite (salts of Alude, Magellan, Vital Mode of Action: Indirect and phosphorous acid Sign, Biophos, PK Plus direct fungitoxic effect. Polyoxins Polyoxin-D Endorse Localized penetrant. Mode of Action: Inhibits chitin used for fungal cell walls. Strobilurins Azoxystrobin Heritage Broad - spectrum, acropetal penetrant. (QoI s) Pyraclostrobin Insignia Localized penetrant. Trifloxystrobin Compass Mode of Action: fluoxystrobin Disarm Blocks fungi from generating ATP

18 Fungicides for Turfgrass Disease Control (Cont d) Chemical Common Trade Comments Family Names Names¹ QiI Cyazofamid Segway New fungicide class for the control of Pythium Diseases of Turf Mineral Oil Isoparifin Civitas * And the Recent Influx of Generic Products

19 Are all Fungicides within a Fungicide Class Equally Effective for the Control of Turfgrass Diseases Not Necessarily

20 Cross Resistance: - Resistance to more than one type of fungicide is being mediated by the same genetic factors. - Within a Chemical Family (i.e., Benzimidazoles (2), Dicarboximides (5) Multiple Resistance: - Resistance to more than one type of fungicide due to mutations of different genes. - Across Chemical Families (I.e., QoIs (12), Dicarboximides (5), and Benzimidazoles (2), Aromatic Hydrocarbons (1) and Dicarboximides (5)

21 Can a fungicide ever be used again if found to be resistant? It depends on the fitness (competitiveness) and winter hardiness of the Isolate

22 How does a fungus develop resistance to a fungicide? Fungicide Resistance development is dependent upon the following: Fungicide mode of action (see Table 2) Specific Site vs. Multisite Fungicides

23 Specific Site vs. Multisite Fungicides. Specific site fungicides: - Fungicides that inhibit only one vital function in the fungal cell. - Benzimidazoles (2), Phenylamides (8), DMIs (4), QoIs (12), Phosphonates (10) Multisite fungicides: - Fungicides that inhibit several vital functions in the fungal cell. -Nitriles (7), Dithiocarbamates (6), Dicarboximides (5), Aromatic Hydrocarbons (1)

24 How does a fungus develop resistance to a fungicide? Fungicide Resistance development is dependent upon the following: Fungicide mode of action (see Table 2) Specific Site vs. Multisite Fungicides Monogenic vs. Polygenic Resistance

25 Monogenic vs. Polygenic Resistance. Monogenic Resistance: - Factors for resistance are controlled by one gene. - Benzimidazoles (2), Phenylamides (8), Dicarboximides (5) Polygenic Resistance: - Factors for resistance are controlled by more than one gene. - All turf other fungicides

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28 Which fungicides are at risk for developing fungal resistance?

29 Table 3. Potential for development of resistance to certain turfgrass fungicides Fungicide Genetic Factor Site of Action Resistance Risk Level Benzimidazoles Monogenic Single Very High Phenylamides Monogenic Single Very High Strobilurins Mono and Poly Single High Moderate High Propamocarb Polygenic Single Moderate High Fosetyl Al Polygenic Single Moderate DMI Polygenic Single Moderate High

30 Table 3. Potential for development of resistance to certain turfgrass fungicides Fungicide Genetic Site of Action Resistance Risk Level Factor Polyoxins Polygenic (?) Single Moderate - High Carboximide Polygenic Single Moderate High Dicarboximides Monogenic Multiple Moderate Aromatic Hydrocarbons Polygenic Multiple Low Dithiocarbamates Polygenic Multiple Low Nitriles Polygenic Multiple Low

31 What are the strategies for combating resistance? 1. Rotate among fungicides. 2. Annual rotation of fungicides. 3. Tank mixing fungicides. 4. Reduced rate tank mixing of fungicides. 5. Combinations of Tank Mixing and Rotation. 6. Limiting number of sprays per season. 7. Proper timing (avoid once disease is active). 8. Use fungicide until you have resistance. 9. Withdrawal of fungicide. 10. Use proper mgm t techniques to reduce disease.

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