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Fungicide Resistance for Common Golf Course Diseases
Frank P. WongFrank P. WongDepartment of Plant Pathology & MicrobiologyUniversity of California, Riverside
TurfNetTurfNet Webinar Webinar April 7, 2009April 7, 2009
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Learning ObjectivesKnow what fungicide classes are at risk for resistance developmentUnderstand how resistance develops in individuals and populationsUnderstand how resistance develops in response to use fungicide use patternsKnow the major diseases where resistance is a problem Develop a strategy to delay & manage resistance development for high risk diseases
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Understanding Fungicide Groups
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Fungicide GroupsAt least 40 different fungicide groups used in agriculture Groups are based on target site and biochemical mode of action (BMOA)FRAC is the intra-manufacturer group that oversees the classification of fungicide groups
FRAC website provides a lot of information on fungicide mode of action & resistancewww.frac.info
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Multi-site vs Single-site inhibitorsMulti-site
Non-specific mode of actionPreventive, non-systemicThese have a minimal or no risk for resistance
Single-siteAffects a specific protein, enzyme or metabolic processCurative, systemicThese have a resistance risk
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Multi-site InhibitorsFRAC Group Chemical
GroupFungicide Example
M1 Inorganics metals
Copper Junction
M2 Inorganic sulfur
Sulphur
M3 Dithio-carbamates
Mancozeb Thiram
ForeSpotrete
M4 Phthalimides Captan CaptanM5 Chloronitriles Chlorothalonil Daconil
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Single-site InhibitorsFRAC Group
Chemical Group Fungicide Example
1 Methyl benzimidazole carbamates (MBCs)
BenomylThiophanates
BenlateCleary's 3336
2 Dicarboxmides IprodioneVinclozlin
Chipco 26GTCuralan
3 Demethylation-inhibitors(DMIs)
MetconazoleMyclobutanilPropiconazoleTriadimefonTriticonazole
TourneyEagleBanner BayletonTriton/trinity
4 Phenylamides Metalaxyl Subdue7 Succinate
dehydrogenase inhibtorsFlutolanilBoscalid
ProstarEmerald
Resistance issues have been seen with groups highlighted in orange
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Single-site InhibitorsFRAC Group
Chemical Group Fungicide Example
11 QoI-fungicides AzoxystrobinFluoxastrobinPyraclostrobinTrifloxystrobin
HeritageDisarmInsiginiaCompass
12 Phenylpyrroles Fludioxonil Medallion14 Aromatic hydrocarbons PCNB
EtridiazolePCBNTerrazole
19 Polyoxins Polyoxin-D Endorse21 QiI-fungicides Cyazofamid Ranman28 Carbamates Propamocarb Banol
Resistance issues have been seen with groups highlighted in orange
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Single-site InhibitorsFRAC Group
Chemical Group Fungicide Example
33 Phosphonates Fosetyl-AlPhosphor. Acid
Aliette/SignatureAlude
43 Benzimides Fluopicolide Stellar44 Microbials Bacillus subtilis Rhapsody
Resistance issues have been seen with groups highlighted in orange
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Fungicide Resistance Development
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Fungicide Resistance DevelopmentRandom mutations result in proteins that are changed in the ability to bind to he fungicide fungicide resulting in Biochemical ResistanceThese mutations are passed along to the next generationRepeated fungicide applications select for these mutants in a populationWhen the frequency in the population is high enough you get Practical Resistance
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Selection for Practical Resistance
Initial PopulationResistant Population
Survivor Population
Repro
duct
ion
The development of Practical Resistance is a step-wise process
Naturally occurring resistant individual
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Cross ResistanceFungicides in the same group have the same BMOA and target siteThe biochemical mechanism of resistance will affect the binding of all fungicides from the same fungicide group to the target site
For example: azoxystrobin resistant individuals are resistant to other QoIs like pyraclostrobin, fluoxastrobin or trifloxystrobin
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Cross ResistanceHowever, cross resistance does not affect fungicides in different fungicide groupsFor example: an azoxystrobin (QoI) resistant individual may still be sensitive to thiophanate-methyl (MBC) Resistance develops independently for different fungicide groupsDouble, triple, quadruple resistance can happen, but each is independent
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Resistance DevelopmentThere are two kinds of resistance phenotypes Qualitative
Individuals are immune to the fungicide groupi.e. MBCs, QoIs, phenylamides
QuantitativeIndividuals are tolerant to the fungicide groupi.e. dicarboximides, DMIs
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increasing fungicide concentration
Sensitive
Tolerant
Immune
0 ppm 10 ppm 1000 ppm
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Theoretical Pattern of Qualitative Resistance Development
This pattern would be typical for MBC, QoI and phenylamideresistance
Increasing rates or applications has no effect on control of resistant isolates
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Theoretical Pattern of Quantitative Resistance Development
This pattern would be typical for DMI and dicarboximideresistance
Increasing rates or shortening application intervals can decrease the impact of resistance
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Fitness of Resistant FungiOnce a high frequency of resistance is established, resistance is usually permanent within the populationResistant isolates in the field are just as “fit” as the rest of the populationOnce selection pressure is applied, resistance may return quickly
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Delaying & Managing Resistance
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Resistance RiskMany factors contribute to the risk of resistance for any given fungicide
RISKMode of Action
Use Patterns
PathogenBiology
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Resistance RiskMutations that result in no normal change in function to the target are at the highest risk of practical resistance development
MBCs, QoIs, phenylamidesMutations that result in some change in function of the target by fungicide are moderately at risk
DMIs and dicarboximidesSome fungicides have not had issues; mutations affecting these may result in less fit individuals that do not survive to become trouble makers
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Relative Resistance Risk
Spring Dead Spot
Take-all Patch
Summer Patch
Pythium Root Rot
Brown Patch
Yellow Patch
Southern Blight
Anthracnose
Dollar Spot
Grey Leaf Spot
Pink Snow Mold
Pythium Blight
HIGHEST RISKHIGHEST RISKMODERATE RISKMODERATE RISKLOWER RISKLOWER RISK
Resistance occurs more frequently in pathogens that:
Have a short generation timeHave a high frequency of reproductionHave long periods of conditions favorable for disease development
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Risk: Use PatternsEvery application is a selection eventThe fastest way to resistance is repeated applicationsLate curative and reduced rate applications are worse:
Incomplete control & selection against a larger population
Limit total applications from a fungicide group by alternation or reducing overall use by using cultural controls
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Fungicide AlternationPrevents repeated selection for resistant individuals
A B
Fungicide B indiscriminately controls Fungicide A - resistant individuals and vice-versa
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Preventative Applications
Minimize late curative applications against large populations
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What About Mixtures???Mixtures are supposed to help delay resistance by exposing pathogens to multiple modes of actionTwo or more fungicides decreases the chance that one of them will fail completelyBut if any of the mixing partners is site specific, it is still a selection eventMulti-site fungicides are preferred mixing partners as they carry no resistance risk
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Fungicide MixturesPrevents control failure caused by resistant
individuals by exposure to multiple modes of action. Fungicide B indiscriminately controls Fungicide A -
resistant individuals and vice-versaA+B
You are more likely to get control with a mixture, but some selection for resistance can still occur
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Assessing ResistanceKeep good records
what worked & what didn’t workenvironmental conditionsequipment condition
Make sure calculations are rightCommunicate well with crewIf all checks out – send samples for testingResistance can be confirmed by University and manufacturer labs
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Managing ResistanceOnce resistance is confirmed – you are officially managing itDue to cross resistance – the whole fungicide class is affected
ex – Heritage resistant GLS is also Compass and Insignia resistant
Resistance does not mean to give up a fungicide class just yet....
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Managing ResistanceFungicide resistance development is independent for pathogens
example: losing QoIs on anthracnose doesn’t mean you’ve lost it for brown patch
Resistance can be localized Within greensWithin fairways Within courses
Resistant pathogens that disperse well may be able to spread to other parts of the course
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Managing Resistance: General StrategiesQoIs, MBCs, Phenylamides
Resistance to these = immunity Switch to another fungicide class
DMIsBump up rates and shorten intervals
DicarboximidesBump up rates and shorten intervalsReserve use for a few years from now
Incorporate multi-site fungicide useDecrease disease pressure by using cultural controls
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Resistance Issues for Specific Diseases and Suggested
Strategies
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Dollar SpotSclerotinia homoeocarpa
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Dollar SpotDollar spot is the most commonly occurring disease of turfgrass in the U.S.The “800 pound gorilla” for fungicide resistance for turf pathogensMajor issues:
Benzimidazole resistanceDicarboxmide resistanceDMI resistance
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Dollar Spot: MBCsMBC resistance is fairly widespreadCourses with a long history of MBC use can no longer get good control with this fungicideLimit the number of seasonal applications of MBC fungicidesTank mixes with a multi-site can still provide good control example: Daconil + 3336, Spectro (a chlorothalonil/t-methyl premix)
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Dollar Spot: DicarboximidesCurrent impact and distribution not well documentedHigh rates and shorter application intervals are recommendedDicarboximide resistance appears to recede over timeMichigan populations appeared to regain some sensitivity when removed from rotation for 3+ yrs (Vargas)
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Dollar Spot: DMIsMainly a problem on fairways when low rates and long application intervals are usedWhen reduced effectiveness is observed, increase rate or shorten application intervalTank mixes with a multi-site will help control the disease
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Dollar Spot: Alternatives Increased nitrogen, leaf wetness management, other cultural controlsMulti-site fungicides
ChlorothalonilBe aware of seasonal restrictions
Single site fungicidesBoscalid (Emerald)Biologicals
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Pythium BlightPythium Blight
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Pythium Blight on Ryegrass and Pythium Blight on Ryegrass and Poa trivialisPoa trivialis overseeded on Bermudaoverseeded on Bermuda
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Fungicide Resistance: Pythium Resistance to metalaxyl/mefenoxam (Subdue) is probably the biggest issue for Pythium
Cases reported from multiple sites since 1980s (P. L. Sanders 1984)Mefenoxam still used frequently for control
Impact is the greatest for protection of seedlings during the overseeding processDriven by multiple, repeated applications (seed treatment, foliar)
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Fungicide Resistance: Pythium QoI resistance has not been detected on courses, but has been in laboratory tests
No more than 2 sequential applicationsUse high rates of azoxystrobin, fluoxastrobin or pyraclostrobin for best control
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Fungicide Alternatives: PythiumFor seedling blight where mefenoxam resistance is present, azoxystrobin, chloroneb, etridiazole, or phosphorous acid fungicides may be effectiveOn established turf, pyraclostrobin, fluoxastrobin, fosetyl-Al, mancozeb and propamocarb can also be usedFluopicolide and cyazofamid are effective on established turf, but there is not enough data on seedling protection
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Pythium AlternativesSince seedlings are so vulnerable, overseeding must be performed outside of the danger window
avg RH + min Temp > 150 = dangernight time > 68F = dangerDelay overseeding to be outside of the window
Time preventive applications for Pythium on established turf for the danger window
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Grey Leaf SpotPyricularia grisea
Courtesy Paul Vincelli, Univ. of KentuckyUddin Viji and Vincelli (2003) Plant Disease 87:880-889
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Fungicide Resistance: Gray Leaf SpotIssues were reported just a few seasons after QoIs were used widespread for GLS controlLikely due to the speed of the disease and its ability to sporulate profuselyUnlike most cases of QoI-resistance, two phenotypes were found
G143A cytb mutants: immuneF129L cytb mutants: tolerant
Unfortunately, immune isolates appeared to dominate resistant locations
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QoI Resistance Management: GLSLimit QoI applications for GLS control
Labels say no more than 2 – 4 sequential applicationsConservatively, rotate to another fungicide group after QoI applicationUse no more than 2 applications per season for GLS
Tank mixing with a contact (chlorothalonil) will help reduce the impact of resistance development
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GLS Fungicide AlternativesDeploy resistant varieties of perennial ryegrass to reduce the impact of GLSModify conditions that promote prolonged leaf wetness periodsReduce nitrogen fertility during summer periods of GLS activityDon’t increase mowing heights
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GLS Fungicide AlternativesChlorothalonil & mancozeb
Both products are effective for GLS control and carry no resistance riskDue to the explosiveness of the disease, applications may be not be effective >14 daysBe aware of chlorothalonil restrictionsTank mixing with site specific fungicides will help reduce the impact of any fungicide resistance
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GLS Fungicide AlternativesThiophanate-methyl (3336)
MBC-resistance has not been an issueReduced rates (4 to 6 oz vs 8 oz) may shorten length of effectiveness Use 1 to 2 applications/yr for GLS; rotate between applicationsTank mix with chlorothalonil or use a premix product (Spectro 90)
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GLS Fungicide AlternativesDMI fungicides
Can provide good control of GLS, especially when tank mixed with a multi-site fungicideNo resistance issues have been identified with these products for GLS control
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AnthracnoseColletotrichum graminicola
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Fungicide Resistance: AnthracnoseResistant isolates detected starting 2002-2003QoIs
New York, New Jersey, Pennsylvania, Georgia, California, Connecticut
MBCsNew York, New Jersey, Pennsylvania, Georgia, California, Connecticut, Massachusetts, Ontario
Resistance to both is considered fairly widespread by now
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Fungicide Resistance: AnthracnoseResistance development is likely due to
Frequent curative applications with site-specific fungicidesActivity of the fungus throughout the year = exposure to greens fungicide applications even when symptoms are not present
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MBC Resistance: AnthracnoseFairly common at locations where it’s been used repeatedlyVery poor to no control on resistant greensLimit use on greens where the product is still performing wellCurative applications are not recommended
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QoI Resistance: AnthracnoseFairly common at locations where it’s been used repeatedlyVery poor to no control on resistant greensCurative applications are not recommendedMaintain use against other summer diseases
Summer Patch Rapid Blight Brown Patch
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DMI Resistance: AnthracnoseSo far, DMI resistance has not been a true problem for anthracnose managementHigh rate use of DMIs on greens is a likely factorHowever, differences between DMIs have been detected that are correlated with disease control
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-2.2
5
-2.0
0
-1.7
5
-1.5
0
-1.2
5
-1.0
0
-0.7
5
-0.5
0
-0.2
5
0.00
0.25
0.50
0.75
1.00
1.25
1.50
Tebuconazole
PropiconazoleMyclobutanil
Triadimefon0
5
10
15
20
25
30
35
40
45
Freq
uenc
y (%
)
Log ED50 (ug/mL) fungicide
Sensitivity to DMI-Fungicides:
0.090ug/mL
0.15ug/mL 0.75
ug/mL 5.6ug/mL
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Intrinsic Activity of DMIsPropiconazole (Banner MAXX) appeared 7X more active than myclobutanil (Eagle) and 35X more active than triadimefon (Bayleton)Tebuconazole (Lynx) was very active, but it is in registration limbo right nowDifferences in intrinsic activity are reflected in actual field control; less active DMIs give poorer control
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Rutgers 2002 Anthracnose Data(Dr. Bruce Clarke)
% Area DiseasedTreatment 18 Jul 14 Aug 10 Sep
Eagle 40W (1 oz) 3.3 10.0 32.8
Banner MAXX (1 fl oz) 0.8 1.3 7.5
Lynx 45W (1.1 oz) 0.0 0.0 0.8
Bayleton 50DF (1 oz) 7.3 60.3 78.5
All treatments applied at 14 day intervals, 2 gal/M
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Intrinsic Activity of DMIsRight now, Banner MAXX appears to be the most active DMI vs anthracnoseOther DMIs are being examined right now, and not enough data exists to make a clear recommendation on these
Triticonazole (Trinity or Chipco Triton)Metconazole (Tourney)
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Fungicide Strategies: AnthracnoseUse cultural controls & don’t stress grassUse high labeled rates of DMIs for early season controlPropiconazole appears to be the most activeUse QoIs and MBCs for other summer diseases, but don’t rely on them for anthracnose controlUse other fungicides preventively for mid summer programs
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Fungicide Strategies: AnthracnoseChlorothalonil
Very useful when applied preventively at 14 day intervals Save chlorothalonil applications for anthracnose when other fungicides can be used for other diseasesTank mix low rates with other fungicides if possible
Fludioxonil 0.33 to 0.5 oz Medallion can be used effectively on 14 day intervalsLimited to 1.5 oz/yr; rotate with other fungicides
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Fungicide Strategies: AnthracnosePolyoxin-D
Use 4 oz preventively at 14 day intervals Rotate with other fungicides
Fosetyl-Al (Chipco Signature) Use 4 to 8 oz of the pigmented form to tank mix with other fungicidesApply tank mix at 14 to 28 day intervals; if used every 28 days, rotate another fungicide at 14 daysThe tank mix partner must also be effectiveChlorothalonil, fludioxonil & polyoxin-D are good choices
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Microdochium Patch/Pink Snow Mold
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Fungicide Resistance: Pink Snow MoldMBC and dicarboximide resistance have been known to be present since the 1980s, as first reported in Washington State.Resistance to QoIs has been observed in California; likely in other locationsResistance development is likely due to
Long application intervals under snow coverCurative applications without snow cover
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Fungicide Resistance: Pink Snow MoldIn cold weather locations, the impact of resistance may be lowPCNB can be used effectively and no resistance issues have been reportedIn areas with PSM issues where PCNB cannot be used safely, the impact will be higher
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Resistance Management: Pink Snow MoldLimit applications of MCB, dicarboximide, or QoIs for PSM control to 1 to 2 applications per seasonDicarboxmide applications are the least risky of these fungicidesTank mix these with a contact or a DMI fungicide for best controlUse high labeled rates if conditions favorable for PSM without snow cover are prolonged (cool, wet weather)
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Fungicide Alternatives: Pink Snow MoldChlorothalonil, mancozeb and thiram are all multi-site fungicide that can be used/tank mixed with other applicationsFludioxonil Polyoxin-DDMI fungicidesChlorothalonil + Fludioxonil + Propiconazole
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Developing Resistance Management Strategies
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Developing a Management StrategyDollar spot, gray leaf spot, Pythium, anthracnose ad pink snow mold are the diseases with the most significant resistance issuesEach disease has a different group of fungicides where resistance is an issueThese fungicides may not be affected by resistance at your course, but should be monitored closelyPerformance issues should be correlated with laboratory tests to confirm resistance
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Developing a Management StrategyBecause of cross-resistance, it is very important to not use the same fungicide group repeatedlyLimiting the use of fungicide applications by rotating fungicides will not stop resistance, but will prolong the usefulness of the fungicidesLimit the use of single-site fungicides by
Incorporating other control measuresKeeping mutli-site fungicides in the program
Use mixtures to improve disease control, but they will not stop resistance development
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Developing a Management StrategyMinimize the use of late curative applicationsHigh rate strategies will improve DMI and dicarboximide effectiveness High rates may be useful for other fungicides where resistance has not yet been a problem (e.g. where resistance mechanisms are not fully understood)Even though some single-site fungicides do not currently have resistance issues, we should not overuse and abuse them
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The Future for Fungicide DevelopmentNew fungicide registrations are becoming harder and harder
Development is expensive ($100s of millions)New fungicides must be extremely safeEffective multi-site fungicides will be extremely rare
Legislation like the Food Quality Protection Act may cancel/restrict some older fungicidesIt is extremely important to prolong the longevity of what we have now
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Summing it All Up
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SummaryFungicide resistance is an issue that affects site-specific fungicidesMulti-site fungicides have no resistance riskFungicide groups are based on target site and mode of actionEach group affects a specific target in the host Mutations in the host target result in fungicide resistance (biochemical resistance)
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SummaryTarget site mutations affect all fungicides in a fungicide group (cross resistance)Fungicide applications select for individuals with naturally occurring target site mutationsRepeated applications increase the frequency of these individuals to a point where disease control is reduced (practical resistance)Resistance is usually not an issue that goes away once it develops
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SummaryResistant individuals are either immune or tolerant
Increasing fungicide rates can still control tolerant fungi but not immune fungi
The best way to select for resistance is repeated applicationsLate curative applications are worse because they allow a larger population to be selected against
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SummaryAlternating and rotating fungicides delays the development of practical resistanceFungicide mixtures can give increased control and limit the impact of resistance, but can still select for resistance developmentOnce resistance is observed and confirmed, you can manage resistance by choosing alternative control measures
Resistance must be delayed to other fungicides that are used as alternatives
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SummaryFive disease are the most impacted by resistanceDollar spot – MBCs, dicarboximides, DMIsPythium - mefenoxamGray leaf spot – QoIsAnthracnose – QoIs and MBCsPink Snow Mold – QoIs, MBCs and dicarboximides
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For More InformationFRAC website: www.frac.infoMcGrath, M.T. 2004. What are Fungicides. The Plant Health Instructor.
http://www.apsnet.org/education/introplantpath/topics/fungicides/default.htm
‘Chemical Approaches to Managing Plant Pathogens’ by W. Koeller in the Handbook of Pest Management edited by John R. Ruberson, CRC Press, 1999.Fungicide Resistance in North America, edited by C.J. Delp, APS Press, 1988
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Contact the SpeakerDr. Frank WongDepartment of Plant Pathology & Microbiology(951) 315 [email protected]