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Fungicide Resistance for
Common Golf Course
Diseases
Frank P. Wong
Department of Plant Pathology & Microbiology
University of California, Riverside
TurfNet Webinar
April 7, 2009
Learning Objectives
Know what fungicide classes are at risk for
resistance development
Understand how resistance develops in
individuals and populations
Understand how resistance develops in
response to use fungicide use patterns
Know the major diseases where resistance is a
problem
Develop a strategy to delay & manage
resistance development for high risk diseases
www.turfpathology.ucr.edu
Understanding Fungicide Groups
www.turfpathology.ucr.edu
Fungicide Groups
At 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 & resistance
www.frac.info
www.turfpathology.ucr.edu
Multi-site vs Single-site inhibitors
Multi-site
Non-specific mode of action
Preventive, non-systemic
These have a minimal or no risk for resistance
Single-site
Affects a specific protein, enzyme or metabolic
process
Curative, systemic
These have a resistance risk
www.turfpathology.ucr.edu
Multi-site Inhibitors
FRAC Group Chemical Fungicide Example
Group
M1 Inorganics Copper Junction
metals
M2 Inorganic Sulphur
sulfur
M3 Dithio- Mancozeb Fore
carbamates Thiram Spotrete
M4 Phthalimides Captan Captan
M5 Chloronitriles Chlorothalonil Daconil
www.turfpathology.ucr.edu
Single-site Inhibitors
FRAC Chemical Group Fungicide Example
Group
1 Methyl benzimidazole Benomyl Benlate
carbamates (MBCs) Thiophanates Cleary's 3336
2 Dicarboxmides Iprodione Chipco 26GT
Vinclozlin Curalan
3 Demethylation-inhibitors Metconazole Tourney
(DMIs) Myclobutanil Eagle
Propiconazole Banner
Triadimefon Bayleton
Triticonazole Triton/trinity
4 Phenylamides Metalaxyl Subdue
7 Succinate Flutolanil Prostar
dehydrogenase inhibtors Boscalid Emerald
Resistance issues have been seen with groups highlighted in orange
www.turfpathology.ucr.edu
Single-site Inhibitors
FRAC Chemical Group Fungicide Example
Group
11 QoI-fungicides Azoxystrobin Heritage
Fluoxastrobin Disarm
Pyraclostrobin Insiginia
Trifloxystrobin Compass
12 Phenylpyrroles Fludioxonil Medallion
14 Aromatic hydrocarbons PCNB PCBN
Etridiazole Terrazole
19 Polyoxins Polyoxin-D Endorse
21 QiI-fungicides Cyazofamid Ranman
28 Carbamates Propamocarb Banol
Resistance issues have been seen with groups highlighted in orange
www.turfpathology.ucr.edu
Single-site Inhibitors
FRAC Chemical Group Fungicide Example
Group
33 Phosphonates Fosetyl-Al Aliette/Signature
Phosphor. Acid Alude
43 Benzimides Fluopicolide Stellar
44 Microbials Bacillus subtilis Rhapsody
Resistance issues have been seen with groups highlighted in orange
www.turfpathology.ucr.edu
Fungicide Resistance
Development
www.turfpathology.ucr.edu
Fungicide Resistance Development
Random mutations result in proteins that are
changed in the ability to bind to he fungicide
fungicide resulting in Biochemical Resistance
These mutations are passed along to the next
generation
Repeated fungicide applications select for
these mutants in a population
When the frequency in the population is high
enough you get Practical Resistance
www.turfpathology.ucr.edu
Selection for Practical Resistance
Naturally occurring
resistant individual Resistant
Initial Population Population
n
io
t
uc
od
pr
Re
The development of Practical Resistance is a step-wise process
Survivor Population
www.turfpathology.ucr.edu
Cross Resistance
Fungicides in the same group have the same
BMOA and target site
The 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
www.turfpathology.ucr.edu
Cross Resistance
However, cross resistance does not affect
fungicides in different fungicide groups
For example: an azoxystrobin (QoI) resistant
individual may still be sensitive to
thiophanate-methyl (MBC)
Resistance develops independently for
different fungicide groups
Double, triple, quadruple resistance can
happen, but each is independent
www.turfpathology.ucr.edu
Resistance Development
There are two kinds of resistance phenotypes
Qualitative
Individuals are immune to the fungicide group
i.e. MBCs, QoIs, phenylamides
Quantitative
Individuals are tolerant to the fungicide group
i.e. dicarboximides, DMIs
www.turfpathology.ucr.edu
Sensitive
Tolerant
Immune
0 ppm 10 ppm 1000 ppm
increasing fungicide concentration
www.turfpathology.ucr.edu
Theoretical Pattern of Qualitative
Resistance Development
This pattern
would be typical
for MBC, QoI and
phenylamide
resistance
Increasing rates
or applications
has no effect on
control of
resistant isolates
www.turfpathology.ucr.edu
Theoretical Pattern of Quantitative
Resistance Development
This pattern would
be typical for DMI
and dicarboximide
resistance
Increasing rates or
shortening
application intervals
can decrease the
impact of resistance
www.turfpathology.ucr.edu
Fitness of Resistant Fungi
Once a high frequency of resistance is
established, resistance is usually
permanent within the population
Resistant isolates in the field are just as
“fit” as the rest of the population
Once selection pressure is applied,
resistance may return quickly
www.turfpathology.ucr.edu
Delaying & Managing Resistance
www.turfpathology.ucr.edu
Resistance Risk
Many factors contribute to the risk of
resistance for any given fungicide
Mode of Pathogen
Action RISK Biology
Use Patterns
www.turfpathology.ucr.edu
Resistance Risk
Mutations that result in no normal change in
function to the target are at the highest risk of
practical resistance development
MBCs, QoIs, phenylamides
Mutations that result in some change in function
of the target by fungicide are moderately at risk
DMIs and dicarboximides
Some fungicides have not had issues; mutations
affecting these may result in less fit individuals
that do not survive to become trouble makers
www.turfpathology.ucr.edu
Relative Resistance Risk
LOWER RISK MODERATE RISK HIGHEST RISK
Spring Dead Spot Pythium Root Rot Anthracnose
Take-all Patch Brown Patch Dollar Spot
Summer Patch Yellow Patch Grey Leaf Spot
Southern Blight Pink Snow Mold
Resistance occurs more frequently in Pythium Blight
pathogens that:
Have a short generation time
Have a high frequency of
reproduction
Have long periods of conditions
favorable for disease development
www.turfpathology.ucr.edu
Risk: Use Patterns
Every application is a selection event
The fastest way to resistance is repeated
applications
Late 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
www.turfpathology.ucr.edu
Fungicide Alternation
Prevents repeated selection for resistant individuals
A B
Fungicide B indiscriminately controls Fungicide A - resistant
individuals and vice-versa
www.turfpathology.ucr.edu
Preventative Applications
Minimize late curative applications against
large populations
www.turfpathology.ucr.edu
What About Mixtures???
Mixtures are supposed to help delay
resistance by exposing pathogens to multiple
modes of action
Two or more fungicides decreases the
chance that one of them will fail completely
But if any of the mixing partners is site
specific, it is still a selection event
Multi-site fungicides are preferred mixing
partners as they carry no resistance risk
www.turfpathology.ucr.edu
Fungicide Mixtures
Prevents control failure caused by resistant
individuals by exposure to multiple modes of action.
Fungicide B indiscriminately controls Fungicide A -
A+B resistant individuals and vice-versa
You are more likely to get control with a mixture, but some selection for
resistance can still occur
www.turfpathology.ucr.edu
Assessing Resistance
Keep good records
what worked & what didn’t work
environmental conditions
equipment condition
Make sure calculations are right
Communicate well with crew
If all checks out – send samples for testing
Resistance can be confirmed by University
and manufacturer labs
www.turfpathology.ucr.edu
Managing Resistance
Once resistance is confirmed – you are
officially managing it
Due 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....
www.turfpathology.ucr.edu
Managing Resistance
Fungicide 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 greens
Within fairways
Within courses
Resistant pathogens that disperse well may be
able to spread to other parts of the course
www.turfpathology.ucr.edu
Managing Resistance: General Strategies
QoIs, MBCs, Phenylamides
Resistance to these = immunity
Switch to another fungicide class
DMIs
Bump up rates and shorten intervals
Dicarboximides
Bump up rates and shorten intervals
Reserve use for a few years from now
Incorporate multi-site fungicide use
Decrease disease pressure by using cultural
controls
www.turfpathology.ucr.edu
Resistance Issues for Specific
Diseases and Suggested
Strategies
www.turfpathology.ucr.edu
Dollar Spot
Sclerotinia homoeocarpa
www.turfpathology.ucr.edu
Dollar Spot
Dollar spot is the most commonly occurring
disease of turfgrass in the U.S.
The “800 pound gorilla” for fungicide
resistance for turf pathogens
Major issues:
Benzimidazole resistance
Dicarboxmide resistance
DMI resistance
www.turfpathology.ucr.edu
Dollar Spot: MBCs
MBC resistance is fairly widespread
Courses with a long history of MBC use can
no longer get good control with this fungicide
Limit the number of seasonal applications of
MBC fungicides
Tank mixes with a multi-site can still provide
good control
example: Daconil + 3336, Spectro (a
chlorothalonil/t-methyl premix)
www.turfpathology.ucr.edu
Dollar Spot: Dicarboximides
Current impact and distribution not well
documented
High rates and shorter application intervals
are recommended
Dicarboximide resistance appears to recede
over time
Michigan populations appeared to regain some
sensitivity when removed from rotation for 3+ yrs
(Vargas)
www.turfpathology.ucr.edu
Dollar Spot: DMIs
Mainly a problem on fairways when low rates
and long application intervals are used
When reduced effectiveness is observed,
increase rate or shorten application interval
Tank mixes with a multi-site will help control
the disease
www.turfpathology.ucr.edu
Dollar Spot: Alternatives
Increased nitrogen, leaf wetness
management, other cultural controls
Multi-site fungicides
Chlorothalonil
Be aware of seasonal restrictions
Single site fungicides
Boscalid (Emerald)
Biologicals
www.turfpathology.ucr.edu
Pythium Blight
www.turfpathology.ucr.edu
Pythium Blight on Ryegrass and
Poa trivialis overseeded on Bermuda
www.turfpathology.ucr.edu
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 process
Driven by multiple, repeated applications (seed
treatment, foliar)
www.turfpathology.ucr.edu
Fungicide Resistance: Pythium
QoI resistance has not been detected on
courses, but has been in laboratory tests
No more than 2 sequential applications
Use high rates of azoxystrobin, fluoxastrobin or
pyraclostrobin for best control
www.turfpathology.ucr.edu
Fungicide Alternatives: Pythium
For seedling blight where mefenoxam
resistance is present, azoxystrobin,
chloroneb, etridiazole, or phosphorous acid
fungicides may be effective
On established turf, pyraclostrobin,
fluoxastrobin, fosetyl-Al, mancozeb and
propamocarb can also be used
Fluopicolide and cyazofamid are effective on
established turf, but there is not enough data
on seedling protection
www.turfpathology.ucr.edu
Pythium Alternatives
Since seedlings are so vulnerable,
overseeding must be performed outside of
the danger window
avg RH + min Temp > 150 = danger
night time > 68F = danger
Delay overseeding to be outside of the window
Time preventive applications for Pythium on
established turf for the danger window
www.turfpathology.ucr.edu
Grey Leaf Spot
Pyricularia grisea
Courtesy Paul Vincelli, Univ. of Kentucky
Uddin Viji and Vincelli (2003) Plant Disease 87:880-889
www.turfpathology.ucr.edu
Fungicide Resistance: Gray Leaf Spot
Issues were reported just a few seasons after
QoIs were used widespread for GLS control
Likely due to the speed of the disease and its
ability to sporulate profusely
Unlike most cases of QoI-resistance, two
phenotypes were found
G143A cytb mutants: immune
F129L cytb mutants: tolerant
Unfortunately, immune isolates appeared to
dominate resistant locations
www.turfpathology.ucr.edu
QoI Resistance Management: GLS
Limit QoI applications for GLS control
Labels say no more than 2 – 4 sequential
applications
Conservatively, rotate to another fungicide group
after QoI application
Use no more than 2 applications per season for
GLS
Tank mixing with a contact (chlorothalonil)
will help reduce the impact of resistance
development
www.turfpathology.ucr.edu
GLS Fungicide Alternatives
Deploy resistant varieties of perennial
ryegrass to reduce the impact of GLS
Modify conditions that promote prolonged leaf
wetness periods
Reduce nitrogen fertility during summer
periods of GLS activity
Don’t increase mowing heights
www.turfpathology.ucr.edu
GLS Fungicide Alternatives
Chlorothalonil & mancozeb
Both products are effective for GLS control
and carry no resistance risk
Due to the explosiveness of the disease,
applications may be not be effective >14 days
Be aware of chlorothalonil restrictions
Tank mixing with site specific fungicides will
help reduce the impact of any fungicide
resistance
www.turfpathology.ucr.edu
GLS Fungicide Alternatives
Thiophanate-methyl (3336)
MBC-resistance has not been an issue
Reduced rates (4 to 6 oz vs 8 oz) may shorten
length of effectiveness
Use 1 to 2 applications/yr for GLS; rotate between
applications
Tank mix with chlorothalonil or use a premix
product (Spectro 90)
www.turfpathology.ucr.edu
GLS Fungicide Alternatives
DMI fungicides
Can provide good control of GLS, especially
when tank mixed with a multi-site fungicide
No resistance issues have been identified with
these products for GLS control
www.turfpathology.ucr.edu
Anthracnose
Colletotrichum graminicola
www.turfpathology.ucr.edu
Fungicide Resistance: Anthracnose
Resistant isolates detected starting 2002-
2003
QoIs
New York, New Jersey, Pennsylvania, Georgia,
California, Connecticut
MBCs
New York, New Jersey, Pennsylvania, Georgia,
California, Connecticut, Massachusetts, Ontario
Resistance to both is considered fairly
widespread by now
www.turfpathology.ucr.edu
Fungicide Resistance: Anthracnose
Resistance development is likely due to
Frequent curative applications with site-
specific fungicides
Activity of the fungus throughout the year =
exposure to greens fungicide applications
even when symptoms are not present
www.turfpathology.ucr.edu
MBC Resistance: Anthracnose
Fairly common at locations where it’s been
used repeatedly
Very poor to no control on resistant greens
Limit use on greens where the product is still
performing well
Curative applications are not recommended
www.turfpathology.ucr.edu
QoI Resistance: Anthracnose
Fairly common at locations where it’s been
used repeatedly
Very poor to no control on resistant greens
Curative applications are not recommended
Maintain use against other summer diseases
Summer Patch
Rapid Blight
Brown Patch
www.turfpathology.ucr.edu
DMI Resistance: Anthracnose
So far, DMI resistance has not been a true
problem for anthracnose management
High rate use of DMIs on greens is a likely
factor
However, differences between DMIs have
been detected that are correlated with
disease control
www.turfpathology.ucr.edu
Sensitivity to DMI-Fungicides:
0.15
0.090 ug/mL 0.75
45 ug/mL ug/mL 5.6
40
ug/mL
35
Frequency (%)
30
25
20
15
10
5
Triadimefon
0
Myclobutanil
-2.25
-2.00
-1.75
-1.50
-1.25
Propiconazole
-1.00
-0.75
-0.50
-0.25
0.00
Tebuconazole
0.25
0.50
0.75
1.00
1.25
Log ED50 (ug/mL) fungicide
1.50
www.turfpathology.ucr.edu
Intrinsic Activity of DMIs
Propiconazole (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 now
Differences in intrinsic activity are reflected in
actual field control; less active DMIs give
poorer control
www.turfpathology.ucr.edu
Rutgers 2002 Anthracnose Data
(Dr. Bruce Clarke)
% Area Diseased
Treatment 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
www.turfpathology.ucr.edu
Intrinsic Activity of DMIs
Right now, Banner MAXX appears to be the
most active DMI vs anthracnose
Other 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)
www.turfpathology.ucr.edu
Fungicide Strategies: Anthracnose
Use cultural controls & don’t stress grass
Use high labeled rates of DMIs for early
season control
Propiconazole appears to be the most active
Use QoIs and MBCs for other summer
diseases, but don’t rely on them for
anthracnose control
Use other fungicides preventively for mid
summer programs
www.turfpathology.ucr.edu
Fungicide Strategies: Anthracnose
Chlorothalonil
Very useful when applied preventively at 14 day
intervals
Save chlorothalonil applications for anthracnose when
other fungicides can be used for other diseases
Tank mix low rates with other fungicides if possible
Fludioxonil
0.33 to 0.5 oz Medallion can be used effectively on 14
day intervals
Limited to 1.5 oz/yr; rotate with other fungicides
www.turfpathology.ucr.edu
Fungicide Strategies: Anthracnose
Polyoxin-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 fungicides
Apply tank mix at 14 to 28 day intervals; if used every
28 days, rotate another fungicide at 14 days
The tank mix partner must also be effective
Chlorothalonil, fludioxonil & polyoxin-D are good
choices
www.turfpathology.ucr.edu
Microdochium Patch/Pink Snow Mold
www.turfpathology.ucr.edu
Fungicide Resistance: Pink Snow Mold
MBC 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 locations
Resistance development is likely due to
Long application intervals under snow cover
Curative applications without snow cover
www.turfpathology.ucr.edu
Fungicide Resistance: Pink Snow Mold
In cold weather locations, the impact of
resistance may be low
PCNB can be used effectively and no
resistance issues have been reported
In areas with PSM issues where PCNB
cannot be used safely, the impact will be
higher
www.turfpathology.ucr.edu
Resistance Management: Pink Snow Mold
Limit applications of MCB, dicarboximide, or
QoIs for PSM control to 1 to 2 applications
per season
Dicarboxmide applications are the least risky
of these fungicides
Tank mix these with a contact or a DMI
fungicide for best control
Use high labeled rates if conditions favorable
for PSM without snow cover are prolonged
(cool, wet weather)
www.turfpathology.ucr.edu
Fungicide Alternatives: Pink Snow Mold
Chlorothalonil, mancozeb and thiram are all
multi-site fungicide that can be used/tank
mixed with other applications
Fludioxonil
Polyoxin-D
DMI fungicides
Chlorothalonil + Fludioxonil + Propiconazole
www.turfpathology.ucr.edu
Developing Resistance
Management Strategies
www.turfpathology.ucr.edu
Developing a Management Strategy
Dollar spot, gray leaf spot, Pythium, anthracnose
ad pink snow mold are the diseases with the
most significant resistance issues
Each disease has a different group of fungicides
where resistance is an issue
These fungicides may not be affected by
resistance at your course, but should be
monitored closely
Performance issues should be correlated with
laboratory tests to confirm resistance
www.turfpathology.ucr.edu
Developing a Management Strategy
Because of cross-resistance, it is very important
to not use the same fungicide group repeatedly
Limiting the use of fungicide applications by
rotating fungicides will not stop resistance, but
will prolong the usefulness of the fungicides
Limit the use of single-site fungicides by
Incorporating other control measures
Keeping mutli-site fungicides in the program
Use mixtures to improve disease control, but
they will not stop resistance development
www.turfpathology.ucr.edu
Developing a Management Strategy
Minimize the use of late curative applications
High 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
www.turfpathology.ucr.edu
The Future for Fungicide Development
New fungicide registrations are becoming
harder and harder
Development is expensive ($100s of millions)
New fungicides must be extremely safe
Effective multi-site fungicides will be extremely rare
Legislation like the Food Quality Protection Act
may cancel/restrict some older fungicides
It is extremely important to prolong the
longevity of what we have now
www.turfpathology.ucr.edu
Summing it All Up
www.turfpathology.ucr.edu
Summary
Fungicide resistance is an issue that affects
site-specific fungicides
Multi-site fungicides have no resistance risk
Fungicide groups are based on target site
and mode of action
Each group affects a specific target in the
host
Mutations in the host target result in fungicide
resistance (biochemical resistance)
www.turfpathology.ucr.edu
Summary
Target site mutations affect all fungicides in a
fungicide group (cross resistance)
Fungicide applications select for individuals
with naturally occurring target site mutations
Repeated 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
www.turfpathology.ucr.edu
Summary
Resistant 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 applications
Late curative applications are worse because
they allow a larger population to be selected
against
www.turfpathology.ucr.edu
Summary
Alternating and rotating fungicides delays the
development of practical resistance
Fungicide mixtures can give increased
control and limit the impact of resistance, but
can still select for resistance development
Once 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
www.turfpathology.ucr.edu
Summary
Five disease are the most impacted by
resistance
Dollar spot – MBCs, dicarboximides, DMIs
Pythium - mefenoxam
Gray leaf spot – QoIs
Anthracnose – QoIs and MBCs
Pink Snow Mold – QoIs, MBCs and
dicarboximides
www.turfpathology.ucr.edu
For More Information
FRAC website: www.frac.info
McGrath, 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
www.turfpathology.ucr.edu
Contact the Speaker
Dr. Frank Wong
Department of Plant Pathology & Microbiology
(951) 315 -1010
[email protected]
www.turfpathology.ucr.edu


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