BY Wayne F. Wilcox, Professor
Department of Plant Pathology
NY State Agricultural Experiment Station
Cornell University, Geneva, NY
Powdery mildew (PM) afflicts vineyards worldwide. Eastern North
America has the dubious distinction of being home to this disease,
and we cannot grow grapes here without controlling it. Although
our climate is different from that in the western U.S., the fungus
responds similarly to environmental factors and control treatments
in both areas. While certain management details may vary among
regions, all control programs employ the same basic principles.
Within this context, Id like to discuss:
The fundamental biology of the disease;
When the crop is most susceptible to infection;
The basics of the fungicides that are used in control
The PM fungus overwinters either within infected buds, which germinate
to form mildewed flag shoots in the spring; or as
minute fruiting bodies (cleistothecia) that lodge in the bark
on the vine. They then release unique spores (ascospores) to infect
new foliage and young clusters in the spring. The subsequent spores
(conidia) produced on infected tissues are the same as those produced
on flag shoots, so further spread throughout the season is the
same regardless of the initial source of infection. Of course,
any program that provides good disease control on the fruit and
foliage during one growing season will limit the production of
both cleistothecia and flag shoots that perpetuate PM the following
Although cleistothecia do require at least a brief rain to release
their ascospores, neither these spores nor the conidia require
moisture in order to germinate and cause infection. Therefore,
the primary factor that controls the spread of PM is temperature.
Table I summarizes work conducted at the University of California,
Davis, in the 1950s, showing the number of days from the time
that a spore lands on a leaf until it forms a mildew colony producing
new spores capable of disease spread.
These data are extremely useful in formulating spray strategies,
and are the guts of the current UC Davis risk index
that has been used so effectively in California over the last
few years. Note that whereas the fungus can multiply rapidly when
temperatures are in the mid-60s to mid-80s, it is inactive while
temperatures remain above 90†F. In fact, some spores and colonies
are killed after relatively short exposures above 95†F, a fact
that also is accounted for by the risk index.
Another environmental factor that influences development of PM
is relative humidity (RH), although just how important a role
it plays remains unclear. In multiple tests on Riesling seedlings,
weve shown that disease severity increases progressively
to a point of doubling as the RH increases from 39% (the lowest
level that could be tested) up to an optimum near 85% to 90%.
(Rain or condensation on the leaves and fruit are detrimental
to disease development).
A model that guides control programs in German vineyards incorporates
humidity as one of its determining factors, and recent work at
UC Davis has provided further evidence that humidity affects the
development of this disease. Although not as influential as temperature,
higher humidities do increase the risk of PM. Thus, coastal regions
appear to face a double whammy, with both temperature
and humidity remaining highly favorable for PM throughout much
of the season.
Powdery mildew is a disease of young, juvenile tissues. Leaves
are highly susceptible to infection while they are expanding,
but become resistant soon after theyre fully expanded. Similarly,
recent research by colleagues at Cornell has shown that berries
are highly susceptible from bloom until shortly after fruit set,
but become much more resistant afterwards.
Although fruit on very susceptible varieties, such as Chardonnay,
may not become highly resistant until more than five weeks after
bloom (much earlier than previous literature has indicated), severe
berry infections appear to develop only when they are initiated
during the first few weeks after flowers open. Emphasizing this
point, repeated fungicide trials have demonstrated that sprays
applied from the start of bloom until two or three weeks later
are responsible for the lions share of PM control on the
berries. Conversely, significant berry infection at harvest can
almost always be traced back to a problem with the control program
during this early post-bloom period.
Now for the fine print:
In climates such as that of the northeastern
U.S., most flowers tend to open within a few days of each other.
Bloom is relatively easy to define, as are the specific
times when berries are highly susceptible to infection and when
they start to acquire significant resistance. However, in climates
such as that of California, particularly in certain locations
and/or years, flowers may open over a much longer period of
time, resulting in some berries acquiring age-related resistance
at a time when others are still young and highly susceptible.
This can extend the danger period in any given vineyard.
In the northeastern U.S. climate, infections
that occur about four weeks post-bloom (near bunch closure,
when berries are in their final stage of susceptibility) produce
few visible symptoms. However, such infections are visible with
magnification, and appear to provide an entry point for bunch
rot and other spoilage microorganisms.
| The message is simple: Unless temperatures are consistently high
enough to shut down the disease, the critical time to control PM on
the fruit is from the start of bloom until a few weeks later. The
key is to maintain good protection through bunch closure. Although
this is certainly not the only time to spray for PM, it is when you
should use your best PM fungicides and do the best possible job of
applying them. There will be times when you need to take shortcuts
in various operations during the season, but dont short-cut
your disease control program during this critical period.
Sulfur is a traditional material with two major positives: its
cheap and effective. Furthermore, its been used to control PM
around the world for nearly 150 years, with no development of resistance.
However, because sulfur acts largely through the vapor phase, its
activity is temperature-sensitive. Conventional wisdom says that sulfur
is relatively inactive at cool temps below 65†F, and can be phytotoxic
at temperatures above 85† to 90†F. Although sulfur products have been
used effectively under such suboptimal conditions, these
potential limitations should be recognized.
DMI fungicides do not inhibit spore germination, but attack the fungus
during its early growth stage within the plant. Thus, they provide
only limited residual or protective activity, but do provide significant
post-infection activity. This probably explains why they were once
so effective under extended spray intervals; that is, when new (unprotected)
leaves developed after one spray and became infected, control was
provided by the post-infection activity of the next spray. However,
their activity is declining in many parts of the world, due to increasing
levels of resistance developed by the PM fungus.
For this reason, very few New York growers still rely on the DMIs
for PM control during the critical bloom through fruit-set period.
Nevertheless, DMI fungicides have remained useful components in many
control programs, and it is beneficial to consider how resistance
to these materials develops and what you can do to minimize resistance
in order to maintain their utility.
Resistance to some fungicides (such as Benlate, Topsin-M, Vangard)
follows an all or nothing model. That is, nearly all individuals
in the fungal population are highly susceptible to the materials when
they are first introduced, but a few are virtually immune to any amount
of it. These individuals build up very quickly once enough sprays
are applied to kill off the susceptible population, and because the
resistant population is completely unaffected by the fungicide, control
failures can occur suddenly if the weather turns in the diseases
In contrast, resistance to DMI fungicides follows a shades of
gray model. In this case, no individuals are immune, but response
to the fungicides is very dose-dependent: an individual that is completely
inhibited at one dose may be only partially inhibited at a lower dose.
Furthermore, individuals within the pathogen populations vary widely
in their susceptibilities to the materials, showing a typical bell-shaped
curve with respect to the distribution of their sensitivities. That
is, most individuals will require an average dose for
control. Decreasing proportions will require progressively lower or
higher doses to achieve the same level of control.
It is important to recognize that fungicide rates are set by experimentation
(usually on populations with little previous exposure to related materials),
and that economic and regulatory pressures encourage labeling of the
lowest rates that will provide full control of about 98% or 99% of
the baseline population.
However, once such a fungicide (or group) has been introduced and
applied repeatedly, the most sensitive members of the population get
eliminated, leaving only those that require a full rate,
along with the original few that were only partially controlled by
that rate. If the dose is then reduced either intentionally
or through poor spray coverage many such individuals become
capable of growing to variable extents. Although they may be at least
partially controlled by each spray, they gradually build up to damaging
levels. Eventually, the fungicide just doesnt work as
well as it used to.
For powdery mildew, this creeping loss of control typically
happens more quickly in regions where many generations or disease
cycles occur every year (moderate summers) versus those with shorter
periods of fungal activity (long, hot summers).
Based on the above, there are a few simple rules to minimize development
of resistance to DMI fungicides and thus maintain their usefulness
into the future:
- Always use full labeled rates with excellent spray coverage.
Remember, the fungus doesnt react to the rate in the tank,
only to the rate on the vine.
- Limit the seasonal use of these materials (we recommend a maximum
of three applications per season).
- Use these fungicides early in the season or to maintain a clean
vineyard later, but do not use them to clean up a PM epidemic
thats gotten out of hand. (The larger the PM population,
the better the chance for selecting resistant individuals when
you spray the fungicide.)
The three principles were tested in New York during the 1996 and 1997
seasons, in a commercial vineyard of the hybrid cultivar Seyval (Chardonnay
parentage). A buildup of the DMI-resistant segment of the PM population
had resulted in Bayleton giving poor control by the early 1990s and
the performance of Rally (sold as Nova in the eastern
U.S.) was just starting to slip.
Various fungicide programs were imposed, using six spray applications
at 14-day intervals beginning two weeks pre-bloom and continuing through
veraison. By varying both the application rate of Rally and the rotational
pattern with sulfur, we examined a number of combination strategies:
- Rally at our recommended rate of 4oz/acre versus 50% of that
- Three sprays each of Rally and sulfur compared to six of Rally
- Rally in the first three sprays, before disease was apparent,
compared to the last three sprays, after significant PM was visible.
| Disease was rated before harvest, and 40 individual mildew colonies
from each treatment were tested in the lab to determine their resistance
status. In this way, we could calculate not only the total disease
control, but also the control of the resistant portion of the population
in each treatment.
The results in Table II demonstrate that the three theoretical anti-resistance
principles actually work under real world conditions. In this particular
case, limiting Rally to three applications per season in rotation
with sulfur, using the material before the disease was well established,
and maintaining our recommended rate of 4oz/acre provided the best
total disease control and the least selection of resistant mildew
The strobilurin fungicides (Abound, Flint, and Sovran, plus additional
materials still under development) appear to be the most important
new group of fungicides since introduction of the DMIs. Because the
strobies are likely to become increasingly important in
grape disease management, its worthwhile to understand how they
work. These are excellent protectant fungicides, providing their best
activity when present on the foliage or fruit before a spore lands
and tries to infect. They also provide some post-infection control
against PM, although it is less reliable and possibly more dangerous
in terms of future resistance development.
Additionally, the strobies show significant anti-sporulant
activity. That is, when applied after infection has occurred but before
symptoms develop, they may allow lesions to form but inhibit the production
of new spores from those lesions. This is a particularly significant
attribute, since it limits the infectious agents responsible for continued
The risk of fungal pathogens developing resistance to the strobies
appears to be high. To date, strobilurin resistance has followed the
Benlate (all or nothing) model, i.e, most resistant isolates are virtually
immune to the fungicides and multiply with impunity if they are not
controlled by some other material, such as by tank-mixing with sulfur.
Therefore, it will be critical to manage these materials carefully
in order to maintain their effectiveness over time.
Minimize the number of annual applications (cost should encourage
that!), use in strict rotation with other fungicide groups, and dont
spray a strobie as an emergency rescue treatment if PM
gets out of control.
The PM fungus is different from all other fungal pathogens of grapes
in that it grows primarily on the surface of infected tissues. Thus,
it is vulnerable to topical applications of various materials that
do not control other diseases, whose causal organisms are embedded
within the tissues and not exposed to such treatments.
Alternative products that are labeled for PM control on
grapes include various oils, potassium salts (monopotassium phosphate,
potassium bicarbonate), and dilute solutions of hydrogen peroxide.
In extensive tests with one such material monopotassium phosphate
weve found that it provides virtually no protective or
residual activity, i.e., no control when sprayed on plants that were
inoculated with the PM fungus one to 10 days later. In contrast, weve
found significant eradicative and anti-sporulant activity when it
was thoroughly applied one to seven days after inoculating with the
Similarly, weve gotten much better activity in field trials
when plants were sprayed every seven days (numerous post-infection
hits) compared to every 14 days with twice the rate (same
amount of fungicide per season, but only half as many hits).
I suspect that this scenario (a quick knockdown with little or no
protection against subsequent infections) is applicable to some of
the other alternatives (such as bicarbonates, oils, and
hydrogen peroxide), and that theyll need to be applied on a
more frequent basis than traditional fungicides. Of course, such activity
as there is assumes complete coverage of the leaves and fruit, which
often is problematical.
- The period of PM activity is determined by temperature. Extended
periods greater than 90†F will arrest its development, whereas
growth is explosive at temps in the mid-60s to mid-80s.
- Although less important than temperature, high humidity promotes
disease development and low humidity reduces it.
- Grape berries are highly susceptible to PM from flowering until
shortly after fruit set, and serious disease losses are a result
of control failures during this time. This is when attention should
be most sharply focused on control (best materials and application
techniques) if temperatures are at all favorable to the disease.
- Although DMI fungicides remain effective in many vineyards,
their efficacy has been compromised by resistance in many locations.
Limited-use, conscientious choices of rates, and thorough application
techniques should be implemented in order to maintain their usefulness.
- New strobilurin fungicides are extremely effective against PM,
but their use should be limited for resistance management purposes.
Two applications during the flowering and/or early post-flowering
period have provided superior control of fruit infections while
also providing supplementary control of Botrytis.
- PM is uniquely susceptible to topical applications of numerous
alternative products (oils, potassium salts, hydrogen peroxide).
However, these appear to act primarily as temporary eradicants,
with little or no protective activity against new infections.