Mary K.
Hausbeck
Michigan State University, East Lansing
The University of Tennessee, Knoxville
Phytophthora capsici on Vegetable Crops:
Research Progress and Management Challenges
Phytophthora capsici was first described
by Leon H. Leonian at the New Mexico
Agricultural Research station in Las Cru-
ces in 1922 (65). In his report, he de-
scribed a novel species of Phytophthora
that caused considerable damage to chili
pepper plants in the fall of 1918. A year
later, the disease reappeared at the same
site and also affected surrounding farms.
During the late 1930s and early 1940s,
recurrent problems with P. capsici in the
Arkansas River Valley of Colorado were
described on several vegetable hosts (51–
55,103). The first reported occurrence of P.
capsici on a cucurbit crop occurred in
1937, when a 3.2-ha field of cucumbers
became diseased resulting in 100% of the
fruit rotting (51). By 1940, P. capsici had
also been described on eggplant, honeydew
melon fruit, summer squash, and tomato
fruit (52,103). The disease on tomatoes
was reportedly so severe that the viability
of the processing tomato industry in the
region was threatened.
These early reports mirror the situation
with P. capsici today on many modern
vegetable production farms, especially
those in the eastern United States
(4,72,84,94). Our research was initiated in
1997, when crop losses caused by P. cap-
sici threatened to bankrupt a number of
vegetable producers in Michigan. Growers
wanted to know why crop rotation and the
use of fungicides in well-drained fields had
not provided adequate protection against
full-scale epidemics. At that time, there
were fundamental gaps in our understand-
ing of P. capsici’s epidemiology in Michi-
gan, and it was difficult to answer these
questions with any degree of certainty. We
did not recognize the extent to which sex-
ual recombination and genetic diversity
could influence management options and
success. In particular, the fungicide me-
Corresponding author: M. K. Hausbeck
E-mail: hausbec1@msu.edu
Publication no. D-2004-1007-01F
© 2004 The American Phytopathological Society
1292 Plant Disease / Vol. 88 No. 12
Kurt H. Lamour
fenoxam was being applied by some grow-
ers, and the sensitivity of natural popula-
tions of P. capsici in Michigan to
mefenoxam was unknown at that time.
Here we review recent advances in our
understanding of P. capsici’s biology, in
particular the role of sexual reproduction,
and provide an overview of some of the
management challenges presented by this
information.
Host Range
and Disease Symptoms
In Michigan, there are 32,356 ha of
vegetables (currently valued at approxi-
mately $134 million) that are highly sus-
ceptible to crown, root, and fruit rot caused
by P. capsici (Table 1). It is estimated that
when weather favors P. capsici, up to 25%
of the state’s value of these vulnerable
vegetables has been lost to disease. Indi-
vidual producers have experienced devas-
tating losses. When a farm in southern
Michigan was unable to harvest 121.4 ha
of diseased pickling cucumbers, an esti-
mated $300,000 was lost, along with a
$40,000 loss on approximately 40.5 ha of
processing tomatoes. Due to the impact of
P. capsici on this farm’s ability to meet
contractual obligations for cucumbers,
production of this crop was discontinued
(57). While ranked nationally as the num-
ber one producer and processor of cucum-
bers for pickling, Michigan also is a major
midwestern supplier of several vegetables
for fresh consumption and for processing
(49). In the north-central region of the
United States, P. capsici also is a reported
problem on cucumber in Wisconsin
(95,96), on pumpkin in Illinois (5), and on
pepper and cucurbit crops in Ohio (72).
The occurrence of P. capsici throughout
many vegetable growing regions in the
United States has prompted recent research
in Virginia (100), New York (70), Florida
(69), Arizona (68), North Carolina (66),
and Georgia (91).
P. capsici affects a wide range of solana-
ceous and cucurbit hosts worldwide
(17,27,43). In 1967, Satour and Butler (87)
reported that 45 species of cultivated
plants and weeds, representing 14 families
of flowering plants, were susceptible to P.
capsici. They found 19 species in 8 fami-
lies that were highly susceptible, with the
roots and crowns completely rotting 7 to
10 days after inoculation. This was the
widest host range study conducted to date.
Beans, lima beans, and soybeans were
reported (87) to be “immune” to P. capsici
infection under greenhouse conditions
highly favorable to infection. It is signifi-
cant, therefore, that in the summers of
2000 and 2001, P. capsici was isolated
from five commercial cultivars of lima
bean in Delaware, Maryland, and New
Jersey (21). Also, P. capsici has recently
been isolated from commercial snap bean
fields in northern Michigan, adding this
crop to the long list of susceptible crops
(35). These snap bean fields had a history
of zucchini cropping and P. capsici infesta-
tion. All isolates from snap bean were
pathogenic to cucumber fruit, and select
isolates were pathogenic to soybean plants
under laboratory conditions (36).
Disease caused by P. capsici may ini-
tially occur in the low areas of a field
where water accumulates. Growers often
assume that stunting or death of plants in
such areas is due to the “waterlogging” of
the roots, but infection by P. capsici may
be to blame. Under warm (25 to 30°C),
Table 1. Crops susceptible to Phytophthora
capsici under field conditions
Cucurbitaceae Solanaceae Leguminosae
Cantaloupe Bell pepper Snap bean
Cucumber Hot pepper Lima bean
Gourd Eggplant
Honeydew Tomato
melon
Pumpkin
Muskmelon
Summer
squash
Watermelon
Winter squash
Zucchini
wet conditions, root and crown infection of
pepper, zucchini, squash, and pumpkin
typically causes permanent wilt and plant
death (Fig. 1D –F,L). Plants often have
brown to black discolored roots and/or
crowns. In contrast, infected cucumber and
tomato plants may be relatively asympto-
matic or exhibit limited root rot and plant
stunting (Fig. 1A,B,M,N). However, when
a rainstorm splashed P. capsici–infested
soil onto the cotyledons of emerging cu-
cumbers, the entire 24.3-ha planting was
killed. Similarly, extremely rainy weather
that saturates soil for extended periods can
prompt a severe root and crown rot that
kills even established tomato plants. Dis-
ease symptoms on snap beans include
water-soaking on the leaves, stem necrosis
(Fig. 1O), and overall decline. Disease
symptoms were most severe on bean plants
located along the surface water drainage
pattern. P. capsici was recovered from
crown, stem, and leaf tissue (35).
While plant death is always a concern
for vegetable producers, fruit rot seems to
be especially insidious on cucurbits. In
general, infected cucurbit fruit initially
exhibit dark, water-soaked lesions (Fig.
1C,I), followed by a distinctive white
“powdered-sugar” layer of spores on the

Fig. 1. Symptoms of disease caused by Phytophthora capsici on: A to C, cucumber; D and E, yellow squash; F, hard squash; G, zuc-
chini; H, immature pumpkin; I, spaghetti squash; J, bell pepper; K and L, banana pepper; M and N, tomato; and O, snap bean.

Plant Disease / December 2004 1293

surface of the fruit 2 to 3 days later (Fig.
1A,G,H). While P. capsici regularly causes
a blight of pepper fruit in other growing
regions (84), this is not a common occur-
rence in Michigan and has been observed
only occasionally in the last several years
(Fig. 1J,K). Cucumber plants appear to
tolerate root infection by P. capsici, yet the
fruit are especially susceptible. In Michi-
gan, fields of healthy-appearing cucumber
vines with mature fruit have been aban-
doned in the field at harvest, or semi-truck
loads of fruit rejected at the processing
facility, due to rot. In our studies, we rou-
tinely observe a delay of at least 48 hours in
symptom expression in cucumber following
successful penetration by P. capsici (K. H.
Lamour and M. K. Hausbeck, unpublished
results). A similar 3- to 6-day lag prior to
symptom expression for P. capsici infecting
peppers has been described previously by
Schlub (89). This delay explains why
producers in Michigan who harvest
seemingly healthy fruit have had entire
loads rejected; fruit become infected while
in the field but the disease progresses during
storage and transit, with symptoms and/or
signs becoming evident after delivery to
the processor or retailer. The increased
temperatures during harvest, storage, and
transit may be an important factor.
The Pathogen
Early investigators recognized that the
genus Phytophthora exhibited striking
dissimilarities to many other fungal organ-
isms, but a full resolution of its taxonomic
and evolutionary standing would not be
made until DNA sequence analysis was
completed by Forster et al. in 1990. They
found that oomycetes are more closely
related to heterokont photosynthetic algae
than to members of the kingdom Fungi
(29). The modern description of P. capsici
as a species falls into Waterhouse’s Group
II (101) and is characterized by sporangia
that are conspicuously papillate with am-
phigynous oospores generally forming
only when A1 and A2 mating types are
paired. Information concerning the differ-
ent spore types produced by members of
the genus Phytophthora accumulated
slowly between 1940 and 1970. In 1970,
Waterhouse (101) provided a useful, and
still used, key for identifying isolates to
species based on the morphology of spo-
rangia and oospores and whether or not an
isolate could produce oospores in single
culture. Research with other Phytophthora
species established much of what is known
about the three dominant spore types pro-
duced by P. capsici (27). The thallus is
composed of coenocytic mycelium which
may give rise to lemon-shaped sporangia
borne on long caducous pedicels (1). When
sporangia are immersed in free water, they
differentiate to produce 20 to 40 bi-motile
swimming zoospores (Fig. 2) (8). Long-
term survival outside of host tissue is ac-
complished by the oospore (2,3,10,42,58–
60), which has a thick, multilayered wall
containing β-glucan and cellulose (27).
Oospores require a dormancy period of at
least a month (27,88) before germinating
directly or by forming sporangia (Fig. 2).
Sexual Reproduction
and Oospores
Approximately half of the 60 recognized
species in the genus Phytophthora are
homothallic (self-fertile), and for these
species, a single isolate is able to complete
the sexual stage and form oospores (27).
The remaining species, including P. cap-
sici, are heterothallic and require two com-
patibility types (=mating types), desig-
nated A1 and A2, to complete the sexual
stage (27). Oospores are formed when A1
and A2 compatibility types come into close
association (Fig. 2) (50). Each of the par-
ent isolates makes both male (antheridium)
and female (oogonium) gametangia once

Fig. 2. Disease cycle of Phytophthora capsici on cucumber. A, Dormant oospores germinate during wet conditions to produce
lemon-shaped sporangia, which may germinate directly or release swimming zoospores. Sporangia are produced on the roots,
crowns, and fruit of infected plants. B, In a cucumber field, sporangia and zoospores are disseminated by rain, irrigation, and drain-
age water, which can saturate soils and contribute to multiple cycles of inoculum that drive the disease during a single growing
season. C, Oospores are formed when A1 and A2 compatibility types come into close proximity; oospores are able to survive for
years in the soil.

1294 Plant Disease / Vol. 88 No. 12

the sexual stage has been initiated, and
self-fertilization is possible in obligate
outcrossing species (50).
To our knowledge, P. capsici is the only
heterothallic Phytophthora species that has
been shown to regularly complete the sex-
ual stage (outcross) in the United States
(37,56,58–62). The A1 and A2 mating
types both occur within natural field popu-
lations of P. capsici. The presence of A1
and A2 isolates of P. capsici in single
fields was reported in New Jersey in 1981
(76) and in North Carolina in 1990 (81).
Both mating types have been recovered
from farms surveyed in other states when
at least 15 isolates were collected from
diverse locations within a field (Table 2).
During 1997 and 1998, 14 Michigan farms
were sampled, with 473 isolates recovered
from cucurbit hosts and 30 from bell pep-
per (58). The A1 and A2 compatibility
types were recovered in roughly a 1:1 ratio
for eight farms. In 2001, we collected iso-
lates of P. capsici from fields in New York,
Connecticut, Pennsylvania, Ohio, North
Carolina, and California; similar trends
were revealed. When 429 isolates from
these states were screened for mating type,
53% (227) were A1 and 47% (202) were
A2 mating types. Both mating types were
recovered from every location, and the
A1/A2 ratio was close to 1:1 within loca-
tions (Table 2).
To determine if both mating types are
present in a field, the timing and spatial
scale of sampling are important. Multiple
cycles of infection and spore production
allow P. capsici to spread rapidly through-
out fields during warm, wet weather, and
samples collected from a few plants at the
height of an epidemic may erroneously
suggest that only a single mating type is
present (76,82). Samples collected every 2
weeks over a 3-month period from a single
field of squash in Michigan illustrated how
the percentage of unique genotypes fell
from 100% at the beginning of the epi-
demic to less than 30% by the end of the
growing season (59).
Papavizas et al. (76) provided the first
report of naturally occurring P. capsici
oospores in diseased host tissue in North
America. In Michigan, amphigynous oo-
spores typical of P. capsici have been
found in infected pumpkin, cucumber (Fig.
3C), and butternut squash fruit and in the
stems of P. capsici–infected yellow squash
seedlings. Interestingly, fungal gnat larvae
(Sciaridae) feeding on pumpkin fruit in-
fected with P. capsici had numerous oo-
spores in the digestive tracts of three speci-
mens (Fig. 3A,B). No attempt to determine
the viability of the excreted oospores was
made, but a study conducted with oospores
of Pythium spp. and fungal gnat larvae
indicates that oospores remain viable and
suggests that the gnat’s larval stage may
serve as a vector (33).
Although oospores have been consid-
ered the primary source of inoculum in the
field, little is known about the influence of
soil physical factors on infection of host
crops in oospore-infested soils. In vitro
treatment with chemicals and physical
factors that may interact with oospores in
the soil can provide information on germi-
nation and viability (44,48). Although
information about oospore germination in
situ is limited and reportedly difficult to
observe and definitively assay (44,64), it is
important to monitor oospore germination
in a simulated, complex soil setting (76).
Oospore survival has been successfully
studied in situ with P. infestans (23). Thus,
an important precedent for research on P.
capsici is in place.
The main impediment to detailed studies
of oospores and the inherent genetics
therein was primarily the difficulty in sepa-
rating and germinating oospores (65,92).
In 1968, Satour and Butler provided cru-
cial information concerning the generation
and germination of P. capsici oospores
(88). They reported that relatively young
oospores produced in paired cultures of P.
capsici germinated to produce recombinant
progeny after 30 days incubation. Prior to
this, it was generally thought that 6- to 9-
month incubation periods were necessary
for oospore germination. The progeny
from their crosses were shown to differ
from the parental types in both morphol-
ogy and pathogenicity. For example, one
progeny isolate exhibited increased viru-
lence on pepper compared with either of
the parents, which suggests that sexual
reproduction could lead to increased viru-
lence in the field. A number of important
milestones were reached in this investiga-
tion. A simple method for the production,
germination, and harvesting of oospore
progeny for P. capsici was formally pre-
sented, and the authors convincingly ar-
gued that proper media containing ample
nutrients as well as genetically compatible
parent isolates are required for successful
crosses. In addition, this work provided
convincing evidence for the potential role
of oospores in generating genetic variation
(88). In 1971, Polach and Webster (80)
corroborated this finding using the oospore
incubation and germination techniques of
Satour and Butler (88). Polach and Web-
ster (80) investigated 391 single oospore

Table 2. Phenotypic diversity of Phytophthora capsici isolates recovered from cucurbit and solana-
ceous hosts at diverse locations in the United States during 2001

No. of Compatibility type/mefenoxam sensitivityb

Location isolatesa A1/S A1/IS A1/I A2/S A2/IS A2/I
Connecticut 25 11 2 1 11 0 0
Pennsylvania 15 6 0 0 9 0 0
California 46 24 0 0 22 0 0
Ohio 20 8 1 0 11 0 0
New York (upstate) 44 10 9 2 10 11 2
New York (Long Island) 95 37 1 0 47 10 0
North Carolina 1 22 11 1 1 0 7 2
North Carolina 2 84 53 4 0 25 2 0
North Carolina 3 51 0 6 26 0 5 14
North Carolina 4 27 4 7 2 2 9 3
Total 429 164 31 32 137 44 21
a Isolates originated from single fields within a state except for New York and North Carolina,
which had 2 and 4 fields sampled, respectively. Fig. 3. Typical amphigynous oospores of
b Mefenoxam sensitivity determined by in vitro screening on 100 ppm AI amended media, with S Phytophthora capsici, A and B, in the gut
(sensitive) = <30% growth of control (GC), IS (intermediately sensitive) = between 30 and 90% of a fungal gnat that was feeding on a P.
GC, and I (insensitive) = >90% GC. capsici–infected pumpkin; and C, on the
fruit of a naturally infected cucumber.

Plant Disease / December 2004 1295

progeny from four mating reactions and
reported that the parent isolates differed in
their pathogenicity to cucurbit and solana-
ceous hosts and that segregation and re-
combination were observed for all the
characters studied.
Role of Sporangia and
Zoospores in Field Epidemics
Like many species in the genus Phy-
tophthora, P. capsici has the potential for
rapid polycyclic disease development from
a limited amount of inoculum (82). The
asexual sporangia and zoospores proved to
be much easier to manipulate and study
than the oospore, and it is not surprising
that the salient features of these spore
types were outlined relatively early
(40,73). P. capsici grows optimally be-
tween 25 and 28°C and can produce copi-
ous amounts of deciduous sporangia on the
surface of infected tissue (1,17,99,102).
When cucumber fruit were inoculated and
incubated at 60, 80, and 98% relative hu-
midity (RH) for 5 days, more sporangia
were produced at 60 and 80% RH than at
>90% RH (Fig. 4) (K. H. Lamour and M.
K. Hausbeck, unpublished results). Mature
sporangia are easily dislodged by rain and
irrigation and can directly germinate or,
when immersed in water, release 20 to 40
motile zoospores (40) that travel with wa-
ter in fields (89). Zoospores exhibit nega-
tive geotropism and chemotactically follow
nutrient gradients while swimming (27).
Once zoospores contact the plant surface,
they encyst and germinate to produce germ
tubes (40). Scanning electron microscopy
illustrates that zoospores are able to di-
rectly penetrate the intact cuticle within an
hour (K. H. Lamour and M. K. Hausbeck,
unpublished data). Penetration of leaf
surfaces by P. capsici occurs directly and
through natural openings such as stomata
(47). P. capsici produces an extra-cellular
macerating enzyme that likely plays a
significant role in breaching the host epi-
dermis and ramifying through susceptible
host tissue (104).
Fig. 4. Average number of sporangia
recovered from cucumber fruit inocu-
lated with Phytophthora capsici and
incubated at 60, 80, and 98% relative
humidity (RH) for 5 days. Error bars indi-
cate standard error of the means.
1296 Plant Disease / Vol. 88 No. 12
In general, sporangia and zoospores are
thought to be relatively ephemeral struc-
tures contributing to the spread of P. cap-
sici within a single growing season but
unlikely to survive the harsh conditions
typical of nonhost periods in North Amer-
ica (2,3,11,58,59,61,62). Results from
investigations with P. capsici in Michigan
suggest that overwintering of clonal inocu-
lum is rare but that reproduction of clonal
populations within a single season is sig-
nificant (58). Tracking a single population
of P. capsici over the course of the grow-
ing season in 1999 using molecular mark-
ers indicated that asexual spread increased
dramatically as the season progressed and
that a single clone accounted for approxi-
mately 50% of the isolates recovered in the
final one-third of the growing season (59).
Thus, the infection and subsequent sporu-
lation on host tissue and fruit likely play a
key role in driving the polycyclic phase of
disease development in the field. The num-
ber of sporangia on a single naturally in-
fected spaghetti squash fruit was estimated
to be 44 million with the potential to re-
lease 840 million zoospores (K. H. Lamour
and M. K. Hausbeck, unpublished results).
In addition to the epidemiological ad-
vantage provided by a large aboveground
reservoir of inoculum, there may be an
additional evolutionary advantage con-
ferred by the large number of hyaline spo-
rangia exposed to UV irradiation on the
surface of infected fruit. Fungicide insensi-
tivity was easily induced in P. capsici us-
ing UV irradiation (14), and it seems rea-
sonable that the thousands of sporangia
present on an infected cucurbit fruit repre-
sent a significant substrate for the effects
of UV-mediated mutation. Dekker (22)
states that the buildup of a chemical-resis-
tant pathogen population will occur faster
in a heavily sporulating pathogen on aerial
plant parts than in a slowly spreading,
soilborne pathogen, and cites as an exam-
ple that the buildup of metalaxyl resistance
in the aerially sporulating P. infestans was
much faster than occurred with P. cinna-
momi causing avocado root disease.
Sexual Reproduction
and Adaptation to PAFs
Historically, growers have relied on a
limited number of fungicides for control of
Phytophthora root, crown, and fruit rot.
The phenylamide class of fungicides
(PAF), specifically metalaxyl and the new-
est fungicide mefenoxam (Ridomil Gold
EC), has been used by many growers to
combat P. capsici. Mefenoxam is the active
enantiomer contained in the racemic fungi-
cide metalaxyl (77,78). Both compounds
are strongly fungicidal to sensitive isolates
(20,75), and isolates recovered from farms
without a history of PAF use are highly
sensitive to both mefenoxam and
metalaxyl (58,78).
Metalaxyl has been shown to specifi-
cally inhibit the incorporation of uridine
into RNA in sensitive oomycetes (20). The
mode of action of metalaxyl is postulated
to be site specific, and it was not surprising
when resistance surfaced in populations of
susceptible plant pathogens after PAFs
were introduced during the late 1970s (20).
As early as 1981, researchers working with
P. capsici demonstrated that insensitivity
to metalaxyl was readily selected for by
using sublethally amended media (12,13).
Insensitivity soon developed in natural
populations of oomycetous organisms
where metalaxyl was heavily relied upon
(18,34,46). Adaptation to PAFs is common
throughout the oomycetes (19,34) and is
generally accepted as inevitable due to
the specificity of this group of fungicides
(20). Studies characterizing the inher-
itance of mefenoxam insensitivity in P.
capsici suggest that insensitivity is
conferred by a single incompletely
dominant locus (58).
Recovering insensitive P. capsici iso-
lates from farms with a history of PAF use
is increasingly common in the United
States. Data from North Carolina, Michi-
gan, and New Jersey indicate that a signifi-
cant proportion of P. capsici populations
under PAF selection pressure may be inter-
mediately or fully insensitive to mefen-
oxam (28,58,77,78). Insensitivity to
mefenoxam, which also conferred insens-
itivity to metalaxyl, was reported from
field populations of P. capsici on bell pep-
per (77). The inheritance of mefenoxam
sensitivity was assessed in naturally occur-
ring populations of P. capsici in Michigan.
In Michigan, greater than half (55%) of the
498 isolates sampled were sensitive, 32%
were intermediate, and 13% were fully
insensitive to mefenoxam (58). Three
farms, two in North Carolina and one in
New York, had a history of mefenoxam
use, and insensitive isolates were recov-
ered from each (Table 2). Overall, 70%
(301) of the isolates were fully sensitive,
17% (75) were intermediately sensitive,
and 13% (53) were insensitive to me-
fenoxam. The majority (40) of the fully
insensitive isolates were recovered from a
single bell pepper field in North Carolina
with a history of mefenoxam use. In North
Carolina, the process of adaptation to me-
fenoxam appears to have occurred rapidly
(78).
Because only sensitive isolates of P.
capsici are controlled by the mefenoxam
fungicide (63), the observed control failure
in some Michigan fields during the last
few years is likely due to the development
and increasing incidence of P. capsici iso-
lates insensitive to this fungicide. Sexual
recombination appears to play an impor-
tant role in adaptation by generating fully
insensitive isolates (e.g., mating between
intermediately sensitive isolates) (Fig. 5).
A Michigan population of P. capsici com-
prised of intermediate and fully insensitive
isolates tracked for 3 years (1999 to 2001)
in the absence of PAF use showed no evi-
dence of reversion back to the wild-type,
PAF-sensitive, state (62).
Effective fungicides that act on a single
enzyme or molecular pathway exert sig-
nificant selection pressure favoring isolates
able to withstand the activity of the fungi-
cide. In the case of mefenoxam, there ap-
pears to be a low level of isolates harbor-
ing a mutation responsible for insensitivity
to mefenoxam. Application of mefenoxam
favors these isolates, and sexual reproduc-
tion results in numerous genetically unique
progeny carrying what was previously a
rare trait. Because of sexual reproduction,
the process of incorporating a novel advan-
tageous trait into numerous genetic back-
grounds makes it less likely that insensitive
isolates will be less fit than their fungicide-
sensitive wild-type counterparts. It is rea-
sonable to suspect that sexual recombina-
tion may play a similar role in the adapta-
tion of P. capsici to other fungicidal
compounds whether they are applied man-
ually or generated by resistant varieties of
plants.
Genetic Diversity
Significant molecular investigations into
the genetics of P. capsici do not appear in
the literature until the late 1980s and early
1990s, when isozyme and restriction frag-
ment length polymorphism (RFLP) analy-
sis of both mitochondrial and nuclear DNA
were conducted on isolates from widely
different geographical locations, years, and
hosts located in a worldwide Phytophthora
culture collection at the University of Cali-
fornia at Riverside (30,71,74). Results
Fig. 5. An illustration of how selection for mefenoxam resistance occurs in the field. A,
Sensitive Phytophthora capsici individuals are unable to infect when mefenoxam is
applied. B, Only the rare intermediately sensitive isolates produce oospores. C, The
process of only the resistant isolates mating and producing oospores is continued
when mefenoxam is applied in subsequent years.
from an isozyme study involving 113 P.
capsici isolates were interpreted as reveal-
ing two subgroups within the P. capsici
species (71). Subgroups are defined as
being significantly different based on spo-
rangial morphology and ontogeny. RFLP
investigation of mitochondrial DNA re-
vealed no patterns of similarity based on
host or geographical location (30). RFLP
analysis of nuclear DNA using low copy
number probes of 15 P. capsici isolates
indicated nuclear DNA diversity was high
(30). These early studies highlighted the
diversity of P. capsici on a worldwide
scale. In the United States, this genetic
diversity has been exploited to better un-
derstand how natural populations of P.
capsici are distributed in space and time.
Almost 15 years ago, J. B. Ristaino (81)
showed that morphological characters
varied widely in natural populations and
that variation in pathogenicity among so-
lanaceous and cucurbit hosts existed in
field populations. This work corroborated
earlier laboratory studies showing that
pathogenicity and virulence to tomato and
pepper segregate during sexual recombina-
tion and that sex can generate strains more
virulent than either parent (88). Mating
type and sensitivity to mefenoxam provide
a limited level of resolution, and choosing
among the many techniques available for
measuring variation at the DNA level can
be difficult due to the advantages and limi-
tations inherent in each. Because P. capsici
has the potential for significant polycyclic
reproduction, one of our primary goals was
to differentiate uniparental (clonal) line-
ages. This is an important consideration to
accurately determine how far P. capsici is
dispersed and if clonal lineages are able to
survive outside of hosts. The amplified
fragment length polymorphism (AFLP)
technique is useful for this type of differ-
entiation because it allows numerous
markers to be resolved simultaneously and
provides a robust sample across individual
genomes. The AFLP technique results in
the selective amplification of restriction
fragments from a digest of total genomic
DNA using the polymerase chain reaction
(PCR). The DNA fragments, called AFLP
markers, are resolved using a polyacryla-
mide gel or, if the PCR primers are labeled
with a fluorescent dye, a DNA sequencing
machine. An example of AFLP analysis by
automated DNA sequencing is shown in
Figure 6. The advantages to this technique
are its reproducibility and sensitivity (e.g.,
between 50 and 70 AFLP markers are re-
solved per reaction per P. capsici isolate)
(9). Characterization of 107 oospore prog-
eny from a laboratory cross between par-
ents with differing AFLP genotypes in-
dicated that the progeny were all
recombinant and that the AFLP markers
segregated as Mendelian characters (59).
A key expectation when studying out-
crossing populations is the recovery of
unique combinations of phenotypic and
molecular characters. If outcrossing is
occurring in natural populations of P. cap-
sici, then multiple combinations of mating
type, mefenoxam sensitivity, and AFLP
markers should be present (Tables 2 and 3)
(98). In Michigan, 70% (454) of the 646
isolates analyzed had unique AFLP pro-
files. In total, 94 AFLP markers were re-
solved but no single population had all 94
markers. Individual populations had be-
tween 68 and 80 AFLP markers, and iso-
lates were clearly more similar based on
geographic locations (60). The high num-
ber of unique AFLP profiles and high pro-
portion of polymorphic markers suggests
that populations residing at all monitored
locations are sexually active (Table 3).
Studies of individual populations over
multiple years indicated that the pools of
genetic diversity remained stable and that
outcrossing among locations was limited
(60–62). As expected for an organism with
the potential for significant polycyclic
disease development, clonal lineages were
detected and were shown to play an impor-
tant role in epidemic development (59–61).
But unlike oomycetes such as P. infestans,
where clonal lineages have made their way
around the world and have persisted for
many years (32), the clonal lineages of P.
capsici were confined in space to single
fields and in time to single years (61).
Management Strategies
and Challenges
As P. capsici has spread to more acreage
devoted to vegetables, producing vulner-
able crops has become a significant, and
Plant Disease / December 2004 1297
Fig. 6. Segments (approximately 90 of 500 bases) of electropherograms from amplified fragment length polymorphism (AFLP) pro-
files of genomic DNA from three Phytophthora capsici isolates recovered from water sources in Michigan. The AFLP profiles were
produced using a Beckman CEQ 8000 capillary genetic analysis system and visualized using the CEQ fragment analysis software.
Polymorphic markers of 325, 335, 349, 358, and 390 nucleotides are clearly visible.

contributing to the disease problem. Some

Table 3. Genetic diversity of Phytophthora capsici isolates recovered from locations in the United
States
Isolates
Location analyzed
Connecticut 12
Pennsylvania 15
California 20
Ohio 15
New York (upstate) 12
New York (Long Island) 42
North Carolina 57
a All isolates have unique multilocus amplified fragment length polymorphism (AFLP) profiles.
for some producers, an overwhelming
challenge. The future of the vegetable in-
dustry in Michigan and other regions of
the United States plagued by P. capsici is
at risk without long-term sustainable ap-
proaches such as genetic resistance and
remediation of infested sites. In the short
term, the economic risk of growing P. cap-
sici–susceptible crops may be reduced by
using several management tools. Ristaino
and Johnston (84) previously provided a
summary of management of this disease in
bell pepper.
Crop rotation. While crop rotation is an
important foundation of disease manage-
ment, the long-term survival of oospores in
absence of a host limits the effectiveness
of this strategy as a stand-alone tool. The
survivability of oospores has been clearly
demonstrated with a number of Phy-
weeds also may play an important role in
the survival of P. capsici from one growing
Unique AFLP markers Polymorphic season to another (31,79).
isolatesa resolved markers (%) Today, many vegetable producers in the
10 78 40 (51) United States recognize that cucurbit and
11 90 51 (57) solanaceous crops are at risk for P. capsici
11 81 42 (52) infection and rotate these crops with other
12 86 45 (52) vegetables (i.e., carrots, beans, onions, and
10 86 50 (58) asparagus are examples from Michigan) or
37 90 58 (64) agronomic crops (soybeans, alfalfa, small
52 88 49 (56)
grains). However, recent reports of com-
mercial losses in lima beans (21) and snap
beans (35,36) from this pathogen and sus-
ceptibility of soybeans (35,36) and other
tophthora spp., including P. capsici (3,11). commonly grown vegetables (97) under
Growers practicing even lengthy rotations laboratory conditions highlight the gaps in
(>5 years) to nonsusceptible hosts have our knowledge and standard management
experienced significant crop loss to P. cap- recommendations and suggest that guide-
sici. A spatiotemporal study conducted on lines for crop rotation should be re-evalu-
a Michigan farm used molecular tools to ated.
identify P. capsici isolates. The data sug- Exclusion. In Michigan, it does not ap-
gest that a P. capsici epidemic on squash in pear that P. capsici is dispersed over long
1999 was initiated by dormant oospores distances, and excluding the pathogen
generated 5 years previously, despite rota- from noninfested growing areas is empha-
tion to corn and soybeans (59). Although a sized to producers during extension pro-
minimum 3- to 4-year rotation to nonsus- grams and farm visits. Increased attention
ceptible hosts is recommended to limit the to the routes by which P. capsici may be
buildup of P. capsici (84), the availability introduced is warranted. Movement of
of noninfested land is becoming increas- other Phytophthora spp. via irrigation
ingly scarce. The development of agricul- water has been documented (27), and
ture land for urban use and the relatively aboveground water sources may play a role
low value of some field crops have forced in the long-distance movement of P. cap-
many vegetable producers to reduce their sici. Runoff water from infested fields can
crop rotation to only 1 or 2 years, thus transport the pathogen from diseased

1298 Plant Disease / Vol. 88 No. 12

plants to nearby water sources used for
irrigation. We began testing aboveground
water sources in Michigan for contamina-
tion with P. capsici during 2001 and recov-
ered the pathogen from irrigation ponds on
two farms (K. H. Lamour and M. K. Haus-
beck, unpublished data). Additional irriga-
tion water sources were monitored for P.
capsici in 2002 and 2003, and the patho-
gen was frequently detected in a river,
creek, and a naturally fed pond (35,36). All
of these water sources were located near
crops infected with P. capsici. Prior to this
research, the presence of P. capsici in
Michigan irrigation sources had not been
reported. Another potential source of P.
capsici–contaminated water may be from
vegetable processing facilities that apply
their waste water to nearby vegetable pro-
duction sites. Using water that may be
contaminated with P. capsici to irrigate
healthy crops must be avoided to limit
pathogen spread.
Identifying factors contributing to the
spread of P. capsici to new locations can
be challenging. Producers are warned
against dumping P. capsici–infected pro-
duce on or near their farms. However, a
survey of cultural practices in Michigan
indicated that in some cases producers
were spreading over- and under-size cull
and diseased fruit onto fields after return-
ing from processing stations. Historically,
some processors mandated that producers
haul culls and diseased fruit from the proc-
essing station for disposal in their fields
even if the fruit were from other farms. A
single fruit infected with both A1 and A2
mating types may contain thousands of
genetically unique oospores that can estab-
lish a resident population of P. capsici in a
field with no history of P. capsici prob-
lems. Once P. capsici is established in a
field, tillage and cultivation distribute dis-
eased plant material and spread oospores
throughout the field and soil profile. It is
possible that P. capsici may be dissemi-
nated to new fields via equipment even
when no remnants of diseased plant mate-
rial are visible.
Cultural control. Commonly recom-
mended cultural control strategies reflect
our understanding of the importance of
water in the epidemiology of P. capsici and
include planting into well-drained fields
and into raised beds whenever possible
(84). Excess moisture is the single most
important component to the initial infec-
tion and subsequent spread of P. capsici
(10,11,82,83,85,89,94). Similar findings
exist for many species in the genus Phy-
tophthora and are not surprising in light of
these organisms’ evolutionary ties to the
algae (25,26).
Since water plays a key role in disease
development (82,89), water is managed
based on the crop and the water dynamics
of the region. A significant problem in the
eastern United States is that heavy rain-
storms typically occur and provide a
strong, uncontrollable force for driving
disease development. In growing areas
where rainfall is prevalent, growers are
encouraged to choose well-drained sites
and plant into raised beds and/or mowed
cover crops (84,86). However, plants
growing in well-drained fields on raised
beds may become diseased if the rainfall is
heavy (≥2.5 cm), because even a well-
drained field may hold standing water long
enough for zoospores to be released. Driv-
ing rain likely assists in disseminating
sporangia. Strategies to limit splash disper-
sal such as planting into mowed cover
crops and trellising of cucurbits appear
promising as the fruit are kept off the
ground and out of standing water (86).
Unfortunately, trellising may not be an
option for large cucurbit fruit such as
pumpkins. In Michigan, the dependence of
many large-acreage cucumber and winter
squash producers on mechanical harvesters
limits the range of cultural modifications
available.
In many areas of the southwestern
United States, P. capsici has plagued vege-
table growers since being described more
than 80 years ago. Although water-poor
farmers may not see it as such, a major
advantage in these arid areas is low annual
rainfall. Growers can control the amount
and frequency of irrigation and thus can
significantly impact the severity of disease
in fields known to harbor P. capsici
(15,16). For example, in California where
rainfall is low, placing drip emitters away
from the stems of pepper plants can reduce
incidence of Phytophthora crown rot of
peppers (15). Café-Filho et al. (16) showed
that the incidence of root and fruit rot of
squash caused by P. capsici in California
increased with increased frequency of
irrigation. They recorded almost total crop
loss with an irrigation frequency of 7 days,
compared with almost no disease when the
field was furrow irrigated every 21 days. In
the absence of the disease, irrigation inter-
vals of 21 days did not negatively affect
fruit yield compared with more frequent
irrigations (16).
Similar observations were reported for
Phytophthora root and crown rot of bell
peppers in North Carolina, where disease
incidence increased with increased fre-
quency of drip irrigation (82,83). Heavy
rainfall (>2.0 cm) was also directly impli-
cated with increased disease (82). In addi-
tion to splash dispersal, a heavy rainfall
causes mass flow of water on the soil sur-
face and inoculum redistribution in the
field. Reducing field wetness periods may
be a useful tool in managing fruit rot. Most
irrigation systems in Michigan use a trav-
eler that produces relatively large water
droplets, thereby increasing the risk of
contaminating fruit with soil that is
splashed via water (67). Irrigation may be
reduced to a minimum after fruit set and
even completely eliminated prior to crop
harvest with no yield reduction (16) and
may reduce fruit rot not only in the field
but also after harvest.
When a field is infested with P. capsici,
narrow spacing enhances disease spread
and development by increasing relative
humidity in the microclimate and length-
ening the duration of soil surface and fruit
wetness after a rain or irrigation episode
(16). Growers of pickling cucumbers in
Michigan have historically used a narrow
(27.9 cm) row spacing in a production
system that was developed over 15 years
ago by university and industry profession-
als to maximize yield through high plant
densities and suppress weeds through early
canopy closure. Most growers have been
reluctant to alter their current production
system because they anticipate a reduced
yield with increased row spacing. How-
ever, Schultheis and Wehner showed that
the density of cucumber plants could be
reduced without significantly reducing
yield (90). They evaluated densities rang-
ing from about 34,500 to 556,000 plants
per ha and observed more culls with high
plant densities.
Preliminary studies have been conducted
at Michigan State University to integrate
cultural control methods of controlling P.
capsici on zucchini, methods including soil
amendments, protective mulches, and water
management. Raised beds, flat beds, and
raised beds with black plastic + 2.5 cm
straw and/or 4,483.3 kg/ha compost were
compared (Fig. 7B,C). Significant dif-
ferences in P. capsici incidence occurred
each year the trial was conducted (Fig. 7A)
(M. K. Hausbeck and B. Cortright,
unpublished data). Although the treatments
with raised beds in combination with
plastic, straw, and/or compost were sig-
nificantly better than flat beds for stand
count, numbers, and weight of healthy fruit
both years (Fig. 7A), disease still occurred
in these treatments. While cultural strategies
offer reasonably effective protection for
fresh-market zucchini or similar bush-type
cucurbit varieties, these management tools
are too costly and impractical for growers of
cucurbits for the processing industry where
the profit margin is relatively small.
Fungicides. While fungicides cannot be
relied upon alone to prevent disease, they
have provided Michigan growers with an
extra degree of protection, especially when
used in combination with other manage-
ment practices, such as crop rotation,
raised beds, and water management. A
limited number of fungicides are available
for combating P. capsici, especially when
the pathogen is resistant to mefenoxam,
but none have proven wholly efficacious
under optimal conditions for disease
(5,41,93). When resistance of P. capsici to
mefenoxam was discovered in Michigan,
we obtained a Specific Exemption in 1998
for the use of the fungicide Acrobat (di-
methomorph). This product now has a full
label, and its efficacy has been demon-
strated in controlled, replicated large-scale
Plant Disease / December 2004 1299
pickling cucumber field studies (Fig. 8A–
C) (38,39). In 2002, the fungicide Gavel
(zoxamide + mancozeb) was registered for
use against P. capsici and has also proven
to be helpful (Fig. 8A). Studies have indi-
cated that mixing a full rate of copper hy-
droxide with Acrobat 50WP or Gavel
75DF may be helpful, and is recommended
(Fig. 8A) (38,39). Seed treatment with
either Apron XL LS (mefenoxam) or Alle-
giance FL (metalaxyl) may be helpful dur-
ing seed germination to limit pre- and
post-damping off caused by P. capsici (7).
Growers are encouraged to alternate fungi-
cides and avoid relying on a single fungi-
cide to delay development of fungicide
resistance in P. capsici.
Good coverage of the plant and fruit
with fungicide is essential for maximum
protection, but can be difficult to achieve
when fruit are shielded by a dense foliar
canopy. Plant spacing within the field has
been increased by some growers to facili-
tate improved fungicide coverage. Early
and frequent fungicide applications are
required for maximum disease control, but
increase the cost of production. In Michi-
gan, a fungicide spray may be needed
every 5 to 7 days when the weather is wet
and rainy. However, the preharvest interval
required for Gavel (≥4 days) makes it diffi-
cult to use this fungicide in some produc-
tion systems. Also, mancozeb (a compo-
nent of Gavel) is a B2 carcinogen, and may
be impacted by the Food Quality Protec-
tion Act.
Fumigation. The long-term persistence
of the oospore in agricultural soils poses a
continual threat to the successful commer-
cial production of host crops (11,64,89).
Oospores germinate asynchronously, and
detecting P. capsici oospores in the soil
prior to an epidemic is notoriously difficult
and the likelihood of obtaining a false
negative is high (27,64). To reduce the risk
and uncertainty of growing P. capsici–
susceptible crops, producers of solana-
ceous and cucurbit crops for the fresh mar-
ket rely on methyl bromide fumigation as
the primary means of ensuring fruit yield
and quality. Methyl bromide is used in

Fig. 7. A, A replicated demonstration trial with a commercial

grower to highlight cultural tools to manage Phytophthora
capsici, including raised planting beds, black plastic mulch,
composted chicken manure, and straw mulch. B, Zucchini
grown on raised planting beds (right) were healthier than those
raised on flat beds (left). C, Using a combination of cultural Fig. 8. A, Efficacy of fungicides in reducing fruit rot incidence
practices, including a raised planting bed, plastic mulch, and compared with untreated fruit. B, Application of fungicide in a
straw mulch over the plastic (right) kept zucchini healthy large-scale, replicated trial. C, Fungicides were applied when
compared with growing zucchini on a flat bed (left). fruit were approximately 2.5, 7.6, and 12.7 cm in length.

1300 Plant Disease / Vol. 88 No. 12

conjunction with raised beds, black plastic, and Islam, Johnston et al., and Driver and University (Pickle Packers International, Inc.),
and fungicide applications. Because of the Louws evaluated commercial varieties and Pickle Seed Research Fund (Pickle Packers Interna-
tional, Inc.), Project GREEEN (a cooperative effort
short plant-back interval of methyl bro- experimental breeding lines of pepper for by plant-based commodities and businesses with
mide, crops can be transplanted as soon as resistance to P. capsici (6,24,45). ‘Paladin,’ Michigan State University Extension, the Michigan
the soil reaches an appropriate temperature a commercially available pepper cultivar Agricultural Experiment Station, and the Michigan
in the spring, allowing access to early mar- with resistance to Phytophthora crown rot, Department of Agriculture), Michigan Department
keting opportunities. Critical Use Exemp- appeared promising in these studies. In of Agriculture Specialty Crop Block Grant, and
Michigan Agriculture Experiment Station.
tions have been submitted and accepted by Michigan, ‘Paladin’ has been commer-
EPA on behalf of Michigan’s solanaceous cially grown in P. capsici–infested sites, Literature Cited
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Mary K. Hausbeck
Dr. Hausbeck is a professor and plant
pathologist with extension and re-
search responsibilities in the Depart-
ment of Plant Pathology at Michigan
State University. She earned her B.S.
and M.S. degrees in horticulture from
Michigan State University and her
Ph.D. in plant pathology from the
Pennsylvania State University. She
joined the faculty at Michigan State
University in 1990 as a visiting assis-
tant professor and became an assis-
tant professor in 1992. Her research
interests include the epidemiology and
management of diseases of veg-
etables in the field and flower crops
and vegetable transplants in the
greenhouse. Dr. Hausbeck received
the Michigan Master Farmer Associate
Award and is a two-time recipient of
the Michigan Extension Specialist
Award for research and extension
contributions to the vegetable industry.
She also received the Society of
American Florists’ 2004 Alex Laurie
Award for research and education.
Evaluation of fungicides and host resistance
for control of Phytophthora crown rot of sum-
mer squash, 1999. Fungic. Nematicide Tests
55:264.
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Black polyethylene mulch and Phytophthora
blight of pepper. Plant Dis. 66:281.
95. Stevenson, W. R., James, R. V., and Rand, R.
E. 2000. Evaluation of selected fungicides to
control Phytophthora blight and fruit rot of
cucumber. Fungic. Nematicide Tests 55:163.
96. Stevenson, W. R., James, R. V., and Rand, R.
E. 2001. Evaluation of selected fungicides to
control Phytophthora blight and fruit rot of
cucumber. Fungic. Nematicide Tests 56:V16.
Online publication.
97. Tian, D., and Babadoost, M. 2004. Host range
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pathogenicity of isolates. Plant Dis. 88:485-
489.
98. Tibayrenc, M., Kjellberg, F., Arnaud, J., Oury,
B., Breniere, S., Darde, M., and Ayala, F.
Kurt H. Lamour
Dr. Lamour finished his Ph.D. in the
Botany and Plant Pathology Depart-
ment at Michigan State University in
2001. His research focused on the
population biology of Phytophthora
capsici—particularly the impact of
sexual reproduction within naturally
occurring populations. He participated
in the APS I. E. Melhus graduate sym-
posium during the final year of his
doctoral work. Dr. Lamour studied
Phytophthora species as a postdoc-
toral researcher and as a visiting
assistant professor at MSU before
starting as an assistant professor in
the Department of Entomology and
Plant Pathology at the University of
Tennessee in Knoxville in January of
2003. He received a National Science
Foundation CAREER award in 2004 to
develop reverse-genetic technology
for Phytophthora functional genomics,
and his research is focused on under-
standing the molecular machinery
underlying Phytophthora’s unique
biology.
1991. Are eukaryotic microorganisms clonal
or sexual? A population genetics vantage.
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Online publication.
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