phytophthora capsici on vegetable crops: research progress ......and disease symptoms in michigan,...

1292 Plant Disease / Vol. 88 No. 12

Mary K. Hausbeck Michigan State University, East Lansing

Kurt H. Lamour 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-

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),

Corresponding author: M. K. Hausbeck E-mail: [email protected]

Publication no. D-2004-1007-01F © 2004 The American Phytopathological Society

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

melon Tomato

Pumpkin Muskmelon Summer

squash

Watermelon Winter squash Zucchini

Plant Disease / December 2004 1293 1293

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.


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 producelemon-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.


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

Compatibility type/mefenoxam sensitivityb

Location No. of

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.

b Mefenoxam sensitivity determined by in vitro screening on 100 ppm AI amended media, with S(sensitive) = <30% growth of control (GC), IS (intermediately sensitive) = between 30 and 90% GC, and I (insensitive) = >90% GC.

Fig. 3. Typical amphigynous oospores of Phytophthora capsici, A and B, in the gut of a fungal gnat that was feeding on a P. capsici–infected pumpkin; and C, on the fruit of a naturally infected cucumber.


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).

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 inheritance 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-

Fig. 4. Average number of sporangiarecovered from cucumber fruit inocu-lated with Phytophthora capsici and incubated at 60, 80, and 98% relativehumidity (RH) for 5 days. Error bars indi-cate standard error of the means.


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

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

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 isapplied. B, Only the rare intermediately sensitive isolates produce oospores. C, The process of only the resistant isolates mating and producing oospores is continuedwhen mefenoxam is applied in subsequent years.


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-

tophthora spp., including P. capsici (3,11). Growers practicing even lengthy rotations (>5 years) to nonsusceptible hosts have experienced significant crop loss to P. cap-sici. A spatiotemporal study conducted on a Michigan farm used molecular tools to identify P. capsici isolates. The data sug-gest that a P. capsici epidemic on squash in 1999 was initiated by dormant oospores generated 5 years previously, despite rota-tion to corn and soybeans (59). Although a minimum 3- to 4-year rotation to nonsus-ceptible hosts is recommended to limit the buildup of P. capsici (84), the availability of noninfested land is becoming increas-ingly scarce. The development of agricul-ture land for urban use and the relatively low value of some field crops have forced many vegetable producers to reduce their crop rotation to only 1 or 2 years, thus

contributing to the disease problem. Some weeds also may play an important role in the survival of P. capsici from one growing season to another (31,79).

Today, many vegetable producers in the United States recognize that cucurbit and solanaceous crops are at risk for P. capsici infection and rotate these crops with other vegetables (i.e., carrots, beans, onions, and asparagus are examples from Michigan) or agronomic crops (soybeans, alfalfa, small 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 commonly grown vegetables (97) under laboratory conditions highlight the gaps in our knowledge and standard management recommendations and suggest that guide-lines for crop rotation should be re-evalu-ated.

Exclusion. In Michigan, it does not ap-pear that P. capsici is dispersed over long distances, and excluding the pathogen from noninfested growing areas is empha-sized to producers during extension pro-grams and farm visits. Increased attention to the routes by which P. capsici may be introduced is warranted. Movement of other Phytophthora spp. via irrigation water has been documented (27), and aboveground water sources may play a role in the long-distance movement of P. cap-sici. Runoff water from infested fields can transport the pathogen from diseased

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 wereproduced 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.

Table 3. Genetic diversity of Phytophthora capsici isolates recovered from locations in the UnitedStates

Location

Isolates analyzed

Unique isolatesa

AFLP markers resolved

Polymorphic markers (%)

Connecticut 12 10 78 40 (51) Pennsylvania 15 11 90 51 (57) California 20 11 81 42 (52) Ohio 15 12 86 45 (52) New York (upstate) 12 10 86 50 (58) New York (Long Island) 42 37 90 58 (64) North Carolina 57 52 88 49 (56)

a All isolates have unique multilocus amplified fragment length polymorphism (AFLP) profiles.


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


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 commercialgrower to highlight cultural tools to manage Phytophthoracapsici, including raised planting beds, black plastic mulch,composted chicken manure, and straw mulch. B, Zucchinigrown on raised planting beds (right) were healthier than thoseraised on flat beds (left). C, Using a combination of culturalpractices, including a raised planting bed, plastic mulch, andstraw mulch over the plastic (right) kept zucchini healthycompared with growing zucchini on a flat bed (left).

Fig. 8. A, Efficacy of fungicides in reducing fruit rot incidence compared with untreated fruit. B, Application of fungicide in a large-scale, replicated trial. C, Fungicides were applied when fruit were approximately 2.5, 7.6, and 12.7 cm in length.


conjunction with raised beds, black plastic, and fungicide applications. Because of the short plant-back interval of methyl bro-mide, crops can be transplanted as soon as the soil reaches an appropriate temperature in the spring, allowing access to early mar-keting opportunities. Critical Use Exemp-tions have been submitted and accepted by EPA on behalf of Michigan’s solanaceous and cucurbit producers for the extended use of methyl bromide on these crops. Given the scheduled phaseout of methyl bromide in the very near future, it is im-perative that effective and cost efficient replacements be identified and imple-mented.

Both registered and experimental fumi-gants have been tested in Michigan in con-junction with commercial producers at known P. capsici–infested sites. A study conducted by the authors in 2003 at a site infested with P. capsici showed that metam sodium (Vapam), 66% methyl bromide, 33% chloropicrin (methyl bromide/chlor-opicrin), and 61% 1,3-dichloropropene, 35% chloropicrin (Telone C-35) all effec-tively limited disease when used in a raised bed, plastic mulch system.

Genetic resistance. Genetic resistance or tolerance is often at the core of inte-grated management programs and would be especially helpful in managing P. cap-sici. Screening cucurbit germ plasm for resistance to P. capsici has been an ongo-ing effort at Michigan State University. To date, the fruit of over 300 cucumber varie-ties have been screened for resistance to this pathogen, including pickling varieties, slicing cucumber varieties, and plant intro-duction accessions. Although complete fruit disease resistance has not been ob-served, varieties that appear to have lim-ited lesion development and sporulation have been identified (A. Gevens and M. K. Hausbeck, unpublished data). Babadoost

and Islam, Johnston et al., and Driver and Louws evaluated commercial varieties and experimental breeding lines of pepper for resistance to P. capsici (6,24,45). ‘Paladin,’ a commercially available pepper cultivar with resistance to Phytophthora crown rot, appeared promising in these studies. In Michigan, ‘Paladin’ has been commer-cially grown in P. capsici–infested sites, although the plants have been observed to eventually succumb to disease when envi-ronmental conditions are favorable. Since neither genetic resistance nor fungicide management appears to be perfect, com-bining the two may provide significant control advances.

Information dissemination. While pre-venting the introduction of the pathogen is optimal, once P. capsici is introduced, several control measures need to be used in a comprehensive management program to reduce losses from disease (Sidebar). As techniques and tools are developed to ease the severity of crop loss due to P. capsici, on-farm research trials and educational workshops are emphasized to enhance grower implementation. Further, education of other crop specialists, extension person-nel, and consultants is ongoing to ensure that growers receive accurate and consis-tent information and recommendations.

Acknowledgments Special thanks to M. McGrath (Cornell Univer-

sity, Riverhead, NY), G. Holmes (North Carolina State University, Raleigh), M. Davis (University of California, Davis), and W. Elmer (Connecticut Agric. Exp. Station, New Haven) for their assis-tance in collecting P. capsici isolates. Research regarding fungicide and fumigation evaluation was designed and conducted with the assistance of B. Cortright (Michigan State University). We thank S. Linderman (Michigan State University) for valu-able assistance in manuscript formatting and prepa-ration of the figures and tables. Portions of the research discussed have been funded by the Pickle and Pepper Research Committee of Michigan State

University (Pickle Packers International, Inc.), Pickle Seed Research Fund (Pickle Packers Interna-tional, Inc.), Project GREEEN (a cooperative effort by plant-based commodities and businesses with Michigan State University Extension, the Michigan Agricultural Experiment Station, and the Michigan Department of Agriculture), Michigan Department of Agriculture Specialty Crop Block Grant, and Michigan Agriculture Experiment Station.

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Recommended Control Strategies for Blight Caused by Phytophthora capsici

Preplant • Use a seed treatment that is effective against oomycetes. • Consider a preplant banded fungicide application for infested fields. • Plant susceptible hosts in well-drained fields. • Utilize raised beds (15 to 20 cm minimum) whenever possible. • Do not plant in low-lying areas of the field.

Production • Monitor fields for disease, including damping-off, plant stunting, root and crown rot. • Do not irrigate a field with water that contains runoff from fields with a history of

Phytophthora disease. • Irrigate conservatively, and if possible, do not irrigate close to harvest time. • Plow under portions of the field with diseased plants, including healthy plants that border

diseased areas. • Remove diseased fruit from the field. • Never dump culls or diseased fruit from other fields or farms into production fields. Once

P. capsici is introduced, it may remain indefinitely. • Apply fungicide preventively and frequently, especially for known problem fields. • Rotate the types of fungicides used.

Postharvest • Harvest fruit as soon as possible from problem fields and plow under crop residue

immediately. • Keep harvested fruit dry and cool.


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Mary K. Hausbeck Dr. Hausbeck is a professor and plantpathologist 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 fromMichigan State University and herPh.D. in plant pathology from thePennsylvania State University. Shejoined the faculty at Michigan StateUniversity in 1990 as a visiting assis-tant professor and became an assis-tant professor in 1992. Her researchinterests include the epidemiology andmanagement of diseases of veg-etables in the field and flower cropsand vegetable transplants in thegreenhouse. Dr. Hausbeck received the Michigan Master Farmer AssociateAward and is a two-time recipient of the Michigan Extension SpecialistAward for research and extensioncontributions to the vegetable industry. She also received the Society ofAmerican Florists’ 2004 Alex Laurie Award for research and education.

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.

phytophthora capsici on vegetable crops: research progress ......and disease symptoms in michigan,...

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