Phytophthora Capsici on Vegetable Crops: Research Progress and Management Challenges

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

1292 Plant Disease / Vol. 88 No. 12 wet conditions, root and crown infection of soil onto the cotyledons of emerging cu- located along the surface water drainage pepper, zucchini, squash, and pumpkin cumbers, the entire 24.3-ha planting was pattern. P. c a psi c i was recovered from typically causes permanent wilt and plant killed. Similarly, extremely rainy weather crown, stem, and leaf tissue (35). death (Fig. 1D–F,L). Plants often have that saturates soil for extended periods can While plant death is always a concern brown to black discolored roots and/or prompt a severe root and crown rot that for vegetable producers, fruit rot seems to crowns. In contrast, infected cucumber and kills even established tomato plants. Dis- be especially insidious on cucurbits. In tomato plants may be relatively asympto- ease symptoms on snap beans include general, infected cucurbit fruit initially matic or exhibit limited root rot and plant water-soaking on the leaves, stem necrosis exhibit dark, water-soaked lesions (Fig. stunting (Fig. 1A,B,M,N). However, when (Fig. 1O), and overall decline. Disease 1C,I), followed by a distinctive white a rainstorm splashed P. capsici–infested symptoms were most severe on bean plants “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, zucchini; 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. The Pathogen composed of coenocytic mycelium which 1A,G,H). While P. capsici regularly causes may give rise to lemon-shaped sporangia a blight of pepper fruit in other growing Early investigators recognized that the borne on long caducous pedicels (1). When regions (84), this is not a common occur- genus Phytophthora exhibited striking sporangia are immersed in free water, they rence in Michigan and has been observed dissimilarities to many other fungal organ- differentiate to produce 20 to 40 bi-motile only occasionally in the last several years isms, but a full resolution of its taxonomic swimming zoospores (Fig. 2) (8). Long- (Fig. 1J,K). Cucumber plants appear to and evolutionary standing would not be term survival outside of host tissue is ac- tolerate root infection by P. capsici, yet the made until DNA sequence analysis was complished by the oospore (2,3,10,42,58– fruit are especially susceptible. In Michi- completed by Forster et al. in 1990. They 60), which has a thick, multilayered wall gan, fields of healthy-appearing cucumber found that oomycetes are more closely containing β-glucan and cellulose (27). vines with mature fruit have been aban- related to heterokont photosynthetic algae Oospores require a dormancy period of at doned in the field at harvest, or semi-truck than to members of the kingdom Fungi least a month (27,88) before germinating loads of fruit rejected at the processing (29). The modern description of P. capsici directly or by forming sporangia (Fig. 2). facility, due to rot. In our studies, we rou- as a species falls into Waterhouse’s Group tinely observe a delay of at least 48 hours in II (101) and is characterized by sporangia Sexual Reproduction that are conspicuously papillate with am- symptom expression in cucumber following and Oospores successful penetration by P. c a p s i c i (K. H. phigynous oospores generally forming Lamour and M. K. Hausbeck, unpublished only when A1 and A2 mating types are Approximately half of the 60 recognized results). A similar 3- to 6-day lag prior to paired. Information concerning the differ- species in the genus Phytophthora are symptom expression for P. c a p si c i infecting ent spore types produced by members of homothallic (self-fertile), and for these peppers has been described previously by the genus Phytophthora accumulated species, a single isolate is able to complete Schlub (89). This delay explains why slowly between 1940 and 1970. In 1970, the sexual stage and form oospores (27). producers in Michigan who harvest Waterhouse (101) provided a useful, and The remaining species, including P. cap- seemingly healthy fruit have had entire still used, key for identifying isolates to sici, are heterothallic and require two com- loads rejected; fruit become infected while species based on the morphology of spo- patibility types (=mating types), desig- in the field but the disease progresses during rangia and oospores and whether or not an nated A1 and A2, to complete the sexual storage and transit, with symptoms and/or isolate could produce oospores in single stage (27). Oospores are formed when A1 signs becoming evident after delivery to culture. Research with other Phytophthora and A2 compatibility types come into close the processor or retailer. The increased species established much of what is known association (Fig. 2) (50). Each of the par- temperatures during harvest, storage, and about the three dominant spore types pro- ent isolates makes both male (antheridium) transit may be an important factor. duced by P. capsici (27). The thallus is 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 drainage 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 from 100% at the beginning of the epi- and germination of P. capsici oospores self-fertilization is possible in obligate demic to less than 30% by the end of the (88). They reported that relatively young outcrossing species (50). growing season (59). oospores produced in paired cultures of P. To our knowledge, P. capsici is the only Papavizas et al. (76) provided the first capsici germinated to produce recombinant heterothallic Phytophthora species that has report of naturally occurring P. capsici progeny after 30 days incubation. Prior to been shown to regularly complete the sex- oospores in diseased host tissue in North this, it was generally thought that 6- to 9- ual stage (outcross) in the United States America. In Michigan, amphigynous oo- month incubation periods were necessary (37,56,58–62). The A1 and A2 mating spores typical of P. capsici have been for oospore germination. The progeny types both occur within natural field popu- found in infected pumpkin, cucumber (Fig. from their crosses were shown to differ lations of P. capsici. The presence of A1 3C), and butternut squash fruit and in the from the parental types in both morphol- and A2 isolates of P. capsici in single stems of P. capsici–infected yellow squash ogy and pathogenicity. For example, one fields was reported in New Jersey in 1981 seedlings. Interestingly, fungal gnat larvae progeny isolate exhibited increased viru- (76) and in North Carolina in 1990 (81). (Sciaridae) feeding on pumpkin fruit in- lence on pepper compared with either of Both mating types have been recovered fected with P. capsici had numerous oo- the parents, which suggests that sexual from farms surveyed in other states when spores in the digestive tracts of three speci- reproduction could lead to increased viru- at least 15 isolates were collected from mens (Fig. 3A,B). No attempt to determine lence in the field. A number of important diverse locations within a field (Table 2). the viability of the excreted oospores was milestones were reached in this investiga- During 1997 and 1998, 14 Michigan farms made, but a study conducted with oospores tion. A simple method for the production, were sampled, with 473 isolates recovered of Pythium spp. and fungal gnat larvae germination, and harvesting of oospore from cucurbit hosts and 30 from bell pep- indicates that oospores remain viable and progeny for P. capsici was formally pre- per (58). The A1 and A2 compatibility suggests that the gnat’s larval stage may sented, and the authors convincingly ar- types were recovered in roughly a 1:1 ratio serve as a vector (33). gued that proper media containing ample for eight farms. In 2001, we collected iso- Although oospores have been consid- nutrients as well as genetically compatible lates of P. capsici from fields in New York, ered the primary source of inoculum in the parent isolates are required for successful Connecticut, Pennsylvania, Ohio, North field, little is known about the influence of crosses. In addition, this work provided Carolina, and California; similar trends soil physical factors on infection of host convincing evidence for the potential role were revealed. When 429 isolates from crops in oospore-infested soils. In vitro of oospores in generating genetic variation these states were screened for mating type, treatment with chemicals and physical (88). In 1971, Polach and Webster (80) 53% (227) were A1 and 47% (202) were factors that may interact with oospores in corroborated this finding using the oospore A2 mating types. Both mating types were the soil can provide information on germi- incubation and germination techniques of recovered from every location, and the nation and viability (44,48). Although Satour and Butler (88). Polach and Web- A1/A2 ratio was close to 1:1 within loca- information about oospore germination in ster (80) investigated 391 single oospore tions (Table 2). situ is limited and reportedly difficult to To determine if both mating types are observe and definitively assay (44,64), it is present in a field, the timing and spatial important to monitor oospore germination scale of sampling are important. Multiple in a simulated, complex soil setting (76). cycles of infection and spore production Oospore survival has been successfully allow P. capsici to spread rapidly through- studied in situ with P. infestans (23). Thus, out fields during warm, wet weather, and an important precedent for research on P. samples collected from a few plants at the capsici is in place. height of an epidemic may erroneously The main impediment to detailed studies suggest that only a single mating type is of oospores and the inherent genetics present (76,82). Samples collected every 2 therein was primarily the difficulty in sepa- weeks over a 3-month period from a single rating and germinating oospores (65,92). field of squash in Michigan illustrated how In 1968, Satour and Butler provided cru- the percentage of unique genotypes fell cial information concerning the generation

Table 2. Phenotypic diversity of Phytophthora capsici isolates recovered from cucurbit and solanaceous hosts at diverse locations in the United States during 2001 b No. of Compatibility type/mefenoxam sensitivity 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 In general, sporangia and zoospores are into RNA in sensitive oomycetes (20). The reported that the parent isolates differed in thought to be relatively ephemeral struc- mode of action of metalaxyl is postulated their pathogenicity to cucurbit and solana- tures contributing to the spread of P. cap- to be site specific, and it was not surprising ceous hosts and that segregation and re- sici within a single growing season but when resistance surfaced in populations of combination were observed for all the unlikely to survive the harsh conditions susceptible plant pathogens after PAFs characters studied. typical of nonhost periods in North Amer- were introduced during the late 1970s (20). ica (2,3,11,58,59,61,62). Results from As early as 1981, researchers working with Role of Sporangia and investigations with P. capsici in Michigan P. capsici demonstrated that insensitivity Zoospores in Field Epidemics suggest that overwintering of clonal inocu- to metalaxyl was readily selected for by Like many species in the genus Phy- lum is rare but that reproduction of clonal using sublethally amended media (12,13). tophthora, P. capsici has the potential for populations within a single season is sig- Insensitivity soon developed in natural rapid polycyclic disease development from nificant (58). Tracking a single population populations of oomycetous organisms a limited amount of inoculum (82). The of P. capsici over the course of the grow- where metalaxyl was heavily relied upon asexual sporangia and zoospores proved to ing season in 1999 using molecular mark- (18,34,46). Adaptation to PAFs is common be much easier to manipulate and study ers indicated that asexual spread increased throughout the oomycetes (19,34) and is than the oospore, and it is not surprising dramatically as the season progressed and generally accepted as inevitable due to that the salient features of these spore that a single clone accounted for approxi- the specificity of this group of fungicides types were outlined relatively early mately 50% of the isolates recovered in the (20). Studies characterizing the inher- (40,73). P. c a p si c i grows optimally be- final one-third of the growing season (59). itance of mefenoxam insensitivity in P. tween 25 and 28°C and can produce copi- Thus, the infection and subsequent sporu- capsici suggest that insensitivity is ous amounts of deciduous sporangia on the lation on host tissue and fruit likely play a conferred by a single incompletely surface of infected tissue (1,17,99,102). key role in driving the polycyclic phase of dominant locus (58). When cucumber fruit were inoculated and disease development in the field. The num- Recovering insensitive P. capsici iso- incubated at 60, 80, and 98% relative hu- ber of sporangia on a single naturally in- lates from farms with a history of PAF use midity (RH) for 5 days, more sporangia fected spaghetti squash fruit was estimated is increasingly common in the United were produced at 60 and 80% RH than at to be 44 million with the potential to re- States. Data from North Carolina, Michi- >90% RH (Fig. 4) (K. H. Lamour and M. lease 840 million zoospores (K. H. Lamour gan, and New Jersey indicate that a signifi- K. Hausbeck, unpublished results). Mature and M. K. Hausbeck, unpublished results). cant proportion of P. capsici populations sporangia are easily dislodged by rain and In addition to the epidemiological ad- under PAF selection pressure may be inter- irrigation and can directly germinate or, vantage provided by a large aboveground mediately or fully insensitive to mefen- when immersed in water, release 20 to 40 reservoir of inoculum, there may be an oxam (28,58,77,78). Insensitivity to motile zoospores (40) that travel with wa- additional evolutionary advantage con- mefenoxam, which also conferred insens- ter in fields (89). Zoospores exhibit nega- ferred by the large number of hyaline spo- itivity to metalaxyl, was reported from tive geotropism and chemotactically follow rangia exposed to UV irradiation on the field populations of P. capsici on bell pep- nutrient gradients while swimming (27). surface of infected fruit. Fungicide insensi- per (77). The inheritance of mefenoxam Once zoospores contact the plant surface, tivity was easily induced in P. capsici us- sensitivity was assessed in naturally occur- they encyst and germinate to produce germ ing UV irradiation (14), and it seems rea- ring populations of P. capsici in Michigan. tubes (40). Scanning electron microscopy sonable that the thousands of sporangia In Michigan, greater than half (55%) of the illustrates that zoospores are able to di- present on an infected cucurbit fruit repre- 498 isolates sampled were sensitive, 32% rectly penetrate the intact cuticle within an sent a significant substrate for the effects were intermediate, and 13% were fully hour (K. H. Lamour and M. K. Hausbeck, of UV-mediated mutation. Dekker (22) insensitive to mefenoxam (58). Three unpublished data). Penetration of leaf states that the buildup of a chemical-resis- farms, two in North Carolina and one in surfaces by P. capsici occurs directly and tant pathogen population will occur faster New York, had a history of mefenoxam through natural openings such as stomata in a heavily sporulating pathogen on aerial use, and insensitive isolates were recov- (47). P. capsici produces an extra-cellular plant parts than in a slowly spreading, ered from each (Table 2). Overall, 70% macerating enzyme that likely plays a soilborne pathogen, and cites as an exam- (301) of the isolates were fully sensitive, significant role in breaching the host epi- ple that the buildup of metalaxyl resistance 17% (75) were intermediately sensitive, dermis and ramifying through susceptible in the aerially sporulating P. infestans was and 13% (53) were insensitive to me- host tissue (104). much faster than occurred with P. cinna- fenoxam. The majority (40) of the fully momi causing avocado root disease. insensitive isolates were recovered from a single bell pepper field in North Carolina Sexual Reproduction with a history of mefenoxam use. In North and Adaptation to PAFs Carolina, the process of adaptation to me- Historically, growers have relied on a fenoxam appears to have occurred rapidly limited number of fungicides for control of (78). Phytophthora root, crown, and fruit rot. Because only sensitive isolates of P. The phenylamide class of fungicides capsici are controlled by the mefenoxam (PAF), specifically metalaxyl and the new- fungicide (63), the observed control failure est fungicide mefenoxam (Ridomil Gold in some Michigan fields during the last EC), has been used by many growers to few years is likely due to the development combat P. capsici. Mefenoxam is the active and increasing incidence of P. capsici iso- enantiomer contained in the racemic fungi- lates insensitive to this fungicide. Sexual cide metalaxyl (77,78). Both compounds recombination appears to play an impor- are strongly fungicidal to sensitive isolates tant role in adaptation by generating fully (20,75), and isolates recovered from farms insensitive isolates (e.g., mating between Fig. 4. Average number of sporangia without a history of PAF use are highly intermediately sensitive isolates) (Fig. 5). recovered from cucumber fruit inoculated with Phytophthora capsici and sensitive to both mefenoxam and A Michigan population of P. capsici com- incubated at 60, 80, and 98% relative metalaxyl (58,78). prised of intermediate and fully insensitive humidity (RH) for 5 days. Error bars indi- Metalaxyl has been shown to specifi- isolates tracked for 3 years (1999 to 2001) cate standard error of the means. cally inhibit the incorporation of uridine in the absence of PAF use showed no evi-

1296 Plant Disease / Vol. 88 No. 12 dence of reversion back to the wild-type, from an isozyme study involving 113 P. ages. This is an important consideration to PAF-sensitive, state (62). capsici isolates were interpreted as reveal- accurately determine how far P. capsici is Effective fungicides that act on a single ing two subgroups within the P. capsici dispersed and if clonal lineages are able to enzyme or molecular pathway exert sig- species (71). Subgroups are defined as survive outside of hosts. The amplified nificant selection pressure favoring isolates being significantly different based on spo- fragment length polymorphism (AFLP) able to withstand the activity of the fungi- rangial morphology and ontogeny. RFLP technique is useful for this type of differ- cide. In the case of mefenoxam, there ap- investigation of mitochondrial DNA re- entiation because it allows numerous pears to be a low level of isolates harbor- vealed no patterns of similarity based on markers to be resolved simultaneously and ing a mutation responsible for insensitivity host or geographical location (30). RFLP provides a robust sample across individual to mefenoxam. Application of mefenoxam analysis of nuclear DNA using low copy genomes. The AFLP technique results in favors these isolates, and sexual reproduc- number probes of 15 P. capsici isolates the selective amplification of restriction tion results in numerous genetically unique indicated nuclear DNA diversity was high fragments from a digest of total genomic progeny carrying what was previously a (30). These early studies highlighted the DNA using the polymerase chain reaction rare trait. Because of sexual reproduction, diversity of P. capsici on a worldwide (PCR). The DNA fragments, called AFLP the process of incorporating a novel advan- scale. In the United States, this genetic markers, are resolved using a polyacryla- tageous trait into numerous genetic back- diversity has been exploited to better un- mide gel or, if the PCR primers are labeled grounds makes it less likely that insensitive derstand how natural populations of P. with a fluorescent dye, a DNA sequencing isolates will be less fit than their fungicide- capsici are distributed in space and time. machine. An example of AFLP analysis by sensitive wild-type counterparts. It is rea- Almost 15 years ago, J. B. Ristaino (81) automated DNA sequencing is shown in sonable to suspect that sexual recombina- showed that morphological characters Figure 6. The advantages to this technique tion may play a similar role in the adapta- varied widely in natural populations and are its reproducibility and sensitivity (e.g., tion of P. capsici to other fungicidal that variation in pathogenicity among so- between 50 and 70 AFLP markers are re- compounds whether they are applied man- lanaceous and cucurbit hosts existed in solved per reaction per P. capsici isolate) ually or generated by resistant varieties of field populations. This work corroborated (9). Characterization of 107 oospore prog- plants. earlier laboratory studies showing that eny from a laboratory cross between par- pathogenicity and virulence to tomato and ents with differing AFLP genotypes in- Genetic Diversity pepper segregate during sexual recombina- dicated that the progeny were all Significant molecular investigations into tion and that sex can generate strains more recombinant and that the AFLP markers the genetics of P. capsici do not appear in virulent than either parent (88). Mating segregated as Mendelian characters (59). the literature until the late 1980s and early type and sensitivity to mefenoxam provide A key expectation when studying out- 1990s, when isozyme and restriction frag- a limited level of resolution, and choosing crossing populations is the recovery of ment length polymorphism (RFLP) analy- among the many techniques available for unique combinations of phenotypic and sis of both mitochondrial and nuclear DNA measuring variation at the DNA level can molecular characters. If outcrossing is were conducted on isolates from widely be difficult due to the advantages and limi- occurring in natural populations of P. cap- different geographical locations, years, and tations inherent in each. Because P. capsici sici, then multiple combinations of mating hosts located in a worldwide Phytophthora has the potential for significant polycyclic type, mefenoxam sensitivity, and AFLP culture collection at the University of Cali- reproduction, one of our primary goals was markers should be present (Tables 2 and 3) fornia at Riverside (30,71,74). Results to differentiate uniparental (clonal) line- (98). In Michigan, 70% (454) of the 646 isolates analyzed had unique AFLP profiles. In total, 94 AFLP markers were resolved but no single population had all 94 markers. Individual populations had between 68 and 80 AFLP markers, and isolates were clearly more similar based on geographic locations (60). The high number of unique AFLP profiles and high proportion 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 important 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 Fig. 5. An illustration of how selection for mefenoxam resistance occurs in the field. A, and Challenges Sensitive Phytophthora capsici individuals are unable to infect when mefenoxam is applied. B, Only the rare intermediately sensitive isolates produce oospores. C, The As P. capsici has spread to more acreage process of only the resistant isolates mating and producing oospores is continued devoted to vegetables, producing vulner- when mefenoxam is applied in subsequent years. 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) profiles 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 weeds also may play an important role in States the survival of P. capsici from one growing Isolates Unique AFLP markers Polymorphic season to another (31,79). Location analyzed isolatesa resolved markers (%) Today, many vegetable producers in the Connecticut 12 10 78 40 (51) United States recognize that cucurbit and Pennsylvania 15 11 90 51 (57) solanaceous crops are at risk for P. capsici California 20 11 81 42 (52) infection and rotate these crops with other Ohio 15 12 86 45 (52) vegetables (i.e., carrots, beans, onions, and New York (upstate) 12 10 86 50 (58) asparagus are examples from Michigan) or New York (Long Island) 42 37 90 58 (64) agronomic crops (soybeans, alfalfa, small North Carolina 57 52 88 49 (56) grains). However, recent reports of com- a All isolates have unique multilocus amplified fragment length polymorphism (AFLP) profiles. mercial losses in lima beans (21) and snap beans (35,36) from this pathogen and susceptibility of soybeans (35,36) and other for some producers, an overwhelming tophthora spp., including P. capsici (3,11). commonly grown vegetables (97) under challenge. The future of the vegetable in- Growers practicing even lengthy rotations laboratory conditions highlight the gaps in dustry in Michigan and other regions of (>5 years) to nonsusceptible hosts have our knowledge and standard management the United States plagued by P. capsici is experienced significant crop loss to P. cap- recommendations and suggest that guide- at risk without long-term sustainable ap- sici. A spatiotemporal study conducted on lines for crop rotation should be re-evalu- proaches such as genetic resistance and a Michigan farm used molecular tools to ated. remediation of infested sites. In the short identify P. capsici isolates. The data sug- Exclusion. In Michigan, it does not ap- term, the economic risk of growing P. cap- gest that a P. c a psi c i epidemic on squash in pear that P. capsici is dispersed over long sici–susceptible crops may be reduced by 1999 was initiated by dormant oospores distances, and excluding the pathogen using several management tools. Ristaino generated 5 years previously, despite rota- from noninfested growing areas is empha- and Johnston (84) previously provided a tion to corn and soybeans (59). Although a sized to producers during extension pro- summary of management of this disease in minimum 3- to 4-year rotation to nonsus- grams and farm visits. Increased attention bell pepper. ceptible hosts is recommended to limit the to the routes by which P. capsici may be Crop rotation. While crop rotation is an buildup of P. capsici (84), the availability introduced is warranted. Movement of important foundation of disease manage- of noninfested land is becoming increas- other Phytophthora spp. via irrigation ment, the long-term survival of oospores in ingly scarce. The development of agricul- water has been documented (27), and absence of a host limits the effectiveness ture land for urban use and the relatively aboveground water sources may play a role of this strategy as a stand-alone tool. The low value of some field crops have forced in the long-distance movement of P. cap- survivability of oospores has been clearly many vegetable producers to reduce their sici. Runoff water from infested fields can demonstrated with a number of Phy- 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 strong, uncontrollable force for driving may reduce fruit rot not only in the field irrigation. We began testing aboveground disease development. In growing areas but also after harvest. water sources in Michigan for contamina- where rainfall is prevalent, growers are When a field is infested with P. capsici, tion with P. capsici during 2001 and recov- encouraged to choose well-drained sites narrow spacing enhances disease spread ered the pathogen from irrigation ponds on and plant into raised beds and/or mowed and development by increasing relative two farms (K. H. Lamour and M. K. Haus- cover crops (84,86). However, plants humidity in the microclimate and length- beck, unpublished data). Additional irriga- growing in well-drained fields on raised ening the duration of soil surface and fruit tion water sources were monitored for P. beds may become diseased if the rainfall is wetness after a rain or irrigation episode capsici in 2002 and 2003, and the patho- heavy (≥2.5 cm), because even a well- (16). Growers of pickling cucumbers in gen was frequently detected in a river, drained field may hold standing water long Michigan have historically used a narrow creek, and a naturally fed pond (35,36). All enough for zoospores to be released. Driv- (27.9 cm) row spacing in a production of these water sources were located near ing rain likely assists in disseminating system that was developed over 15 years crops infected with P. capsici. Prior to this sporangia. Strategies to limit splash disper- ago by university and industry profession- research, the presence of P. capsici in sal such as planting into mowed cover als to maximize yield through high plant Michigan irrigation sources had not been crops and trellising of cucurbits appear densities and suppress weeds through early reported. Another potential source of P. promising as the fruit are kept off the canopy closure. Most growers have been capsici–contaminated water may be from ground and out of standing water (86). reluctant to alter their current production vegetable processing facilities that apply Unfortunately, trellising may not be an system because they anticipate a reduced their waste water to nearby vegetable pro- option for large cucurbit fruit such as yield with increased row spacing. How- duction sites. Using water that may be pumpkins. In Michigan, the dependence of ever, Schultheis and Wehner showed that contaminated with P. capsici to irrigate many large-acreage cucumber and winter the density of cucumber plants could be healthy crops must be avoided to limit squash producers on mechanical harvesters reduced without significantly reducing pathogen spread. limits the range of cultural modifications yield (90). They evaluated densities rang- Identifying factors contributing to the available. ing from about 34,500 to 556,000 plants spread of P. capsici to new locations can In many areas of the southwestern per ha and observed more culls with high be challenging. Producers are warned United States, P. capsici has plagued vege- plant densities. against dumping P. capsici–infected pro- table growers since being described more Preliminary studies have been conducted duce on or near their farms. However, a than 80 years ago. Although water-poor at Michigan State University to integrate survey of cultural practices in Michigan farmers may not see it as such, a major cultural control methods of controlling P. indicated that in some cases producers advantage in these arid areas is low annual capsici on zucchini, methods including soil were spreading over- and under-size cull rainfall. Growers can control the amount amendments, protective mulches, and water and diseased fruit onto fields after return- and frequency of irrigation and thus can management. Raised beds, flat beds, and ing from processing stations. Historically, significantly impact the severity of disease raised beds with black plastic + 2.5 cm some processors mandated that producers in fields known to harbor P. capsici straw and/or 4,483.3 kg/ha compost were haul culls and diseased fruit from the proc- (15,16). For example, in California where compared (Fig. 7B,C). Significant dif- essing station for disposal in their fields rainfall is low, placing drip emitters away ferences in P. capsici incidence occurred even if the fruit were from other farms. A from the stems of pepper plants can reduce each year the trial was conducted (Fig. 7A) single fruit infected with both A1 and A2 incidence of Phytophthora crown rot of (M. K. Hausbeck and B. Cortright, mating types may contain thousands of peppers (15). Café-Filho et al. (16) showed unpublished data). Although the treatments genetically unique oospores that can estab- that the incidence of root and fruit rot of with raised beds in combination with lish a resident population of P. capsici in a squash caused by P. capsici in California plastic, straw, and/or compost were sig- field with no history of P. c a psi c i prob- increased with increased frequency of nificantly better than flat beds for stand lems. Once P. capsici is established in a irrigation. They recorded almost total crop count, numbers, and weight of healthy fruit field, tillage and cultivation distribute dis- loss with an irrigation frequency of 7 days, both years (Fig. 7A), disease still occurred eased plant material and spread oospores compared with almost no disease when the in these treatments. While cultural strategies throughout the field and soil profile. It is field was furrow irrigated every 21 days. In offer reasonably effective protection for possible that P. capsici may be dissemi- the absence of the disease, irrigation inter- fresh-market zucchini or similar bush-type nated to new fields via equipment even vals of 21 days did not negatively affect cucurbit varieties, these management tools when no remnants of diseased plant mate- fruit yield compared with more frequent are too costly and impractical for growers of rial are visible. irrigations (16). cucurbits for the processing industry where Cultural control. Commonly recom- Similar observations were reported for the profit margin is relatively small. mended cultural control strategies reflect Phytophthora root and crown rot of bell Fungicides. While fungicides cannot be our understanding of the importance of peppers in North Carolina, where disease relied upon alone to prevent disease, they water in the epidemiology of P. capsici and incidence increased with increased fre- have provided Michigan growers with an include planting into well-drained fields quency of drip irrigation (82,83). Heavy extra degree of protection, especially when and into raised beds whenever possible rainfall (>2.0 cm) was also directly impli- used in combination with other manage- (84). Excess moisture is the single most cated with increased disease (82). In addi- ment practices, such as crop rotation, important component to the initial infection to splash dispersal, a heavy rainfall raised beds, and water management. A tion and subsequent spread of P. capsici causes mass flow of water on the soil sur- limited number of fungicides are available (10,11,82,83,85,89,94). Similar findings face and inoculum redistribution in the for combating P. capsici, especially when exist for many species in the genus Phy- field. Reducing field wetness periods may the pathogen is resistant to mefenoxam, tophthora and are not surprising in light of be a useful tool in managing fruit rot. Most but none have proven wholly efficacious these organisms’ evolutionary ties to the irrigation systems in Michigan use a trav- under optimal conditions for disease algae (25,26). eler that produces relatively large water (5,41,93). When resistance of P. capsici to Since water plays a key role in disease droplets, thereby increasing the risk of mefenoxam was discovered in Michigan, development (82,89), water is managed contaminating fruit with soil that is we obtained a Specific Exemption in 1998 based on the crop and the water dynamics splashed via water (67). Irrigation may be for the use of the fungicide Acrobat (di- of the region. A significant problem in the reduced to a minimum after fruit set and methomorph). This product now has a full eastern United States is that heavy rain- even completely eliminated prior to crop label, and its efficacy has been demon- storms typically occur and provide a harvest with no yield reduction (16) and strated in controlled, replicated large-scale

Plant Disease / December 2004 1299 pickling cucumber field studies (Fig. 8A– Good coverage of the plant and fruit be impacted by the Food Quality Protec- C) (38,39). In 2002, the fungicide Gavel with fungicide is essential for maximum tion Act. (zoxamide + mancozeb) was registered for protection, but can be difficult to achieve Fumigation. The long-term persistence use against P. capsici and has also proven when fruit are shielded by a dense foliar of the oospore in agricultural soils poses a to be helpful (Fig. 8A). Studies have indi- canopy. Plant spacing within the field has continual threat to the successful commer- cated that mixing a full rate of copper hy- been increased by some growers to facili- cial production of host crops (11,64,89). droxide with Acrobat 50WP or Gavel tate improved fungicide coverage. Early Oospores germinate asynchronously, and 75DF may be helpful, and is recommended and frequent fungicide applications are detecting P. capsici oospores in the soil (Fig. 8A) (38,39). Seed treatment with required for maximum disease control, but prior to an epidemic is notoriously difficult either Apron XL LS (mefenoxam) or Alle- increase the cost of production. In Michi- and the likelihood of obtaining a false giance FL (metalaxyl) may be helpful dur- gan, a fungicide spray may be needed negative is high (27,64). To reduce the risk ing seed germination to limit pre- and every 5 to 7 days when the weather is wet and uncertainty of growing P. capsici– post-damping off caused by P. capsici (7). and rainy. However, the preharvest interval susceptible crops, producers of solana- Growers are encouraged to alternate fungi- required for Gavel (≥4 days) makes it diffi- ceous and cucurbit crops for the fresh mar- cides and avoid relying on a single fungi- cult to use this fungicide in some produc- ket rely on methyl bromide fumigation as cide to delay development of fungicide tion systems. Also, mancozeb (a compo- the primary means of ensuring fruit yield resistance in P. capsici. nent of Gavel) is a B2 carcinogen, and may 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 tions have been submitted and accepted by Michigan, ‘Paladin’ has been commer- Michigan Agriculture Experiment Station. EPA on behalf of Michigan’s solanaceous cially grown in P. capsici–infested sites, Literature Cited and cucurbit producers for the extended although the plants have been observed to 1. Alconero, R., and Santiago, A. 1972. Charac- use of methyl bromide on these crops. eventually succumb to disease when envi- teristics of asexual sporulation in Phytoph- Given the scheduled phaseout of methyl ronmental conditions are favorable. Since thora palmivora and Phytophthora parasitica bromide in the very near future, it is im- neither genetic resistance nor fungicide nicotianae. Phytopathology 62:993-997. perative that effective and cost efficient management appears to be perfect, com- 2. Ansani, C. V., and Matsuko, K. 1983. Infec- tividade e viabilidade de Phytophthora cap- replacements be identified and imple- bining the two may provide significant sici no solo. Fitopatol. Bras. 8:137-146. mented. control advances. 3. Ansani, C. V., and Matsuko, K. 1983. Both registered and experimental fumi- Information dissemination. While pre- Sobevivencia de Phytophthora capsici no gants have been tested in Michigan in con- venting the introduction of the pathogen is solo. Fitopatol. Bras. 8:269-276. junction with commercial producers at optimal, once P. capsici is introduced, 4. Babadoost, M. 2004. Phytophthora blight: A serious threat to cucurbit industries. APSnet known P. capsici–infested sites. A study several control measures need to be used in feature, Apr.-May. Online publication. Ameri- conducted by the authors in 2003 at a site a comprehensive management program to can Phytopathological Society, St. Paul, MN. infested with P. capsici showed that metam reduce losses from disease (Sidebar). As 5. Babadoost, M., and Islam, S. Z. 2001. Eval- sodium (Vapam), 66% methyl bromide, techniques and tools are developed to ease uation of fungicides for control of Phytoph- 33% chloropicrin (methyl bromide/chlor- the severity of crop loss due to P. capsici, thora blight of processing pumpkin, 2000. Fungic. Nematicide Tests 56:V65. Online opicrin), and 61% 1,3-dichloropropene, on-farm research trials and educational publication. 35% chloropicrin (Telone C-35) all effec- workshops are emphasized to enhance 6. Babadoost, M., and Islam, S. Z. 2002. Bell tively limited disease when used in a raised grower implementation. Further, education peppers resistant to Phytophthora blight. bed, plastic mulch system. of other crop specialists, extension person- (Abstr.) Phytopathology 92:S5. Genetic resistance. Genetic resistance nel, and consultants is ongoing to ensure 7. Babadoost, M., and Islam, S. Z. 2003. Fungi- cide seed treatment effects on seedling damp- or tolerance is often at the core of inte- that growers receive accurate and consis- ing-off of pumpkin caused by Phytophthora grated management programs and would tent information and recommendations. capsici. Plant Dis. 87:63-68. be especially helpful in managing P. cap- 8. Bernhardt, E. A., and Grogan, R. G. 1982. Ef- sici. Screening cucurbit germ plasm for Acknowledgments fect of soil matric potential on the formation and indirect germination of sporangia of Phy- resistance to P. capsici has been an ongo- Special thanks to M. McGrath (Cornell Univer- tophthora parasitica, Phytophthora capsici, sity, Riverhead, NY), G. Holmes (North Carolina ing effort at Michigan State University. To and Phytophthora cryptogea rots of tomatoes, State University, Raleigh), M. Davis (University of date, the fruit of over 300 cucumber varie- Lycopersicon esculentum. Phytopathology California, Davis), and W. Elmer (Connecticut ties have been screened for resistance to 72:507-511. Agric. Exp. Station, New Haven) for their assis- 9. Blears, M. J., De Grandis, S. A., Lee, H., and this pathogen, including pickling varieties, tance in collecting P. capsici isolates. Research Trevors, J. T. 1998. Amplified fragment slicing cucumber varieties, and plant intro- regarding fungicide and fumigation evaluation was length polymorphism (AFLP): A review of designed and conducted with the assistance of B. duction accessions. Although complete the procedure and its applications. J. Ind. Mi- Cortright (Michigan State University). We thank S. fruit disease resistance has not been ob- crobiol. Biotech. 21:99-114. Linderman (Michigan State University) for valu- served, varieties that appear to have lim- 10. Bowers, J. H., and Mitchell, D. J. 1990. Ef- able assistance in manuscript formatting and prepa- fect of soil-water matric potential and peri- ited lesion development and sporulation ration of the figures and tables. Portions of the odic flooding on mortality of pepper caused have been identified (A. Gevens and M. K. research discussed have been funded by the Pickle by Phytophthora capsici. Phytopathology and Pepper Research Committee of Michigan State Hausbeck, unpublished data). Babadoost 80:1447-1450. 11. Bowers, J. H., Papavizas, G. C., and Johns- ton, S. A. 1990. Effect of soil temperature and soil-water matric potential on the survival of Recommended Control Strategies for Blight Caused by Phytophthora capsici Phytophthora capsici in natural soil. Plant Dis. 74:771-778. Preplant 12. Bruin, G. C., and Edgington, L. V. 1980. In- • Use a seed treatment that is effective against oomycetes. duced resistance to ridomil of some oomy- • Consider a preplant banded fungicide application for infested fields. cetes. (Abstr.) Phytopathology 70:459. • Plant susceptible hosts in well-drained fields. 13. Bruin, G. C. A. 1981. Adaptive resistance in • Utilize raised beds (15 to 20 cm minimum) whenever possible. Peronosporales to metalaxyl. Can. J. Plant • Do not plant in low-lying areas of the field. Pathol. 3:201-206. Production 14. Bruin, G. C. A., and Edgington, L. V. 1982. • Monitor fields for disease, including damping-off, plant stunting, root and crown rot. Induction of fungal resistance to metalaxyl by

• Do not irrigate a field with water that contains runoff from fields with a history of ultraviolet irradiation. Phytopathology 72:476- 480. Phytophthora disease. 15. Café-Filho, A. C., and Duniway, J. M. 1996. • Irrigate conservatively, and if possible, do not irrigate close to harvest time. Effect of location of drip irrigation emitters • Plow under portions of the field with diseased plants, including healthy plants that border and position of Phytophthora capsici infec- diseased areas. tions in roots on Phytophthora root rot of pep- • Remove diseased fruit from the field. per. Phytopathology 86:1364-1369. • Never dump culls or diseased fruit from other fields or farms into production fields. Once 16. Café-Filho, A. C., Duniway, J. M., and Davis, P. capsici is introduced, it may remain indefinitely. R. M. 1995. Effects of the frequency of fur- • Apply fungicide preventively and frequently, especially for known problem fields. row irrigation on root and fruit rots of squash • Rotate the types of fungicides used. caused by Phytophthora capsici. Plant Dis. Postharvest 79:44-48. • Harvest fruit as soon as possible from problem fields and plow under crop residue 17. Crossan, D. F., Haasis, F. A., and Ellis, D. E. immediately. 1954. Phytophthora blight of summer squash. • Keep harvested fruit dry and cool. Plant Dis. Rep. 38:557-559. 18. Crute, I. R. 1987. The occurrence, character-

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1302 Plant Disease / Vol. 88 No. 12 76. Papavizas, G. C., Bowers, J. H., and Johns- ton, S. A. 1981. Selective isolation of Phy- tophthora capsici from soils. Phytopathology 71:129-133. 77. Parra, G., and Ristaino, J. 1998. Insensitivity to Ridomil Gold (mefenoxam) found among field isolates of Phytophthora capsici causing Phytophthora blight on bell pepper in North Carolina and New Jersey. Plant Dis. 82:711. 78. Parra, G., and Ristaino, J. B. 2001. Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing Phy- tophthora blight of bell pepper. Plant Dis. 85:1069-1075. 79. Ploetz, R. C., Heine, G., Haynes, J., and Wat- son, M. 2002. An investigation of biological attributes that may contribute to the importance of Phytophthora capsici as a vegetable pathogen in Florida. Ann. Appl. Biol. 140:61-67. 80. Polach, F. J., and Webster, R. K. 1972. Identi- fication of strains and inheritance of patho- Mary K. Hausbeck Kurt H. Lamour genicity in Phytophthora capsici. Phytopa- thology 62:20-26. Dr. Hausbeck is a professor and plant Dr. Lamour finished his Ph.D. in the 81. Ristaino, J. B. 1990. Intraspecific variation pathologist with extension and re- Botany and Plant Pathology Depart- among isolates of Phytophthora capsici from search responsibilities in the Depart- ment at Michigan State University in pepper and cucurbit fields in North Carolina. ment of Plant Pathology at Michigan 2001. His research focused on the Phytopathology 80:1253-1259. State University. She earned her B.S. population biology of Phytophthora 82. Ristaino, J. B. 1991. Influence of rainfall, and M.S. degrees in horticulture from capsici—particularly the impact of drip irrigation, and inoculum density on the Michigan State University and her sexual reproduction within naturally development of Phytophthora root and crown Ph.D. in plant pathology from the occurring populations. He participated rot epidemics and yield in bell pepper. Phyto- pathology 81:922-929. Pennsylvania State University. She in the APS I. E. Melhus graduate sym- 83. Ristaino, J. B., Hord, M. J., and Gumpertz, joined the faculty at Michigan State posium during the final year of his M. L. 1992. Population densities of Phy- University in 1990 as a visiting assis- doctoral work. Dr. Lamour studied tophthora capsici in field soils in relation to tant professor and became an assis- Phytophthora species as a postdoc- drip irrigation, rainfall, and disease incidence. tant professor in 1992. Her research toral researcher and as a visiting Plant Dis. 76:1017-1024. interests include the epidemiology and assistant professor at MSU before 84. Ristaino, J. B., and Johnston, S. A. 1999. management of diseases of veg- starting as an assistant professor in Ecologically based approaches to manage- etables in the field and flower crops the Department of Entomology and ment of Phytophthora blight on bell pepper. and vegetable transplants in the Plant Pathology at the University of Plant Dis. 83:1080-1089. greenhouse. Dr. Hausbeck received Tennessee in Knoxville in January of 85. Ristaino, J. B., Larkin, R. P., and Campbell, the Michigan Master Farmer Associate 2003. He received a National Science C. L. 1993. Spatial and temporal dynamics of Phytophthora epidemics in commercial bell Award and is a two-time recipient of Foundation CAREER award in 2004 to pepper fields. Phytopathology 83:1312-1320. the Michigan Extension Specialist develop reverse-genetic technology 86. Ristaino, J. B., Parra, G., and Campbell, C. L. Award for research and extension for Phytophthora functional genomics, 1997. Suppression of Phytophthora blight in contributions to the vegetable industry. and his research is focused on under- bell pepper by a no-till wheat cover crop. She also received the Society of standing the molecular machinery Phytopathology 87:242-249. American Florists’ 2004 Alex Laurie underlying Phytophthora’s unique 87. Satour, M. M., and Butler, E. E. 1967. A root Award for research and education. biology. and crown rot of tomato caused by Phy- tophthora capsici and P. parasitica. Phytopa- thology 57:510-515. 88. Satour, M. M., and Butler, E. E. 1968. Com- parative morphological and physiological Evaluation of fungicides and host resistance 1991. Are eukaryotic microorganisms clonal studies of the progenies from intraspecific for control of Phytophthora crown rot of sum- or sexual? A population genetics vantage. matings of Phytophthora capsici. Phytopa- mer squash, 1999. Fungic. Nematicide Tests Proc. Natl. Acad. Sci. USA 88:5129-5133. thology 58:183-192. 55:264. 99. Tompkins, C. M. 1937. Phytophthora rot of 89. Schlub, R. L. 1983. Epidemiology of Phy- 94. Springer, J. K., and Johnston, S. A. 1982. honeydew melon. J. Agric. Res. 54:933-944. tophthora capsici on bell pepper. J. Agric. Black polyethylene mulch and Phytophthora 100. Waldenmaier, C. M. 2004. Evaluation of Sci., Camb. 100:7-11. blight of pepper. Plant Dis. 66:281. fungicides for control of pumpkin diseases, 90. Schultheis, J. R., and Wehner, T. C. 1996. 95. Stevenson, W. R., James, R. V., and Rand, R. 2003. Fungic. Nematicide Tests 59:V064. Optimum density of determinate and normal E. 2000. Evaluation of selected fungicides to Online publication. pickling cucumbers harvested once-over. control Phytophthora blight and fruit rot of 101. Waterhouse, G. M. 1970. Taxonomy of Phy- (Abstr.) Proc. Pickling Cucumber Improve- cucumber. Fungic. Nematicide Tests 55:163. tophthora. Phytopathology 60:1141-1143. ment Conf., 5 Oct. 1995, Lexington, KY. 96. Stevenson, W. R., James, R. V., and Rand, R. 102. Weber, G. F. 1932. Blight of peppers in Flor- 91. Seebold, K. W., and Horten, T. B. 2003. E. 2001. Evaluation of selected fungicides to ida caused by Phytophthora capsici. Phytopa- Evaluation of fungicides for control of Phy- control Phytophthora blight and fruit rot of thology 22:775-780. tophthora crown and fruit rot of summer cucumber. Fungic. Nematicide Tests 56:V16. 103. Wiant, J. S. 1940. A rot of winter queen squash, 2002. Fungic. Nematicide Tests Online publication. watermelons caused by Phytophthora capsici. 58:V098. Online publication. 97. Tian, D., and Babadoost, M. 2004. Host range J. Agric. Res. 60:73-88. 92. Shaw, D. S. 1967. A method of obtaining of Phytophthora capsici from pumpkin and 104. Yoshikawa, M., Tsukadaira, T., Masago, H., single-oospore cultures of Phytophthora cac- pathogenicity of isolates. Plant Dis. 88:485- and Minoura, S. 1977. A non-pectolytic pro- torum using live water snails. Phytopathology 489. tein from Phytophthora capsici that macer- 57:454. 98. Tibayrenc, M., Kjellberg, F., Arnaud, J., Oury, ates plant tissue. Physiol. Plant Pathol. (UK) 93. Shishkoff, N., and McGrath, M. T. 1999. B., Breniere, S., Darde, M., and Ayala, F. 11:61-70.

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