Ecologically Based Approaches to Management of Phytophthora Blight on Bell Pepper

Jean Beagle Ristaino North Carolina State University, Raleigh

Stephen A. Johnston Rutgers Agricultural Research and Extension Center, Bridgeton, NJ

Symptoms and Life Cycle P. capsici can infect virtually every part of the pepper plant. The pathogen causes a root and crown rot on pepper (Fig. 1) and also forms distinctive black lesions on the Ecologically Based stem (Fig. 2). P. capsici can also infect the leaves and causes lesions that are circular, grayish brown, and water-soaked (Fig. 3). Leaf lesions and stem lesions are common Approaches to when inoculum is splash dispersed from the soil to lower portions of the plant. The pathogen can also infect fruit and causes Management lesions that are typically covered with white sporangia, a sign of the pathogen (Fig. 4). P. capsici typically causes a fruit of Phytophthora Blight rot or stem rot on cucumbers and squash (Fig. 5). P. capsici reproduces by both sexual and asexual means (Fig. 6). The pathogen pro- on Bell Pepper duces two mating types, known as the A1 and A2. These are actually compatibility types and do not correspond to dimorphic forms. Each mating type produces hor- mones that are responsible for gametangia differentiation in the opposite mating type. Both A1 and A2 mating types are common Phytophthora blight, caused by the oo- input of knowledge concerning a pathogen in fields in North Carolina and have also mycete pathogen, Phytophthora capsici, is life cycle, and secondarily, when necessary, been identified within the same plant (59). a devastating disease on bell pepper and on physical, chemical, and biological sup- P. capsici produces a male gametangium, cucurbit crops in the United States and plements for disease management. An un- called the antheridium, and a female worldwide (29,40). P. capsici causes a root derstanding of the ecological processes that gametangium, called the oogonium. The and crown rot, as well as an aerial blight of are suppressive to plant diseases is empha- antheridium is amphigynous in this spe- leaves, fruit, and stems, on bell pepper sized rather than secondary inputs (25). cies. Meiosis occurs within the gametan- (Capsicum annuum), tomatoes, cucumber, Fortunately, we have a considerable gia, and plasmogamy and karyogamy result watermelon, squash, and pumpkin (29,35, amount of information available on the 40,57,73). The disease was first described biology and ecology of P. capsici, which on bell pepper in New Mexico in 1922 can now be integrated to improve our abil- (40). In recent years, epidemics have been ity to manage the disease using ecologi- severe in areas of North Carolina, Florida, cally based approaches. Strategies recom- Georgia, Michigan, and New Jersey. Oo- mended for management of Phytophthora spores are believed to provide the initial blight involve integrated approaches that source of inoculum in the field, and the focus first on cultural practices that reduce disease is polycyclic within seasons high soil moisture conditions, but also (1,7,59,60,67). In this article, we discuss include monitoring and reduction of propa- the biology and epidemiology of Phy- gules of P. capsici that persist in the soil, tophthora blight on bell pepper and also utilization of cultivars with resistance to describe management strategies that can be the disease, and when necessary, judicious implemented based on existing knowledge fungicide applications. of the ecology of this devastating pathogen. The objectives of ecologically based pest management (EBPM) are the safe, profitable, and durable management of pests that includes a total systems approach (25). EBPM relies primarily on biological

Dr. Ristaino’s address is: Box 7616 Department of Plant Pathology, North Carolina State University, Raleigh 27695; E-mail: [email protected]

Publication no. D-1999-0927-01F Fig. 1. Root and crown rot on bell pep- Fig. 2. Black stem lesion caused by Phy- © 1999 The American Phytopathological Society per caused by Phytophthora capsici. tophthora capsici on bell pepper.

1080 Plant Disease / Vol. 83 No. 12 in the formation of oospores, which are the in saturated soil (3). Zoospores can move propagule types from soil, but it is not sexual spores that serve as the overwinter- readily under saturated conditions and sufficiently quantitative to estimate inocu- ing inoculum of the pathogen (Fig. 7). The infect roots or aboveground portions of lum densities (38). Infected leaf disks are diploid nature of the oomycetes was docu- plants (18,19). plated onto semiselective media, and the mented in early studies on the genetics of presence of colonies of the pathogen al- P. capsici (66). Oospores can germinate Detection and Quantification lows qualitative determination of the pres- either directly via formation of a germ tube Traditionally, P. capsici has been recov- ence of the pathogen in the soil or water or indirectly via sporangium formation ered by isolation of the pathogen from sample. Soil dilution plating directly onto (Fig. 6). infected tissue and plating onto a semise- semiselective media without prior sample The pathogen also reproduces asexually lective medium (32,41). The pathogen can incubation is useful for the quantification via sporangia that are borne on branched also be isolated from soil following soil of zoospores and sporangia in soil, whereas sporangiophores (40,69). Sporangia are dilution plating in dilute water agar onto a soil dilution plating after sample saturation generally ovoid and have a prominent pa- semiselective medium such as Masago’s and incubation allows recovery of oospores pillum at their apex (Fig. 8). Sporangia are medium (Fig. 9) (41). No single assay from soil (38). The incubation period pro- easily dislodged from the sporangiophore method is suitable for the accurate detec- vides an opportunity for oospores to ger- and can be dispersed within fields by wind, tion and quantification of all propagule minate and produce sporangia and zoo- rain, and irrigation water (8,11,61). Spo- types of P. capsici in soil (38). A leaf disk spores that are then detected by the dilution rangia germinate indirectly and release baiting assay in which circular disks of plate assay. Many of the traditional soil motile, biflagellate zoospores under condi- pepper leaves are floated on saturated soil assays are laborious and time-consuming tions of free moisture on plant surfaces or provides high levels of detection of all and require replication to reduce sampling variation. Traditionally, accurate identification of the pathogen required morphological ob- servations of sporangiophores, sporangia, zoospore release, and oospores (69). Iden- tification using classical taxonomic methods is time-consuming and requires exper- tise. Isozyme analysis, serological assays, DNA probes, restriction fragment length polymorphism (RFLP), and polymerase chain reaction (PCR) methods have been used to identify and evaluate the genetic variation among Phytophthora species (16,20,28,39,45,46,50). The nuclear small subunit rDNA sequences evolve relatively slowly and are useful for studying distantly related organisms, whereas the internal transcribed spacer (ITS) regions and inter- genic region of the nuclear rRNA repeat units vary among species and populations (74). Sequencing studies with small subunit ribosomal RNA sequences (20) have elucidated the evolutionary lineage of Fig. 3. Grayish brown water-soaked lesions on leaves of bell pepper caused by Phy- the oomycetes. Phytophthora species are tophthora capsici. actually more closely related to nonphoto-

Fig. 4. Lesion caused by Phytophthora capsici with white mycelium and sporangia of the pathogen on the bell pepper fruit. Fig. 5. Phytophthora blight lesions on fruit of cucumbers and squash.

Plant Disease / December 1999 1081 synthetic algae than to true fungi or land 140 bp, are present in P. capsici after di- studies are also needed to relate levels of plants and have been placed in the phylo- gestion with MspI (Fig. 11, lanes 5). P. propagules of the pathogen to levels of genetic assemblage, stramenopile (14,24). capsici can be differentiated from P. DNA recovered from soil. The nuclear small subunit rDNA and citrophthora by restriction digest of ITS ITS sequences have been used to develop DNA with RsaI (64). Impact of Soil Water rapid tools for identification of the eco- PCR assays should make diagnosis of P. Soil moisture, especially the matric nomically important species within the capsici in infected plant material, soil, or component of soil water potential (ψm), genus Phytophthora (39,64). A primer water samples more accurate. PCR is more plays an important role in the life cycle of called PCAP was developed based on se- rapid and efficient than traditional isolation Phytophthora spp. that cause root rots, quence data published previously for a P. methods in identification of P. capsici in including P. capsici (18,19). Sporangia of capsici-specific DNA probe (39,64). PCAP infected plant samples. We tested the PCR P. capsici form abundantly in saturated soil is used with ITS 1 in PCR reactions and assay and found that 92% of infected pep- within 24 h on mycelial disks that are first amplifies an approximately 172-bp frag- per plants with visible lesions that were incubated at drier ψm of –20.0 to –30.0 ment of DNA in all isolates of P. capsici positive by traditional isolation on media J/kg (1 J/kg = 10 millibars; a ψm value of 0 tested from a range of hosts (Fig. 10, lanes were also positive by PCR using the PCAP is fully saturated soil) (3). Release of zoo- 2 to 9 and 12). Isolates of P. citrophthora and ITS 1 primers (64). PCR with these spores from sporangia in Phytophthora (Fig. 10, lane 10) are also amplified by the primers also detected infection in 32% of species is extremely sensitive to small PCAP primer, but the amplified product the samples where the pathogen was not changes in ψm and occurs predominantly at size is larger than that of P. capsici (Fig. identified previously by traditional isola- high ψm values between 0 and –1.0 J/kg 10, lanes 2 to 9 and 12) or P. citricola (Fig. tion on agar media (64). This indicates that (19). Zoospores are released from sporan- 10, lane 11). Digestions of the 172-bp the PCR technique was able to detect false gia of P. capsici previously formed at soil fragment with MspI allows differentiation negatives and could be useful for detection water ψm of –30.0 J/kg within 4 h of soil of P. capsici from P. citrophthora and P. of the pathogen in lesions during the incu- saturation (3). citricola, which are not digested by this bation period, when symptoms and signs of P. capsici produces oospores, which are enzyme. None of the other major species the pathogen are not obvious. PCR meth- considered to be primary survival struc- of Phytophthora, including P. cactorum, P. ods are not useful in detection of the tures in soil (1,7,56). Factors affecting the palmivora, P. nicotianae, P. infestans, P. pathogen in severely decayed tissue, since germination of oospores of P. capsici have mirabilis, P. fragariae, P. soj ae, P. megas- inhibition of PCR by decomposing plant been well documented and include light, perma, P. cinnamomi, P. cryptogea, and P. products or bacteria can occur. Further temperature, and soil water matric poten- erythroseptica, are amplified with the research needs to be done to develop in- tial (6,7,26,27). Oospores have been re- PCAP primer (64). P. capsici (Fig. 11, lane field, quick PCR assays that can be used ported in naturally infected pepper plants 5) can also be differentiated from P. citri- with fluorescent detection methods for and germinate predominantly by formation cola (Fig. 11, lane 6) by restriction digest assays of the pathogen directly from plant, of sporangia in distilled water, root extract, of ITS DNA with MspI. Four fragments, soil, or water samples using miniaturized and soil extract (26,52,56,59). Oospore approximately 290 bp, 219 bp, 194 bp, and thermocycling devices. Quantitative PCR germination in root and soil extract is

Fig. 6. Life cycle of Phytophthora capsici, causal agent of Phytophthora blight on bell pepper.

1082 Plant Disease / Vol. 83 No. 12 asynchronous and increases with time of contact. Inoculum can also spread in sur- Phytophthora diseases, and this is the pre- incubation (26). Germination of oospores face water, or inoculum can be splash dis- dominant mechanism of dispersal of P. is initiated when oospores are first incu- persed from soil to leaves, stems, or fruit. capsici in naturally infested fields (8,11– bated in drier soils at ψm of –2.5 to –10.0 Local aerial dispersal from sporulating 13,48,62,63). Soilborne members of the J/kg prior to saturation (27). lesions on leaves, stems, or fruit may also genus Phytophthora are disseminated con- Experiments have been conducted under occur in this pathosystem. siderable distances in the direction of water controlled conditions of ψm to determine Components of the primary inoculum flow in furrows during irrigation events the effect of cyclical changes in ψm on dispersal of P. capsici have been evaluated (11,13,48). For example, inoculum of P. disease caused by oospores in soil (6,27). in field soils (63,72). Primary inoculum of capsici can be dispersed up to 70 m from Final incidence of disease was higher in P. capsici in the soil causes root infections point sources of inoculum with furrow plants held at ψm of –2.5, –5.0, or –10 J/kg that progress to crown infections (63). irrigations (13). Movement of inoculum for 10 days than for 5 days prior to satura- Wilting almost always precedes crown down rows with surface rain water or fur- tion, and disease increased with decreasing lesion development in naturally infested row irrigation can result in rapid increases ψm (27). Periods of continuous soil satura- fields, suggesting the importance of root in disease (13,63). P. capsici can spread tion are not conducive to oospore germina- infections and the soilborne phase of the from plant to plant within rows from initial tion or disease, and in fact, disease devel- disease (63). In controlled field tests, an inoculum sources and across rows from opment was less than 10% in plants grown infected plant containing sporangia and primary foci of disease (8,65). Spread of in oospore-infested soil maintained under zoospore inoculum was placed in PVC inoculum may be detected unidirectionally constant saturation (27). These results tubes on the soil surface, and rainfall within many rows for long distances, and serve to illustrate that it is the cyclical events spread inoculum to roots in soil. disease foci increase in size over time (Fig. changes in ψm that stimulate oospore ger- Infection of the crowns and roots of adja- 12A and B) (8,11,60,65). mination in soil and infection in this patho- cent plants in the plot was more rapid Splash dispersal of inoculum from the system. Even brief periods of soil satura- when inoculum moved to roots than when soil to aboveground parts of plants with tion after oospores have germinated in spread of inoculum of the pathogen in soil rainfall, wind, or overhead irrigation water drier soils can result in high levels of dis- occurred via growth of healthy roots to can also occur, resulting in rapid pathogen ease. Periods of constant soil saturation inoculum buried in soil or root-to-root inhibit oospore germination and disease. contact in soil (72). Management strategies Further experiments are needed in the field that minimize inoculum dispersal in and on in regions where pepper is grown under the soil surface have great potential for irrigated conditions to determine whether disease reduction in this pathosystem. disease due to primary inoculum from Inoculum movement down rows with oospores can be reduced by maintaining surface water is also an important mecha- more constant soil moisture throughout the nism of dispersal for many polycyclic growing season. Dispersal of P. capsici and Disease Development Virtually every part of the plant can become infected by P. capsici, and the patho- Fig. 10. DNA amplified with the primers gen can spread by several distinct mecha- PCAP and ITS 1 from isolates of Phy- nisms, including primary inoculum move- tophthora capsici (lanes 2 to 9, 13). The ment from root to root down rows via (i) primer also amplifies P. citrophthora root growth to inoculum, (ii) inoculum (lane 10) and P. ci tri co l a (lane 11). Diges- movement to roots, or (iii) root-to-root tion with MspI differentiates P. capsici from the other two species. Lanes 1 and 14 contain 100-bp ladders, and lane 13 Fig. 8. Sporangia of Phytophthora cap- contains a no-template control. sici are asexual structures that release zoospores under saturated conditions. They have a medium pedicel and are easily dislodged from the sporangiophore.

Fig. 11. Restriction digest with MspI of DNA amplified with universal primers ITS 5 and ITS 4 from Phytophthora cactorum (lane 2), P. infestans (lane 3), P. mirabilis (lane 4), P. capsici (lane 5), and Fig. 7. Thick-walled oospore of Phytoph- P. ci tri co l a (lane 6). P. capsici has a thora capsici. An amphigynous an- Fig. 9. Petri dish containing semiselec- unique amplified fragment restriction theridium is attached at the base of the tive Masago’s medium and colonies of fingerprint. Lanes 1 and 7 contain 100- oospore. Phytophthora capsici isolated from soil. bp ladders.

Plant Disease / December 1999 1083 spread and disease increase (8,37,63). Spo- agement strategies based on the ecology of (>23 cm high) to avoid extensive soil rangia can move rapidly on polyethylene the pathogen. moisture accumulation around the base of mulch with rain events, resulting in rapid Problem: Phytophthora blight is more plants (Fig. 14). Beds should be prepared disease spread (8,65). In artificially in- severe under conditions of high soil mois- prior to transplanting. Flat bed culture and fested plots, final disease became very high ture from frequent rainfalls or irrigations. ridging by cultivation after transplanting when surface inoculum was spread on Management strategy: Use site prepa- can cause water to accumulate around the plastic or splash dispersed on bare soil ration, waterway systems, bed structures, crowns of plants, thus exacerbating dis- (Fig. 13). If the numbers of infected plants and transplanting procedures that minimize ease. Peppers should be transplanted on top are minimal, these plants can be removed water accumulation and irrigate appropri- of a small ridge or raised, crowned bed in from fields to reduce the amount of spo- ately. bare ground culture (Fig. 15A). Rainfall rangial inoculum that is dispersed in the Site preparation. Fields must be well during the season can result in bed field during rainfall events. In addition, drained and must not have low-lying areas “washout” in bare ground culture, so culti- removal of a 61- to 91-cm-wide section of that collect water, since these areas are vation may be necessary to reshape beds polyethylene mulch between healthy and often the focal points for epidemic devel- during the growing season. Polyethylene infected plants can be useful to prevent opment (37) (Fig. 12A and C). Waterway mulch culture of pepper can result in in- spread of the pathogen down rows. systems and drainage ditches can be con- creased yields and has become the pre- structed in fields with extensive low-lying ferred method of production in the major- Ecologically Based areas prior to production of peppers, and a ity of production areas in the United States Disease Management land plane or laser level can be used to (Fig. 14B and C). However, polyethylene A great deal is known about the biology level the field as much as possible before mulch culture of pepper can result in high and ecology of P. capsici that can be used planting to minimize areas of standing levels of Phytophthora blight if the proper to develop ecologically based disease man- water. In addition, fields can be subsoiled cultural practices are not implemented agement strategies. Phytophthora blight or chisel plowed to improve drainage in (8,65) (Figs. 13 and 14A). Beds should be poses many problems for commercial pep- compacted areas (22). shaped with a crown to allow water to run per production. For each problem listed Transplanting procedures. Peppers should off during rainfall events (Fig. 14B and C). below, we have developed disease man- be transplanted on raised, crowned beds Transplanting equipment must also be adjusted properly to avoid making depres- sions in beds during transplanting that accumulate water during rainfall or irrigation events and create conditions conducive for infection by P. capsici around the crown of the plant (Fig. 15B). On polyethylene mulch, the transplanter must be driven slowly enough to allow the entire root ball to be buried in soil, and sur- rounding soil needs to be used to fill in transplant holes to create a mound at the base of each plant (Fig. 15C and D). Phy- tophthora blight can be severe if this pro- cedure is not followed and a heavy rainfall occurs in a P. capsici–infested field. Phytophthora blight usually develops first in fields in low-lying areas where water accumulates between beds at the ends of rows (37,62) (Figs. 12 and 14D). A 76-m-wide waterway area can be con-

Fig. 13. Incidence of plant mortality Fig. 12. Spatial pattern map of disease severity caused by Phytophthora capsici on caused by Phytophthora capsici on bell bell pepper at (A) day 168 and (B) day 217 in a naturally infested field. Spatial pattern pepper in artificially infested plots af- map of (C) gravimetric soil water content and (D) propagule levels of the pathogen in fected by cultural and chemical control soil at day 171 in the same field. strategies.

1084 Plant Disease / Vol. 83 No. 12 structed at both ends of the field to ac- reducing inoculum spread and subsequent (Fig. 16). Use of filtered irrigation water commodate drainage of large volumes of disease. from subsurface wells can reduce the water from rainfall events or prolonged Depth of placement of drip irrigation problem of contamination of water sup- irrigation so excess water does not back up emitters in soil can also have a large im- plies by the pathogen. In addition, testing into the field. Furrows also need to be pact on Phytophthora blight epidemics water samples for the presence of the unobstructed between beds at both ends of (10). Drip irrigation close to the stem or pathogen and if necessary subsequent the rows to allow water to drain from the crown of the plant results in high disease, treatment of water with chlorine or fungi- field readily. whereas subsurface drip irrigation results cides can reduce propagule levels of the Irrigation management. Both rainfall in lower levels of disease (10). Drip irriga- pathogen. Water from fields with a history and irrigation have large effects on the tion lines positioned 15 cm below ground of disease should not be drained into irri- time of onset and final incidence of Phy- level in the plant row result in the most gation water supplies. tophthora blight epidemics (4,8,10,23,60). efficient control of Phytophthora blight in Problem: P. capsici splashes from soil Disease incidence can become very high the field without reducing yields (10). in the row or on polyethylene mulch from after either heavy rainfall or frequent drip Early-season propagule densities of the between rows to foliage and causes infec- irrigation (60). Propagule densities of P. pathogen in soil are higher near the drip tions. capsici in soils are highest early in epi- irrigation line than in drier soils opposite Management strategy: Reduce splash demic development in plots that are irri- the drip line (61). Irrigation stimulates dispersal of inoculum from soil with straw gated frequently and are highly correlated zoospore discharge from sporangia and mulch between rows or on bare soil with with high soil water content and disease dispersal in soil and also stimulates root stubble from a cover crop. incidence early in the season (61). In fact, growth, thus making root contact with Modifications in cultural practices, in- disease occurrence in fields is spatially inoculum more probable. In arid agricul- cluding growth of pepper in a no-till cover correlated with areas of fields where high ture regions, subsurface irrigation encour- crop, can have a large impact on the devel- soil moisture occurs early in the season ages root growth deep in the soil profile opment of Phytophthora blight epidemics (Fig. 12A and C) (23,37). Propagules of and minimizes inoculum dispersal near the in bell pepper (Fig. 17). Dispersal of soil the pathogen may be distributed widely in crown and major roots of the plant at the inoculum can be suppressed and final inci- soil in a given field (Fig. 12D), but disease surface (10). Thus, the plant can escape dence of disease can be greatly reduced develops initially where conditions of soil disease by irrigation management. when pepper is grown in stubble from a moisture are conducive (37). Soil moisture in polyethylene mulch fall-sown, no-till rye or wheat cover crop ψ Irrigation frequency, duration, and the culture of peppers can be maintained at m (65) (Fig. 13). In controlled field experi- mode of irrigation can all affect the inci- of 20 to 40 J/kg in coarse-textured soils ments, final disease incidence was highest dence of Phytophthora blight epidemics utilizing tensiometers placed at 15- and 30- and pathogen spread occurred within and (4,10,11,60). Disease incidence and sever- cm depths within the bed. Irrigation can across rows when pepper was planted into ity are more severe and onset occurs earlier thus be timed based on actual reading of bare soil and all dispersal mechanisms with more frequent than with less frequent ψm (22). Phytophthora blight can be effec- were operative (Fig. 13). Inoculum moved irrigation episodes (11,12,60). A less fre- tively managed by avoiding excessive lev- rapidly down black polyethylene mulch quent irrigation schedule of 21 days versus els of high soil moisture and excessive with rainfall events, and disease onset was 7 days resulted in less Phytophthora blight cyclical changes in soil moisture in the earliest in these plots. The fungicide without a reduction in yield (11). In areas beds. metalaxyl applied in the irrigation system where furrow irrigation is used, alternate- Maintenance of an irrigation water did not suppress within-row spread of sur- row irrigations can reduce the incidence of source free from the pathogen is also a face inoculum from a sporulating fruit on Phytophthora root rot in pepper to a greater very important management strategy for plastic but did limit across-row spread; extent than a combination of irrigation of Phytophthora blight. If irrigation ponds final disease incidence in metalaxyl-treated every row and application of fungicides contain inoculum of the pathogen and are plots was less than 10%. Pathogen disper- (4,17). This strategy reduces the amount of used as a source of water for drip or over- sal mechanisms were modified most dra- free water that runs down furrows, thus head irrigation, results can be disastrous matically by the no-till cropping system

Fig. 14. (A) High incidence of Phytophthora blight using Fig. 15. (A) Pepper transplanted into soil on a small ridge in bare polyethylene mulch without raised bed culture. (B) Crown ground culture. (B) A water wheel transplanter that holds water raised bed construction prior to laying polyethylene mulch. and punctures polyethylene mulch and soil prior to manually (C) Bell pepper production on well-constructed raised beds transplanting peppers. (C) Recently transplanted peppers with a with polyethylene mulch culture. (D) Water accumulation at water wheel transplanter. Note the depression around the base of the ends of rows between beds where drainage ditches were each transplant. (D) Supplemental soil added around the base of a not established to allow excess water to leave fields following pepper transplant to fill in the depression following transplanting rain events. with a water wheel transplanter in polyethylene mulch culture.

Plant Disease / December 1999 1085 (Fig. 13). We know little about the biologi- dence following soil treatment with methyl common in high rainfall areas. Therefore, cal effects of green manures, living bromide in this study (75). Unfortunately, regularly scheduled applications of a cop- mulches, or intercropping with summer soil solarization often only kills pathogen per fungicide must be applied from mid- cover crops on epidemic development in propagules at shallow depths in soil. season until the end of the season to assist this pathosystem. Further experiments are Propagule densities of P. capsici at 10-cm in control of this phase of the disease on needed to examine the effects of different depths after solarization were similar to Paladin. Additional new sources of germ kinds of cover crops, including nitrogen those in methyl bromide–treated soil, but plasm and breeding efforts are needed to fixing legumes, on disease suppression and no reductions in propagule densities oc- identify and map resistance genes in bell yield of bell pepper. curred at soil depths of 25 cm after solari- pepper to P. capsici and develop durable Problem: Inoculum of the pathogen zation treatments (15). Soil solarization has levels of resistance in pepper. persists in soil. been used effectively to control Phytoph- Problem: Resistance to the fungicide Management strategy: Use long crop thora blight in plastic houses in Italy (55). metalaxyl has been found in populations of rotation schedules, soil solarization, or Fewer studies have been conducted to P. capsici in fields. organic amendments to reduce pathogen examine the effect of soil amendments on Management strategy: Use fungicide propagule levels in soil. Phytophthora blight. Soil amendments with mixtures, alternative fungicides, or bio- Crop rotation. Peppers should not be chitosan or crab shell waste were suppres- logical alternatives to reduce populations produced in a field that has had a crop of sive to Phytophthora blight in some years of resistant isolates in the field. peppers, cucumbers, muskmelons, pump- in Florida, but results were variable (33). Chemical measures can be integrated kins, winter squash, summer squash, wa- Further field work with organic soil into Phytophthora blight management pro- termelons, eggplants, or tomatoes for at amendments including animal manures and grams to provide control of the pathogen in least 3 years because propagules of P. cap- composted plant materials is needed to test areas of the field where high soil moisture sici persist in field soils following the re- their efficacy in suppression of Phy- may accumulate, since cultural practices peated growth of susceptible crops. Oo- tophthora blight before recommendations are generally not completely implemented spores of the pathogen are capable of can be made. or effective in a given field. The first line survival in the absence of a host crop, but Problem: Most pepper varieties cur- of defense against this disease needs to viability declines to a large extent after 27 rently grown are susceptible to P. capsici. focus on strategies that reduce soil mois- weeks (7). Oospores remained viable and Management strategy: Deploy pepper ture conditions conducive for disease. Use capable of causing disease in a greenhouse varieties with resistance to the pathogen in of fungicides alone for control of Phy- bioassay after 16 weeks (7). Sporangia and the field on a wider scale. tophthora blight without the implementa- zoospores have limited survival ability in Numerous attempts have been made to tion of ecologically based practices can soil and are not detectable after 4 weeks find sources of resistance to P. capsici in result in a high incidence of disease in P. (7). Propagule densities of the pathogen are bell peppers; yet few resistant cultivars are capsici–infested fields. greatly reduced in the absence of a suscep- deployed commercially (2,34,49,58). One Captafol (trade name Difolatan) was one tible crop; thus crop rotation is an excellent of the first commercial cultivars with re- of the most effective fungicides for the and straightforward strategy to reduce sistance to Phytophthora blight was Adra control of the foliar phase of Phytophthora disease incidence in subsequently grown from Abbott & Cobb Seed Co., Feaster- blight and received emergency registration susceptible crops. ville, PA (11). The resistant cultivar Emer- (Section 18 specific exemption of the Fed- Soil solarization and organic amend- ald Isle was released from Harris Moran eral Insecticide Fungicide and Rodenticide ments. Experiments have been conducted Seed Co., Modesto, CA. Unfortunately, Act) in New Jersey in 1980 and 1981 to evaluate the use of soil solarization or Adra and Emerald Isle did not possess (31,51,68). However, Captafol was with- soil amendments with organic materials on sufficient horticultural characteristics to be drawn from the U.S. marketplace in 1982 the incidence of Phytophthora blight in bell accepted by the majority of bell pepper and never received federal registration for pepper (15,33,55,75). Soil solarization growers in the United States. Recently, the use on peppers to control Phytophthora involves the heating of soil under clear resistant cultivar Paladin was released by blight. polyethylene mulch during the hottest Novartis Seeds Inc., Rogers Brand, Boise, In the early 1980s, the systemic fungi- months of the summer and has been dem- ID. Paladin possesses excellent resistance cide metalaxyl (trade name Ridomil, No- onstrated to reduce levels of many soil- to the crown rot phase of Phytophthora vartis Crop Protection) was demonstrated borne pathogens (15,75). Soil solarization blight and has excellent horticultural char- to provide excellent control of the crown alone reduced disease incidence from 39.8 acteristics that enable it to be marketed rot phase of Phytophthora blight (30,42, and 42.9% to 24.1 and 19.7% in 2 years of commercially (Fig. 18). However, Paladin 43,51,68). Metalaxyl received a federal field tests in Turkey (75). In fact, disease does not possess resistance to the foliar registration for the control of Phytophthora incidence following solarization was not phase of Phytophthora blight, which is blight of peppers in the United States in the significantly different from disease inci- 1990s. Two applications of metalaxyl are required at 30-day intervals following the

Fig. 17. Pepper grown in stubble from a Fig. 16. Phytophthora blight on bell fall-grown no-till wheat cover crop. The pepper grown on black polyethylene wheat straw was mowed and distributed Fig. 18. Bell pepper cultivar Paladin, plastic. The pathogen was distributed in the furrows to slow splash dispersal which is resistant to Phytophthora cap- through the field via a contaminated of the pathogen, thus greatly reducing sici, on the left and a susceptible local irrigation pond and drip irrigation. disease. variety of a cherry pepper on the right.

1086 Plant Disease / Vol. 83 No. 12 initial application at planting in order to hydroponic system were treated with for- Plant Pathology; Marcia Gumpertz, Department of maintain control of Phytophthora blight mulations of phosphite (Nutri-Phite), Statistics, N.C. State University; Robert Larkin, USDA, University of ME, Orono; Ludwik and avoid phytotoxicity of the older leaves. which is the salt of phosphorous acid (21). Sujkowski, Laboratory Corporation of America, Foliar applications of a copper-containing The incidence of Phytophthora blight was Research Triangle Park, NC; Ronald French, fungicide are then made every 7 to 10 days significantly reduced by treatment with University of Florida; Melanie Hord, University of from 2 to 3 weeks following the last phosphite; yet the pathogen was isolated Costa Rica; and Pam Puryear, Department of metalaxyl application until the end of the from plants in which symptoms did not Communication Services, N.C. State University, occur (21). These alternative chemical are gratefully acknowledged. The pathogen life season (22). cycle was drawn by Greg Parra. Resistance to metalaxyl has been re- methods of disease control may have ap- ported in many oomycete pathogens (47). plications for Phytophthora blight in field Literature Cited Until recently, metalaxyl-resistant isolates situations where inoculum is dispersed into 1. Ansani, C. V., and Matsuoka, K. 1983. Infec- of P. capsici had only been reported in the fields from infested irrigation water, but tividade e viabilidade de oosporos de Phy- laboratory after mutagenesis (5,9). Re- further field trials are needed to confirm or tophthora capsici no solo. Fitopatol. Bras. cently, the manufacturer replaced meta- refute this hypothesis. 8:137-146. laxyl with mefenoxam (trade name 2. Barksdale, T. H., Papavizas, G. C., and John- Outlook ston, S. A. 1984. Resistance to foliar blight Ridomil Gold). Mefenoxam is the active and crown rot of pepper caused by Phy- component contained in the fungicide Phytophthora blight of bell pepper has tophthora capsici. Plant Dis. 68:506-509. metalaxyl and is applied at similar fre- increased in occurrence and severity in 3. Bernhardt, E. A., and Grogan, R. G. 1982. quencies and methods as metalaxyl, but at recent years in many areas of the United Effect of soil matric potential on the forma- lower rates of manufactured product. Me- States. In some regions, this situation may tion and indirect germination of sporangia of Phytophthora parasitica, P. capsici, and P. fenoxam was used widely in peppers for be exacerbated by intensive production of cryptogea. Phytopathology 72:507-511. the first time in 1997. Disease occurred in susceptible crops in the same fields with 4. Biles, C. L., Lindsey, D. L., and Liddell, C. fields that were treated with multiple ap- minimal rotation to nonhost crops. In other M. 1992. Control of Phytophthora root rot of plications of mefenoxam in 1997 in North areas, development of fungicide-resistant chile peppers by irrigation practices and fun- Carolina and New Jersey (53). Infected isolates may be the source of the problem. gicides. Crop Prot. 11:225-228. 5. Bower, L. A., and Coffey, M. D. 1985. Devel- plants from 12 fields in North Carolina and Effective management of the disease will opment of laboratory tolerance to phosphorus one in New Jersey were sampled, and P. require ecologically based approaches such acid, and fosetyl-Al, and metalaxyl in Phy- capsici was isolated from tissue. A total of as those described in this paper. In addi- tophthora capsici. Can. J. Plant Pathol. 7:1-6. 161 isolates were screened for sensitivity tion, innovative research to develop and 6. Bowers, J. H., and Mitchell, D. J. 1990. Effect to mefenoxam in petri dish assays. Thirty- implement improved methods for detection of soil-water matric potential and periodic flooding on mortality of pepper caused by three percent of the isolates were sensitive, of the pathogen in soil are needed so that Phytophthora capsici. Phytopathology 10% of the isolates were intermediate in fungicides can be applied to soil only 80:1447-1450. sensitivity, and 57% of the isolates were where necessary and more judiciously 7. Bowers, J. H., Papavizas, G. C., and Johnston, resistant to mefenoxam (53). Resistance rather than on a widespread scale. The S. A. 1990. Effect of soil temperature and frequencies ranged from 25 to 100% within development of fungicide resistance in P. soil-water matric potential on the survival of Phytophthora capsici in natural soil. Plant sampled populations from individual fields capsici populations poses new problems Dis. 74:771-777. (53). The greatest number of resistant iso- for the use of Ridomil Gold, which is cur- 8. Bowers, J. H., Sonoda, R. M., and Mitchell, lates was recovered from fields where rently one of the few labeled compounds D. J. 1990. Path coefficient analysis of the ef- Ridomil Gold was used alone rather than in available for chemical control of the root fect of rainfall variables on the epidemiology combination with other fungicides. Both and crown rot phase of this disease on of Phytophthora blight of pepper caused by Phytophthora capsici. Phytopathology mating types were found among resistant pepper. Resistance management plans will 80:1439-1446. isolates, suggesting that these isolates may be needed to reduce future occurrences of 9. Bruin, G. C. A., and Edington, L. V. 1981. persist as oospores in soil. Mefenoxam- resistance to mefenoxam in populations of Adaptive resistance in Peronosporales to resistant isolates of P. capsici have also P. capsici in the field. Improved monitor- metalaxyl. Can. J. Plant Pathol. 3:201-206. been reported recently from fields in Italy, ing methods for detection of pathogen 10. Café-Filho, A. C., and Duniway, J. M. 1995. Effect of location of drip irrigation emitters Georgia, and Michigan (36,44,54). Alter- resistance to this fungicide are also needed and position of Phytophthora capsici infec- native fungicides with activity against in this and other Phytophthora species. tions on roots on Phytophthora root rot of oomycete pathogens have not been ade- Durable host resistance may represent one pepper. Phytopathology 86:1364-1369. quately evaluated in the field for Phy- of the most effective means of disease 11. Café-Filho, A. C., and Duniway, J. M. 1995. tophthora blight, and none are presently management, yet few resistant cultivars are Effects of furrow irrigation schedules and host genotype on Phytophthora root rot of labeled. However, a number of compounds currently available with horticultural traits pepper. Plant Dis. 79:39-43. with action against oomycete pathogens that are acceptable to growers. Manage- 12. Café-Filho, A. C., Duniway, J. M., and Davis, are currently being evaluated as alterna- ment of soil water via manipulation of R. M. 1995. Effects of the frequency of fur- tives. cultural practices that reduce dispersal of P. row irrigation on root and fruit rots of squash Work is underway by a number of re- capsici will continue to be the key to an caused by Phytophthora capsici. Plant Dis. 79:44-48. searchers to test alternative fungicides and ecologically based system for management 13. Café-Filho, A. C., and Duniway, J. M. 1995. biologicals for management of Phytoph- of Phytophthora blight in bell pepper. Dispersal of Phytophthora capsici and P. thora blight on bell pepper. Spread of P. parasitica in furrow-irrigated rows of bell capsici was greatly reduced and disease Acknowledgments pepper, tomato and squash. Plant Pathol. incidence was low in peppers grown in Research discussed in this article was funded in 44:1025-1032. part by the North Carolina Agricultural Research 14. Chesnick, J. M., Tuxbury, K., Coleman, A., rock wool hydroponic systems that were Burger, G., and Lang, F. 1996. Utility of the treated with the nonionic surfactant Aqua- Service, the New Jersey Agricultural Extension Service, the North Carolina Vegetable Growers mitochondrial nad4L gene for algal and pro- Gro 2000L (Aquatrols, Cherry Hills, NJ) Association, and the National Research Initiatives tistan phylogenetic analysis. J. Phycol. (70). The surfactant reduced the dispersal Competitive Grants Program, United States De- 32:452-456. of zoospores in the hydroponic solution partment of Agriculture. Lee Campbell thoroughly 15. Coelho, L., Chellemi, D. O., and Mitchell, D. reviewed this manuscript before his untimely J. 1999. Efficacy of solarization and cabbage from a point source of inoculum and killed amendment for the control of Phytophthora zoospores. An extensive review of the death, and his many contributions over the years on aspects of this work will be missed and are spp. in North Florida. Plant Dis. 83:293-299. mode of action of biosurfactants has been gratefully acknowledged. Many other contribu- 16. Cooke, D. E. L., and Duncan, J. M. 1997. published (71). In another study, tomato tions from Agricultural Research Specialists Greg Phylogenetic analysis of Phytophthora spe- and pepper plants grown in a greenhouse Parra and Charles Harper (retired), Department of cies based on ITS 1 and 2 sequences of the

Plant Disease / December 1999 1087 rDNA gene repeat. Mycol. Res. 101:667-677. 23. Gumpertz, M. L., Graham, J., and Ristaino, J. 1991. Restriction fragment length polymor- 17. Daniell, I. R., and Falk, C. L. 1994. Economic B. 1997. Autologistic model of spatial pattern phisms of mtDNA among Phytophthora cap- comparison of Phytophthora root rot control of Phytophthora epidemics in bell pepper: Ef- sici isolates from pepper (Capsicum annuum). methods. Crop Prot. 13:331-336. fects of soil variables on disease presence. J. System. Appl. Microbiol. 14:111-116. 18. Duniway, J. M. 1976. Movement of zoospores Agric. Biol. Environ. Stat. 2:1-26. 29. Hwang, B. K., and Kim, C. H. 1995. Phy- of Phytophthora cryptogea in soils of various 24. Gunderson, J. H., Elwood, H., Ingold, H., tophthora blight of pepper and its control in textures and matric potentials. Phytopathol- Kindle, A., and Sogin, M. L. 1987. Phyloge- Korea. Plant Dis. 79:221-227. ogy 66:877-882. netic relationships between chlorophytes, 30. Johnston, S. A. 1982. Control of the crown rot 19. Duniway, J. M. 1979. Water relations of water chrysophytes, and oomycetes. Proc. Natl. phase of Phytophthora blight of pepper with molds. Annu. Rev. Phytopathol. 17:431-460. Acad. Sci. U.S.A. 84:5823-5827. fungicide drenches, 1981. Fungic. Nematicide 20. Forster, H., Coffey, M., Elwood, H., and 25. Hardy, R. 1996. Ecologically-based Pest Tests 37:73. Sogin, M. L. 1990. Sequence analysis of the Management: New Solutions for a New Cen- 31. Johnston, S. A., and Springer, J. K. 1980. small subunit ribosomal RNA’s of three zoo- tury. National Research Council, National Control of pepper blight with foliar sprays, sporic fungi and implications for fungal evo- Academy Press, Washington, DC. 1979. Fungic. Nematicide Tests 35:77-78. lution. Mycologia 82:306-312. 26. Hord, M. J., and Ristaino, J. B. 1991. Effects 32. Kannawischer, M. E., and Mitchell, D. J. 21. Forster, H. G., Adaskaveg, J. E., Kim, D. H., of physical and chemical factors on the ger- 1978. The influence of a fungicide on the epi- and Stanghellini, M. E. 1998. Effect of mination of oospores of Phytophthora capsici demiology of black shank of tobacco. Phyto- phosphite on tomato and pepper plants and on in vitro. Phytopathology 81:1541-1546. pathology 68:1760-1765. susceptibility of pepper to Phytophthora root 27. Hord, M. J., and Ristaino, J. B. 1992. Effect 33. Kim, K. D., Nemec, S., and Musson, G. 1997. and crown rot in hydroponic culture. Plant of the matric component of soil water poten- Effects of composts and soil amendments on Dis. 82:1165-1170. tial on infection of pepper seedlings in soil in- soil microflora and Phytophthora root and 22. Garrison, S. A. 1999. 1999 Commercial fested with oospores of Phytophthora capsici. crown rot of bell pepper. Crop Prot. 16:165- vegetable production recommendations - New Phytopathology 82:792-798. 172. Jersey. Ext. Bull. E0010. Rutgers Cooperative 28. Hwang, B. K., DeCock, A. W. A. M., 34. Kim, Y. J., Hwang, B. K., and Park, K. W. Extension. NJAES. New Brunswick, NJ. Bahnweg, G., Prell, H., and Heitefuss, R. 1989. Expression of age-related resistance in pepper plants infected with Phytophthora capsici. Plant Dis. 73:745-747. 35. Kreutzer, W. A., Bodine, E. W., and Durrell, L. W. 1940. Cucurbit disease and rot of tomato fruit caused by Phytophthora capsici. Phytopathology 30:972-976. 36. Lamour, K. H., and Hausbeck, M. K. 1999. Characteristics of P. capsici populations in Michigan. Phytopathology 89:S43. 37. Larkin, R. P, Gumpertz, M. L., and Ristaino, J. B. 1995. Geostatistical analysis of Phy- tophthora epidemics in commercial bell pepper fields. Phytopathology 84:191-203. 38. Larkin, R. P., Ristaino, J. B., and Campbell, C. L. 1995. Detection and quantification of Phytophthora capsici in soil. Phytopathology 85:1057-1063. 39. Lee, S. B., White, T. J., and Taylor, J. W. 1993. Detection of Phytophthora species by oligonucleotide hybridization to amplified ribosomal DNA spacers. Phytopathology 83:177-181. 40. Leonian, L. H. 1922. Stem and fruit blight of pepper caused by Phytophthora capsici species nov. Phytopathology 12:401-408. 41. Masago, H., Yoshikawa, M., Fukada, M., and Jean Beagle Ristaino Stephen A. Johnston Nakanishi, N. 1977. Selective inhibition of Pythium spp. on a medium for direct isolation Dr. Ristaino is a professor in the De- Dr. Johnston is an extension special- of Phytophthora spp. from soils and plants. partment of Plant Pathology at North ist in plant pathology with Rutgers Phytopathology 67:425-428. Carolina State University. She re- Cooperative Extension located at the 42. Matheron, M. E., and Matejka, J. C. 1988. In ceived a B.S. in biological sciences Rutgers Agricultural Research & Ex- vitro activity of sodium tetrathiocarbonate on with a botany emphasis and an M.S. tension Center in Bridgeton, New sporulation and growth of six Phytophthora in plant pathology from the University Jersey. He received his B.S. in bot- species. Phytopathology 78:1234-1237. of Maryland. She worked in the Soil- any and his M.S. in plant pathology at 43. Matheron, M. E., and Matejka, J. C. 1995. borne Diseases Laboratory, USDA, North Carolina State University, and Comparative activities of sodium tetrathiocarbonate and metalaxyl on Phytophthora Beltsville, from 1982 to 1984. She his Ph.D. in plant pathology at Rut- capsici and root and crown rot on chile pep- received her Ph.D. in plant pathology gers University in New Brunswick, per. Plant Dis. 79:56-59. from the University of California in New Jersey. He is responsible for 44. Mathis, W. L., Williams-Woodward, J., and Davis in 1987 and joined the faculty extension activities and applied re- Csinos, A. S. 1999. Insensitivity of P. capsici at North Carolina State University search on disease management of to mefenoxam in Georgia. Phytopatholoy that same year. Her research has vegetable crops in New Jersey. 89:S49. focused primarily on the population 45. Miller, S. A., Bhat, R. G., and Schmitthenner, biology, ecology, and epidemiology of A. F. 1994. Detection of Phytophthora capsici Phytophthora diseases on pepper, in pepper and cucurbit crops in Ohio with two potato, and tomato, and Southern blight commercial immunoassay kits. Plant Dis. 78:1042-1046. caused by Sclerotium rolfsii on vege- 46. Miller, S. A., Madden, L. V., and Schmitthen- table crops. A major goal of her work ner, A. F. 1997. Distribution of Phytophthora is to develop ecologically based spp. in field soils determined by immunoas- disease management practices that say. Phytopathology 87:101-107. reduce our reliance on pesticides. She 47. Morton, H. V., and Urech, P. A. 1988. History teaches a graduate course on Agri- of the development of resistance to phenyla- culture, Ethics, and the Environment mide fungicides. Pages 59-60 in: C. E. Delp, and was an AAAS Environmental ed. Fungicide Resistance in North America. Science Fellow at the EPA in 1996. American Phytopathological Society, St. Paul, MN. 48. Neher, D., and Duniway, J. M. 1992. Disper-

1088 Plant Disease / Vol. 83 No. 12 sal of Phytophthora parasitica in tomato 58. Reifschneider, F. J. B., Boiteux, L. S., Della tophthora capsici on bell pepper. J. Agric. fields by furrow irrigation. Plant Dis. 76:582- Vecchia, P. T., Poulos, J. M., and Kuroda, N. Sci. Camb. 100:7-11. 586. 1992. Inheritance of adult plant resistance to 68. Schlub, R. L., and Johnston, S. A. 1982. 49. Ortega, R. G., Espanol, C. P., and Zueco, J. C. Phytophthora capsici in pepper. Euphytica Control of Phytophthora on pepper using 1992. Genetic relationship among four pepper 62:45-49. captafol and metalaxyl. Phil. Agric. 65:215- genotypes resistant to Phytophthora capsici. 59. Ristaino, J. B. 1990. Intraspecific variation 219. Plant Breed. 108:118-125. among isolates of Phytophthora capsici from 69. Stamps, D. J., Waterhouse, G. M., Newhook, 50. Oudemans, P., and Coffey, M. D. 1991. A pepper and cucurbit fields in North Carolina. F. J., and Hall, G. S. 1990. Revised Tabular revised systematics of twelve papillate Phy- Phytopathology 80:1253-1259. Key to the Species of Phytophthora. CAB In- tophthora species based on isozyme analysis. 60. Ristaino, J. B. 1991. Influence of rainfall, drip ternational Mycological Institute, Mycol. Pap. Mycol. Res. 95:1025-1046. irrigation, and inoculum density on the devel- 162. 51. Papavizas, G. C., and Bowers, J. H. 1981. opment of Phytophthora root and crown rot 70. Stanghellini, M. E., Kim, D. H., Rasmussen, Comparative fungitoxicity of captafol and epidemics and yield in bell pepper. Phytopa- S. L., and Rorabaugh, P. A. 1996. Control of metalaxyl to Phytophthora capsici. Phytopa- thology 81:922-929. Phytophthora root rot of peppers caused by thology 71:123-128. 61. Ristaino, J. B., Hord, M. J., and Gumpertz, M. Phytophthora capsici with a nonionic surfac- 52. Papavizas, G. C., Bowers, J. H., and Johnston, L. 1992. Population densities of Phytophthora tant. Plant Dis. 80:1113-1116. S. A. 1981. Selective isolation of Phytoph- capsici in field soils in relation to drip irriga- 71. Stanghellini, M. E., and Miller, R. M. 1997. thora capsici from soils. Phytopathology tion, rainfall, and disease incidence. Plant Dis. Biosurfactants: Their identity and potential 71:129-133. 76:1017-1024. efficacy in the biological control of zoosporic 53. Parra, G., and Ristaino, J. 1998. Insensitivity 62. Ristaino, J. B., Larkin, R. P., and Campbell, plant pathogens. Plant Dis. 81:4-12. to Ridomil Gold (mefenoxam) found among C. L. 1993. Spatial and temporal dynamics of 72. Sujkowski, L. S., Ristaino, J. B., Parra, G. R., field isolates of Phytophthora capsici causing Phytophthora epidemics in commercial bell and Gumpertz, M. L. 1996. Effect of dispersal Phytophthora blight on bell pepper in North pepper fields. Phytopathology 83:1312-1320. of inoculum of Phytophthora capsici in soil Carolina and New Jersey. Plant Dis. 82:711. 63. Ristaino, J. B., Larkin, R. P., and Campbell, on temporal dynamics of disease. Phytopa- 54. Pennisi, A. M., Agosteo, G. E., Cacciola, S. C. L. 1994. Spatial dynamics of disease thology 86:S108. O., Pane, A., and Faedda, R. 1998. Insensitiv- symptom expression during Phytophthora 73. Weber, G. F. 1932. Blight of peppers in Flor- ity to metalaxyl among isolates of Phytoph- epidemics on bell pepper. Phytopathology ida caused by Phytophthora capsici. Phyto- thora capsici causing root and crown rot of 84:1015-1024. pathology 22:775-780. pepper in southern Italy. Plant Dis. 82:1283. 64. Ristaino, J. B., Madritch, M., Trout, C. L., 74. White, T. J., Bruns, T., Lee, S., and Taylor, J. 55. Polizzi, G., Agosteo, G. E., and Cartia, G. and Parra, G. 1998. PCR amplification of ri- 1990. Amplification and direct sequencing of 1994. Soil solarization for the control of bosomal DNA for species identification in the fungal ribosomal RNA genes for phylogenet- Phytophthora capsici on pepper. Acta Hortic. plant pathogen genus Phytophthora. Appl. ics. Pages 315-322 in: PCR Protocols: A 366:331-338. Environ. Microbiol. 68:948-954. Guide to Methods and Applications. M. A. 56. Ramirez, V. J., and Cova, S. R. 1980. Su- 65. Ristaino, J. B., Parra, G., and Campbell, C. L. Innis, D. H. Gelfand, J. J. Sninshy, and T. J. pervivencia de Phytophthora capsici Leonian, 1997. Suppression of Phytophthora blight in White, eds. Academic Press, New York. agente causal de la marchitez del chile. Agro- bell pepper by a no-till wheat cover crop. 75. Yucel, S. 1995. A study on soil solarization ciencia 39:9-18. Phytopathology 87:242-249. and combined with fumigant application to 57. Ramsey, G. B., Smith, M. A., Wright, W. R., 66. Sansome, E. 1976. Gametangial meiosis in control Phytophthora crown blight and Beraha, L. 1960. Phytophthora rot of Phytophthora capsici. Can. J. Bot. 54:1535- (Phytophthora capsici Leonian) on peppers in water melons on the market. Plant Dis. Rep. 1545. the East Mediterranean region of Turkey. 44:692-694. 67. Schlub, R. L. 1983. Epidemiology of Phy- Crop Prot. 14:653-655.

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