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, zuc- chini; H, immature pumpkin; I, spaghetti squash; J, bell pepper; K and L, banana pepper; M and N, tomato; and O, snap bean. Plant Disease / December 2004 1293 surface of the fruit 2 to 3 days later (Fig. 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.