Part I. Infectious Diseases Diseases Caused by Fungi and Oomycetes The plant-pathogenic fungi and oomycetes discussed in this section are also listed in the appendix. Readers will note that in both the appendix and the text, alternative names of fungi are identified exclusively as “synonyms,” rather than as specific life cycle stages (e.g., “anamorph,” “teleomorph”). This practice reflects the policy for naming fungi issued in 2011 by the International Botanical Congress: namely, that the use of multiple names for the same fungus be abandoned. (Readers interested in learning more about this policy are referred to the 2011 article by Hawksworth [see Selected Reference].) Going forward, accommodating this new policy may mean that the most familiar names of some fungi will change. Changes to the names of fungi, as well as other updates to taxonomy and nomenclature, will be made in the Common Names of Plant Diseases list for lettuce, which is available on the website of The American Phytopathological Society.
stage has not been identified. Mycelia are composed of slender, hyaline, septate hyphae that grow inter-and intracellularly within the host tissue. Mycelia give rise to acervuli that consist of densely packed, upright conidiophores 20–60 µm tall. Conidia are typically two celled, slightly curved, and hyaline and may contain one or two large oil droplets. Conidia are usually constricted at the septa and measure 4 × 17 µm. Immature conidia may lack septa. Microsclerotia, which are 60–100 µm in diameter, may form within infected tissue and serve as a primary source of inoculum.
Selected Reference Hawksworth, D. L. 2011. A new dawn for the naming of fungi: Impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. IMA Fungus 2:155-162.
Anthracnose Anthracnose (also referred to as “shot hole,” “ring spot,” and “rust”) occurs on lettuce worldwide. Losses from anthracnose are considerable in some areas, especially during periods of cool and moist conditions. In Australia, entire fields have been lost to this disease. Anthracnose affects most commercial varieties of lettuce, as well as wild lettuce, endive, and escarole.
Fig. 9. Small, tan, water-soaked lesions on the outer foliage of crisphead lettuce, symptomatic of anthracnose (Microdochium panattonianum). (Courtesy S. T. Koike—© APS)
Symptoms The first symptom of anthracnose is the appearance of small, tan, water-soaked spots on the outermost foliage. These lesions may later expand to 2–3 mm in diameter and become straw colored and circular, unless constricted by veins (Fig. 9). As lesions mature, their necrotic centers fall out, giving the disease its characteristic shot-hole appearance. Infection is usually most prevalent along the midrib on the lower leaf surface. Lesions directly on the midrib become elongated (2.0–2.5 × 4–5 mm) along the leaf axis and are dark brown and sunken, but the tissue does not fall through (Fig. 10). A severe infection may result in poor head formation and require excessive trimming at harvest. Damaged tissue is invaded by secondary organisms—particularly soft rot bacteria, which can rapidly decay an entire head.
Causal Organism The causal agent of lettuce anthracnose is Microdochium panattonianum (syn. Marssonina panattoniana). The sexual
Fig. 10. Symptoms of anthracnose (Microdochium panattoni anum) on midribs of crisphead lettuce. (Courtesy S. T. Koike— © APS)
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Disease Cycle and Epidemiology In the absence of lettuce, the pathogen survives in infested debris and as microsclerotia in the soil. Upon germination, microsclerotia produce hyphae and/or conidiophores capable of spore production. Free moisture from dew, rain, or overhead irrigation is required for conidia production, germination, and infection. The fungus may penetrate directly through the leaf epidermis or enter through stomatal openings. Under favorable temperatures, periods of leaf wetness as short as 4 h may be suitable for infection, although longer durations are much more conducive. Splashing water is the most important method of dissemination, but conidia may also be spread by mechanical means when the foliage is wet. Anthracnose is favored by cool, wet conditions because of its water requirement. Maximum disease development occurs at 20°C. The host range for the pathogen is confined largely to species of the genus Lactuca, although endive has also been reported as a host. The possibility of infected seed serving as an inoculum source for lettuce anthracnose has generally been discounted. Host plant resistance has been reported, along with at least five pathogenic variants of the pathogen.
Management Methods for managing anthracnose include crop rotation, plowing to bury debris and microsclerotia, and controlling collateral hosts, such as wild lettuce. These measures serve to reduce the level of primary inoculum in the field. Cultural practices should be designed to minimize leaf wetness and to avoid physical contact with the plant when the canopy is wet. Where conditions are frequently favorable and disease pressure is severe, fungicide applications may be economically justified. Strobilurin fungicides and phosphorous acid compounds were shown to be most efficacious in an Australian trial. Breeding for anthracnose resistance has not generally been a priority. However, genetic resistance has been identified among commercially available cultivars and may offer management potential. Selected References Brandes, E. W. 1918. Anthracnose of lettuce caused by Marssonina panattoniana. J. Agric. Res. 13:261-280. Couch, H. B., and Grogan, R. G. 1955. Etiology of lettuce anthracnose and host range of the pathogen. Phytopathology 45:375-380. Galea, V. J., and Price, T. V. 1988. Survival of the lettuce anthracnose fungus (Microdochium panattonianum) in Victoria. Plant Pathol. 37:54-63. Galea, V. J., Price, T. V., and Sutton, B. C. 1986. Taxonomy and biology of the lettuce anthracnose fungus. Trans. Br. Mycol. Soc. 86:619-628. Ochoa, O., Delp, B., and Michelmore, R. W. 1987. Resistance in Lactucae spp. to Microdochium panattonianum (lettuce anthracnose). Euphytica 36:609-614. Patterson, C. L., and Grogan, R. G. 1991. Role of microsclerotia as primary inoculum of Microdochium panattonianum, incitant of lettuce anthracnose. Plant Dis. 75:134-138. Patterson, C. L., Grogan, R. G., and Campbell, R. N. 1986. Economically important diseases of lettuce. Plant Dis. 70:982-987. Rogers, G., and Kimpton, T. 2012. Developing a Strategy to Control Anthracnose in Lettuce. Rep. no. VG10123. Horticulture Australia Limited, Sydney, New South Wales. Wicks, T. J., Hall, B., and Pezzaniti, P. 1994. Fungicidal control of anthracnose (Microdochium panattonianum) on lettuce. Aust. J. Exp. Agric. 34:277-283.
tributed on lettuce. When it occurs, plants can be significantly stunted because of extensive damage to small feeder roots.
Symptoms Affected lettuce seedlings can be stunted and delayed in development but otherwise appear healthy. If black root rot is severe early in the crop cycle, infected lettuce plants will remain small, the field will appear uneven (Fig. 11), and plants will not reach marketable size (Fig. 12). Stunting is usually most evident from the rosette stage through plant maturity. In advanced cases, the lower leaves of the plant may turn yellow or even brown. Root symptoms of black root rot include the formation of numerous small (4–8 mm long), dark-brown to black bands and lesions on small feeder and larger secondary roots (Fig. 13). As the disease progresses, the lesions coalesce and cause significant damage to the root system. The lesions do not penetrate into the root vascular tissue. Black root rot affects both crisphead and leaf/romaine cultivars.
Causal Organism Black root rot is caused by the soilborne fungus Thielaviopsis basicola (syn. Chalara elegans). This pathogen is widespread throughout the world and has a broad host range. On most agar media, colonies of T. basicola are gray with a velvety texture. Endoconidia are hyaline, thin walled, single celled, and cylindrical, and they measure 3–6 × 7–17 µm. Conidia form within slender phialides and are then pushed out from the tips of the conidiophores in fragile chains that readily break apart. Because these spores are catenulate, the ends of the endoconidia are truncated. T. basicola also forms aleurioconidia that are dark brown, thick walled, single celled, and subrectangular. Aleurioconidia are 5–8 × 10–16 µm and form in stacks or chains of five to eight or more spores; these stacks tend to remain intact until the spores reach maturity, at which point they break apart. Differences in isolates of T. basicola may exist. When lettuce isolates were inoculated onto lettuce and various other crops known to be hosts, T. basicola was very aggressive and caused significant damage to lettuce and bean; however, inoculation did not result in disease on cotton or other crops. Thus, T. basicola isolates from lettuce may have a host preference for lettuce and a few other plants.
Disease Cycle and Epidemiology Aleurioconidia enable T. basicola to survive in dry soil for extended periods (more than 1 year). Under moist conditions, however, survival is reduced to 7 months or less. Optimum temperatures for infection and disease development range
(Prepared by R. N. Raid)
Black Root Rot Black root rot of lettuce has been reported in Australia and the United States (California) but otherwise is not widely dis26
Fig. 11. Uneven growth of romaine lettuce plants, caused by black root rot (Thielaviopsis basicola). (Courtesy S. T. Koike—© APS)
from 15 to 20°C. Inoculum is spread by the movement of soil via tillage operations and flooding. Repeated cropping of lettuce and other susceptible crops likely increases inoculum levels in the soil. T. basicola has been recovered from peat- based rooting media, indicating that it may be a source of primary inoculum if lettuce transplants are used. Shore fly (Scatella stagnalis) adults and larvae can be internally contaminated with T. basicola aleurioconidia and thereby serve as possible vectors of the pathogen among transplants in a greenhouse.
Management Black root rot of lettuce is a minor problem, and management in the field is not warranted. For other crops, black root rot is managed through a combination of resistant cultivars, crop rotation to nonhosts, sanitation practices (to prevent spreading contaminated soil/mud to uninfested fields), and application of fungicides to seedlings. Lettuce cultivars vary in susceptibility to T. basicola.
Selected References Ellis, M. B., and Subramanian, C. V. 1968. Thielaviopsis basicola. Descriptions of Pathogenic Fungi and Bacteria, no. 170. Commonwealth Mycological Institute, Kew, Surrey, UK. Graham, J. H., and Timmer, N. H. 1991. Peat-based media as a source of Thielaviopsis basicola causing black root rot on citrus seedlings. Plant Dis. 75:1246-1249. Koike, S. T. 2008. Black root rot caused by Thielaviopsis basicola on lettuce in California. Plant Dis. 92:1368. O’Brien, R. G., and Davis, R. D. 1994. Lettuce black root rot—A disease caused by Chalara elegans. Australas. Plant Path. 23:106-111. Stanghellini, M. E., Rasmussen, S. L., and Kim, D. H. 1999. Aerial transmission of Thielaviopsis basicola, a pathogen of corn-salad, by adult shore flies. Phytopathology 89:476-479. Tabachnik, M., DeVay, J. E., Garber, R. H., and Wakeman, R. J. 1979. Influence of soil inoculum concentrations on host range and disease reactions caused by isolates of Thielaviopsis basicola and comparison of soil assay methods. Phytopathology 69:974-977.
(Prepared by S. T. Koike and R. F. Smith)
Black Rot
Fig. 12. Reduced size of romaine lettuce plants infected with Thielaviopsis basicola, causal agent of black root rot. (Courtesy S. T. Koike—© APS)
The only report of black rot on hydroponically grown lettuce came from Brazil in 2006. Since then, reports from Brazil and other lettuce-producing countries have been unavailable; thus, the impact of black rot on lettuce production is uncertain. The symptoms of black rot are fairly nondescript; they include severe stunting of plants and the entire root system turning black and becoming shriveled and rotten. White mycelium and partially sunken perithecia appear in symptomatic hypocotyl and roots. The pathogen, Ceratocystis fimbriata, produces dark-brown perithecia that have globose bases of 140–210 µm and are ornamented with hyphal hairs. The neck of a perithecium is erect, 650–890 µm long, and ornamented with divergent ostiolar hyphae. At the base of the neck, the width is 23–33 µm, and at the apex, 15–18 µm. Acospores are hyaline and hat shaped, measure 2.6–4.7 × 7.3–7.8 µm, and are surrounded by a gelatinous matrix. Selected Reference Halfeld-Vieira, B. A., and Nechet, K. L. 2006. Black rot in lettuce: A new disease caused by Ceratocystis fimbriata in hydroponic culture in Brazil. Plant Pathol. 55:300.
(Prepared by K. V. Subbarao)
Bottom Rot
Fig. 13. Banded roots and reduced-sized secondary roots caused by black root rot (Thielaviopsis basicola). (Courtesy S. T. Koike— © APS)
Lettuce bottom rot was first described in Massachusetts (United States) glasshouses in 1900, and the first field occurrence was reported in Florida (United States) in 1905. The disease is now found wherever lettuce is grown. Although the fungal pathogen can cause damping-off of seedlings, bottom rot is most commonly associated with plants at or near maturity. Favored by warm, wet conditions, the disease can cause crop losses as high as 70% (Fig. 14). Under severe disease pressure, entire lettuce heads are unmarketable, but even under less favorable conditions, the extra trimming required to remove affected leaves reduces head weight and size, strongly influencing packaging and marketability. Bottom rot occurs on all types of lettuce, as well as on escarole and endive. Other lettuce diseases often confused with bottom rot are gray mold and lettuce drop. 27
Symptoms Lesions typically appear first on lower leaves in direct contact with the soil. Symptoms of initial infection include small, rust- colored to chocolate-brown spots primarily on the undersides of leaf midribs (Fig. 15). While these symptoms may be evident as early as 4 weeks after direct seeding, advanced symptoms of the disease are usually not apparent until heading (Fig. 16). Under favorable temperature and moisture conditions, bottom rot lesions are capable of rapid expansion, quickly rotting the midribs and leaf blades (Fig. 17). Amber-colored droplets sometimes ooze from the lesions on infected midribs. The stem, which is somewhat more resistant to colonization by the patho-
gen, is the last part of the head to decay. Wilting of the outer wrapper leaves is one of the first symptoms observed when infected plants are viewed from above. Decaying heads are at first slimy and brown but become almost black as they collapse and dry. A tan to brown, weblike mycelium of the causal fungus is frequently observed without magnification within infected head tissue and on the soil immediately beneath the head (Fig. 18). Irregularly shaped, cinnamon-brown to dark-brown sclerotia are produced during later stages of the disease (Fig. 19). The damage caused by infection also provides entry points for secondary rot organisms, particularly soft rot bacteria. These organisms may be responsible for the rapid decay observed in later stages of bottom rot.
Causal Organism Bottom rot is caused by the soilborne fungus Rhizoctonia solani (syn. Thanatephorus cucumeris). R. solani hyphae are white to brown and septate. A hypha typically branches at a near-right angle, and a crosswall develops just after branching. Branches are conspicuously constricted (Fig. 20). Asexual fruit-
Fig. 14. Near-mature crisphead lettuce plants with bottom rot, caused by Rhizoctonia solani. (Courtesy S. Glucksman—© APS)
Fig. 16. Later symptoms of bottom rot (Rhizoctonia solani) include sunken lesions on lettuce midribs. (Courtesy S. Glucksman— © APS)
Fig. 15. Early symptoms of bottom rot (Rhi zoctonia solani) include rust-colored lesions along lettuce midribs. (Courtesy R. N. Raid— © APS)
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Fig. 17. Rotted midribs and leaf blades are advanced symptoms of bottom rot, caused by Rhizoctonia solani. (Cour tesy R. N. Raid—© APS)
ing structures and spores are lacking. Small, tan to dark-brown sclerotia form among connecting mycelial threads. Basidia of the perfect state measure 8–11 × 18–23 µm. Basidiospores are hyaline and single celled (4–7 × 7–13 µm). R. solani exhibits extensive biological specialization. Field isolates capable of hyphal fusion (anastomosis) are assigned to the same anastomosis group (AG). Anastomosis occurs between isolates in the same group but not between isolates in different groups. R. solani AG 1-1B was most frequently isolated from infected lettuce in Germany, along with AG 1-1C and AG 2-1. AG 1-1B isolates also caused strong symptom development on spinach, broccoli, radish, kohlrabi (Brassica oleracea var. gongylodes), and millet (Pennisetum glaucum) but little symptom development on maize, tomato, and onion.
Disease Cycle and Epidemiology Fig. 18. Advanced stage of bottom rot on lettuce, indicated by a light-brown mycelial web of the causal agent, Rhizoctonia solani. (Courtesy R. N. Raid—© APS)
R. solani is a common soil inhabitant. As a capable soil saprophyte, the fungus survives between crops as sclerotia and mycelium associated with infected crop debris. It is disseminated and carried long distances (especially as sclerotia) in any manner that moves soil. Basidiospores, which are disseminated via wind and water, are also capable of long-distance spread. Under favorable moisture and temperature conditions, sclerotia germinate and produce mycelial growth capable of extending 7–10 cm to reach a food source. The pathogen is capable of direct penetration, entering the plant through healthy or wounded tissue or through stomata. Colonization is both inter-and intracellular. Warm, moist conditions are most conducive to the development of brown rot. Optimal mycelial growth occurs between 20 and 30°C (optimum 25°C) and over a broad range of pH (from 5 to 8). The interval from infection to initial symptom development may be as short as 36–48 h. Minimum and maximum temperatures for mycelial growth are 5 and 36°C, respectively. The incubation period lengthens considerably as the temperature varies from the optimal range. R. solani isolates vary significantly in pathogenicity, virulence, and survival, and it is difficult to make generalized statements. However, the occurrence of bottom rot is heavily influenced by the previous crop, the length of time between crops, the virulence of the particular isolates present, and the ability of those isolates to survive in the soil.
Management Fig. 19. Sclerotia of Rhizoctonia solani, the fungus that causes bottom rot, beginning to form on infected lettuce tissue. (Courtesy R. N. Raid—© APS)
Optimum management of bottom rot is achieved by using various cultural practices in combination with fungicide applications. Plowing instead of disking before planting effectively buries sclerotia, and the viability of these survival structures appears to lessen as the depth of incorporation increases. Crop rotation also reduces inoculum potential. Growing lettuce on high beds improves aeration and minimizes foliar contact with the ground—the point at which infection typically occurs. Avoiding irrigation close to harvest and planting lettuce cultivars with erect plant architecture may reduce losses. Good drainage and weed control are also important. Several fungicides registered in the early 2000s for use on lettuce have greatly improved the prospects for managing bottom rot. Placement and timing are extremely important. Biological controls have shown promise, but season-long, commercially acceptable levels of control have not been achieved in the field. Selected References
Fig. 20. Hyphae of Rhizoctonia solani. Note constriction of the hyphae and septation near branching. (Courtesy R. N. Raid— © APS)
Clark, W. S., and McPherson, G. M. 1981. The use of iprodione for control of Rhizoctonia bottom rot of lettuce. Proc. Brighton Crop Prot. Conf. 2:475-479. Grosch, R., and Kofoet, A. 2003. Influence of temperature, pH, and inoculum density on bottom rot of lettuce caused by Rhizoctonia solani. J. Plant Dis. Prot. 110:366-378.
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Grosch, R., Schneider, J. H. M., and Kofoet, A. 2003. Characterization of Rhizoctonia solani anastomosis groups causing bottom rot in field-grown lettuce in Germany. Eur. J. Plant Path. 110:53-62. Grosch, R., Koch, T., and Kofoet, A. 2004. Control of bottom rot on lettuce caused by Rhizoctonia solani with commercial biocontrol agents and a novel fungicide. J. Plant Dis. Prot. 111:572-582. Heo, K. R., Lee, K. Y., Lee, S. H., Jung, S. J., Lee, S. W., and Moon, B. J. 2008. Control of crisphead lettuce damping-off and bottom rot by seed coating with alginate and Pseudomonas aeruginosa LY-11. Plant Pathol. J. 24:67-73. Herr, L. J. 1992. Characteristics of Rhizoctonia isolates associated with bottom rot of lettuce in organic soils in Ohio. Phytopathology 82:1046-1050. Herr, L. J. 1993. Host sources, virulence and overwinter survival of Rhizoctonia solani anastomosis groups isolated from field lettuce with bottom rot symptoms. Crop Prot. 12:521-526. Koike, S., and Martin, F. 2005. Evaluation of fungicides for controlling bottom rot of iceberg lettuce. Fung. Nemat. Tests 60:V150. Mahr, S. E. R., Stevenson, W. R., and Sequeira, L. 1986. Control of bottom rot of head lettuce with iprodione. Plant Dis. 70:506-509. Pieczarka, D. J., and Lorbeer, J. W. 1974. Control of bottom rot of lettuce by ridging and fungicide application. Plant Dis. Rep. 58:837-840. Pieczarka, D. J., and Lorbeer, J. W. 1975. Microorganisms associated with bottom rot of lettuce grown on organic soil in New York State. Phytopathology 65:16-21. Stone, G. E., and Smith, R. E. 1900. The rotting of greenhouse lettuce. Mass. Agric. Exp. Stn. Bull. 69. Townsend, G. R. 1934. Bottom rot of lettuce. N.Y. (Cornell) Agric. Exp. Stn. Mem. 158. Weber, G. F., and Foster, A. C. 1928. Diseases of lettuce, romaine, escarole, and endive. Fla. Agric. Exp. Stn. Bull. 195.
but quickly acquire pigmentation. In culture, mature mycelium generally ranges from dark green to dark brown in color. Conidiophores are amphigenous, fasciculate, olivaceous brown, unbranched, and septate; they bear conidia on newly developed tips. Conidial scars at the points of conidial attachment are large and conspicuous. Conidia are hyaline and cylindrical to obclavate, with an obconically truncate base and a tapering, obtuse apex. They range from 11 to 170 µm in length and have basal and apical widths that average 7.5 and 3.8 µm, respectively. A conidium generally has from one to 18 septa but can have as many as 28. Although germ tubes may rise from any or all cells, the basal cell usually germinates first, followed by the apical cell. No sexual stage has been reported.
Disease Cycle and Epidemiology Spread of Cercospora leaf spot in the field appears to occur entirely by means of conidia and is heavily dependent on relatively long periods of leaf wetness. The pathogen survives between cropping seasons on plant material in the field and in association with wild lettuce and closely related hosts. Conidial germination occurs only in the presence of free moisture or under nearly saturated atmospheric conditions.
(Prepared by R. N. Raid)
Cercospora Leaf Spot Cercospora leaf spot of lettuce is found in many parts of the world but is rarely destructive in the field. First reported in 1929, it is most common in the tropics and subtropics. Reports of its economic significance are varied. For example, it is not considered an important disease in China, but it is responsible for major crop losses in the Ivory Coast. In the United States, Cercospora leaf spot has been reported in Florida, Illinois, Indiana, Texas, Virginia, and Wisconsin. It can affect both cultivated and wild lettuce, and since 2000, it has been reported as a major pathogen in glasshouse lettuce production, where warm temperatures and high humidity levels favor spore production and infection by the pathogen.
Fig. 21. Chlorotic and necrotic lesions on lettuce caused by Cercospora lactucae-sativae, the causal agent of Cercospora leaf spot. (Courtesy S. Glucksman—© APS)
Symptoms Infection normally appears first on older, lower leaves. Lesions begin as minute, brown spots surrounded by chlorotic tissue and enlarge to become irregular or angular spots that vary in color from tan to brown (Fig. 21) and frequently have white spots in their centers (Fig. 22). Fully developed lesions are slightly sunken and necrotic. Cercospora leaf spot spreads progressively upward. Extensive areas of tissue may be killed when infections are numerous.
Causal Organisms A number of Cercospora spp. have been reported to cause Cercospora leaf spot. In Asia and the United States, Cercospora leaf spot is caused by C. lactucae-sativae (syn. C. longissima), and in Australia, it is caused by C. apii. Like other Cercospora spp., lettuce isolates may exhibit narrow host specificity. Young hyphae of C. lactucae-sativae are septate, slender, and 1.5–3.5 µm wide; they appear granular. More mature hyphae are thicker (3–6 µm) and more closely septate; they frequently contain conspicuous oil globules. Hyphae are initially hyaline 30
Fig. 22. White-centered lesions on lettuce, symptomatic of Cercospora leaf spot (Cer cospora lactucae-sativae). (Cour tesy R. N. Raid—© APS)
Reportedly, durations of leaf wetness in excess of 24 h are required for germ tube development and successful penetration of the leaf through the stomata. Appressoria are not necessary for penetration. Following initial penetration, germ tubes branch repeatedly, facilitating intercellular colonization of host tissues. At the optimal temperature of 25°C, susceptible tissues are rapidly colonized by the advancing hyphae, and symptoms may become apparent within 3 days after inoculation. At the suboptimal temperatures of 15, 20, and 30°C, incubation periods of 7, 5, and 5 days, respectively, have been reported. Subsequently, sporulation may begin in as few as 5 days at 25°C. Conidia are borne singly on conidiophores produced in fascicles on the leaf surface and become airborne during periods of low humidity when exposed to even the slightest turbulence. In addition to atmospheric transport, spores are scattered by rain and by irrigation splash. In culture, Czapek-Dox V-8 juice agar supports maximum radial growth and sporulation. The average optimum temperature for growth, sporulation, and production of the longest conidia on this particular medium is 25°C.
of injury is identified by a discolored, constricted area near the soil surface (Fig. 24). The magnitude of the dark discoloration is dependent on the age of the seedling and the duration of environmental conditions favorable for disease development. As the lettuce seedling continues to grow, root-tip necrosis may continue to develop, but the risk of plant death from postemergence damping-off rapidly decreases. Partially girdled plants, as well as those subject to continued root-tip necrosis, may be stunted to varying degrees, resulting in lettuce plantings with uneven growth and development.
Causal Organisms Pythium irregulare, P. myriotylum, P. sylvaticum, and P. ultimum can cause pre-and postemergence damping-off of lettuce, whereas P. dissotocum, P. uncinulatum, and P. violae incite root-tip necrosis and inhibition of lateral root formation. Rhizoctonia solani may also cause pre-emergence death of seedlings but usually causes necrosis of the stem at or near the soil surface, which is marked by a distinct margin between infected and healthy tissue.
Management Cultural practices for the management of Cercospora leaf spot include crop rotation, good drainage, and destruction of wild lettuce and other closely related hosts near the lettuce crop. In certain areas, the application of foliar fungicides may be justified for disease control. Selected References Liberato, J. R., and Stephens, P. M. 2006. Cercospora apii s. lat. on lettuce in Australia. Australas. Plant Path. 35:379-381. Raid, R. N., and Nagata, R. T. 2002. Evaluation of assorted foliar applications for control of Cercospora leaf spot on lettuce. Fung. Nemat. Tests 58:V120. Raid, R. N., and Nagata, R. T. 2002. Evaluation of fungicides for control of Cercospora leaf spot and downy mildew on lettuce. Fung. Nemat. Tests 58:V119. Savery, S. 1983. Epidemiology of Cercospora leaf spot of lettuce in Republic of Ivory Coast. Argon. Sci. Prod. Veg. Environ. 3:903-9 09. Suwan, N., Nuandee, N., Akimitsu, K., and Sarunya, N. 2012. Analysis of β-tubulin gene from carbendazim resistant isolates of Cercospora lactucae-sativae on lettuce in Thailand. J. Agric. Tech. 8:711-723. Szeto, M., and Bau, Y. S. 1975. Some notes on leaf spot (Cercospora longissima) disease of lettuce. Agric. Hong Kong 1:278-285. Toro, R. A. 1929. Plant disease notes from the Central Andes II. Phytopathology 19:969-974.
Fig. 23. Damping-off of lettuce seedlings caused by Pythium ulti mum. (Courtesy F. N. Martin and K. V. Subbarao—© APS)
(Prepared by R. N. Raid)
Damping-Off Damping-off of lettuce seedlings occurs wherever the crop is grown. The disease is expressed as seed decay, pre-or postemergence damping-off, and infection of roots or stems of young plants. Damping-off is favored by excessive soil moisture, compacted and poorly drained soils, and temperatures unfavorable for germination and lettuce growth.
Symptoms Lettuce may be attacked by damping- off pathogens and destroyed before seed germination, during emergence of the radicle, or before the hypocotyl has reached the soil surface. After seedling emergence, the hypocotyl may be penetrated near the soil surface, leading to plant collapse and death (Fig. 23). As the seedling grows, the damping-off pathogens can destroy only the outer layer of cells around the stem. This type
Fig. 24. Discolored, constricted root of a lettuce seedling infected by Rhizoctonia solani, a causal agent of damping-off. (Cour tesy S. T. Koike—© APS)
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Disease Cycle and Epidemiology Pythium spp. survive in soil as thick-walled oospores and as sporangia in some species. These spores are stimulated to germinate by nutrients such as those in seed and root exudates. After the primary infection, secondary infections may occur from zoospores released from sporangia. Zoospores are motile and swim short distances in films of water in soil or move greater distances in surface water. Pythium spp. have a broad host range and can also colonize fresh organic matter in soil. Damping-off caused by Pythium spp. usually occurs in fields with high organic matter and/or poor drainage—conditions that favor the growth and asexual reproduction of these pathogens. R. solani survives between crops as sclerotia or mycelium in soil and infested plant debris. It infects host cells directly by infection pegs produced from infection cushions or by individual hyphae that colonize the plant through natural openings and wounds. Damping-off incited by a Pythium or Rhizoctonia pathogen is favored by suboptimal growth of lettuce seedlings caused by factors such as unfavorable temperatures, excessive moisture, low light, and overfertilization.
Management Cultural and chemical measures can be effective means of managing damping-off. Planting high-quality seed under environmental conditions that favor rapid germination and seedling growth reduces the chance of infection. Excessive irrigation and compacted and poorly drained soils should be avoided. Seed and soil treatments with appropriate fungicides may prevent infection and protect seedlings when they are most susceptible to damping-off. Selected References Hine, R., Matheron, M., and Byrne, D. 1991. Diseases of lettuce in Arizona. Univ. Ariz. Coll. Agric. Publ. 191050. Sherf, A. F., and MacNab, A. A. 1986. Vegetable Diseases and Their Control. 2nd ed. John Wiley & Sons, New York. Stanghellini, M. E., and Kronland, W. C. 1986. Yield loss in hydroponically grown lettuce attributed to subclinical infection of feeder rootlets by Pythium dissotocum. Plant Dis. 70:1053-1056. Stanghellini, M. E., Kim, D. H., Rakocy, J., Gloger, K., and Klinton, H. 1998. First report of root rot of hydroponically grown lettuce caused by Pythium myriotylum in a commercial production facility. Plant Dis. 82:831.
sions are angular, variable in size, and often limited by large veins. Under optimal environmental conditions, a downy, white mat of asexual sporangiophores and sporangia forms 1–2 weeks after infection, primarily on the lower sides of leaves (Fig. 26). Older lesions often become necrotic or transparent because of the presence of secondary pathogens. Necrotic lesions with few or no sporangiophores also develop when oospores are produced as part of the sexual cycle. Lettuce is susceptible to downy mildew at all growth stages. Adult plants are rarely killed by the pathogen, but young seedlings are particularly susceptible; their cotyledons and primary leaves may be completely covered by sporangiophores, and they may die of severe infection. An early infection rarely leads to a systemic infection. Systemic symptoms on leaves include elongated discolored regions, which turn dark green to brown; sporulation is often not present until late in disease development. The central core of the stem and roots of a systemically infected plant is streaked dark brown to black (Fig. 27). Sporulation of the pathogen can be induced after incubating the infected tissue in a moist chamber in darkness.
Causal Organisms The primary causal agent of lettuce downy mildew is Bremia lactucae, an obligate parasite. The hyphae of the pathogen are coenocytic, filamentous, branched, and hyaline. The mycelium grows intercellularly and forms spherical or claviform haustoria in host cells. One to three sporangiophores arise from stomata. The sporangiophores are septate and colorless; they are inflated at the base, and the upper part branches several times. Branching of sporangiophores is acute and dichotomous (or rarely trichotomous). The tip of each branch expands into a disc or spherical shape, and three to six sterigmata are formed, each with one sporangium at the tip. Sporangia are colorless, spherical or oval, 12–31 µm long, and 11.0–27.5 µm wide. Two mating types, B1 and B2 , are needed for sexual reproduction of B. lactucae, although homothallic isolates have also been found. Both mating types have been frequently isolated in Europe and in New York State (United States). Isolates from
(Prepared by M. E. Matheron)
Downy Mildew Downy mildew is a major disease of lettuce in field and greenhouse production systems worldwide. Relatively cool temperatures and humid climatic conditions favor infection and spread of downy mildew. A downy mildew epidemic can be devastating during a cool and/or wet season. In a semiarid climate, such as in California (United States) and Australia, disease intensity and crop loss vary dramatically among seasons and weather conditions. Because lettuce is most commonly consumed fresh, a relatively low level of infection can downgrade the crop, cause significant trimming losses at harvest, and escalate postharvest decay during transit and storage. A high level of disease can render an entire planting unmarketable.
Symptoms The typical symptom of downy mildew is the development of local lesions on leaves, appearing first on lower leaves. These lesions are at first light green or slightly chlorotic, and they turn yellow or necrotic after the onset of sporulation (Fig. 25). Le32
Fig. 25. Advanced symptoms of downy mildew (Bremia lactucae) on (A) crisphead lettuce and (B) stem lettuce. (Courtesy A. H. C. van Bruggen and K. V. Subbarao—© APS)
cultivated lettuce in California are predominately the B2 mating type, whereas isolates carrying the B1 mating type are rare. Oospores have rarely been observed in nature but are abundantly produced in cotyledons or leaves artificially inoculated with the two mating types. When hyphae of opposite mating types meet, asexual sporulation is suppressed and gametangia (oogonium and antheridium) are produced at the point of contact. Meioses occur synchronously in the oogonium and antheridium, and haploid gametes are transferred from the antheridium to the oogonium for fertilization. Oospores are yellow brown, spherical (27–30 µm in diameter), and surrounded by a thick wall (Fig. 28). Germination of oospores has only occasionally been observed under controlled conditions, and the conditions required for oospore germination remain unclear. In addition to the mating types, pathotypes can also be distinguished by their virulence on lettuce genotypes with differential resistance genes (Dm). Studies have revealed multiple dominant genes for resistance (Dm genes) in lettuce plants matched by avirulence genes (Avr) in B. lactucae. High diversity of virulence phenotypes has been observed in Europe, California, and New York State. Prevalent races and pathotypes occur in Europe (BL1 to 32) and in California (CAI to VIII), respectively, that are widely distributed and persist from year to year. Another pathogen, Plasmopara lactucae-radicis, causes downy mildew exclusively on the roots of hydroponically grown lettuce. This pathogen has not been observed on field-grown lettuce.
Disease Cycle and Epidemiology
Secondary spread of B. lactucae occurs via airborne sporangia. Sporulation is affected significantly by temperature, relative humidity, and wind speed. Sporangia of B. lactucae are produced at night after a few hours of near-saturation humidity and low wind speed. Spore production is suppressed by light, and suppression increases with temperature. The most suppressive wavelength is from 400 to 450 nm. At 15°C, sporulation of B. lactucae follows a clear diurnal pattern independent of lightness or darkness at the onset of sporulation. Although spore production is optimal at 15°C, sporulation occurs over a wide temperature range (5–25°C). Spore production is abundant at relative humidity greater than or equal to 90% in still air, and spores are not formed at wind speeds greater than 0.5 ms–1. Sporangia are released in the morning; release is triggered by light initiation and a reduction in relative humidity. The density of B. lactucae sporangia in the air usually starts to increase at sunrise and peaks between 10:00 a.m. and noon. The longevity of sporangia is mainly affected by solar radiation (particularly in the ultraviolet B spectrum), ambient humidity, and temperature. Relatively short periods of exposure to sunlight or hot conditions can inactivate sporangia of the pathogen in arid climates. In more humid climates, sporangia can survive during the day and infect the next night. Germination of sporangia and penetration of plants by the pathogen requires a relatively low temperature and free water or relative humidity near saturation, and this process can take as little as 2–3 h under optimum temperatures (approximately 15°C). High temperatures within a few hours immediately after penetration (as measured in California) can significantly reduce successful infection. After that, the temperature mainly affects
Potential sources of initial inoculum of B. lactucae include lettuce seed, plant debris, wild Lactuca spp., and nearby lettuce fields. Lettuce seed may be an important source, based on findings from an early study that six out of 23,000 seeds were contaminated with the pathogen. However, the risk of infection from contaminated seed has not been determined. Both mating types are observed in many parts of the world, and oospores in lettuce debris may serve as primary inoculum (although oospores of the pathogen are apparently absent and have not been reported in California). However, B. lactucae has been found to change virulence phenotypes in response to the deployment of new Dm genes, and it is unclear how the pathogen survives crop-free periods in California. B. lactucae has been reported to infect plants in several genera in the Asteraceae. However, isolates of B. lactucae are host specific, and the wild lettuce species L. serriola (prickly lettuce) seldom supports growth of the pathogen. Although sporangia from nearby lettuce fields can be another source of inoculum, their long-distance dispersal is questionable, because they survive for less than 15 h after release because of damage produced by ultraviolet radiation and high temperatures in sunlight.
Fig. 27. Systemic infection caused by Bremia lactucae, the oomycete that causes downy mildew on lettuce. (Courtesy A. H. C. van Bruggen—© APS)
Fig. 26. Sporulating downy mildew lesions (Bremia lactucae) on crisphead lettuce. (Courtesy A. H. C. van Bruggen—© APS)
Fig. 28. Oospores of Bremia lactucae. (Courtesy A. H. C. van Bruggen—© APS)
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the length of the latent period. Under constant or slightly varying temperatures, downy mildew has a short latent period (4–7 days) at 20–22°C and a long latent period (24–34 days) at 6°C. However, under oscillating temperatures, the mean daily temperature has a relatively small effect on the latent period compared with constant temperatures with the same mean. Field studies in California have found that infection of lettuce by B. lactucae occurs primarily on days during which leaf wetness ends late in the morning. Thus, sporangia released around sunrise may infect that same morning if leaf wetness continues 3 h or longer. In commercial production, irrigation practices also have significant effects on epidemics of lettuce downy mildew. Usually, disease is more severe under sprinkler irrigation than under furrow irrigation, because longer leaf wetness duration, increased canopy air humidity, and/or enhanced dispersal of inoculum by splashing are usually associated with sprinkler irrigation. To some extent, these effects are also dependent on the time that irrigation is applied. Downy mildew is further reduced in surface and subsurface drip-irrigated fields compared with furrow- irrigated fields, probably because of the longer daily wet period and higher daytime humidity associated with furrow-irrigated fields. Additionally, growing five or more rows of lettuce on a wide (2-m) bed may create microclimatic conditions conducive to lettuce downy mildew because of the high canopy density and poor drainage associated with the wide bed configuration. However, in coastal California, mesoclimate effects on downy mildew development seem to outweigh microclimate effects as a result of differences in irrigation.
Management The easiest and cheapest way to manage downy mildew is to select and grow resistant cultivars with either pathotype-specific resistance genes (single dominant genes) or moderate levels of field resistance (probably multiple genes). Single-gene resistance has provided high levels of control for specific races, but the use of resistant cultivars often results in genetic changes in pathogen populations and the rise of strains of B. lactucae that overcome this resistance. Although considerable effort has been made to develop resistant cultivars, these cultivars have provided only transient control, because B. lactucae has overcome many of the downy mildew resistance genes employed. Interactions between cultivars of lettuce and isolates of B. lactucae are defined by numerous gene-for-gene relationships. Specificity is determined by dominant resistance genes (Dm) or resistance factors in the plants matched by dominant factors for avirulence (avr factors) in the pathogen. At least 27 major Dm genes or resistance (R) factors are known that provide resistance against specific isolates of B. lactucae in a gene-for-gene manner. Older cultivars often have moderate levels of quantitative resistance, which is presumably conferred by multiple resistance genes with minor effects. Classical plant breeding, combined with the identification of quantitative trait loci (QTLs), has been revived to produce modern cultivars with durable resistance. Several protective fungicides (e.g., mancozeb, maneb, azadirachtin, fenamidone, ametoctradin–dimethomorph mixture) and systemic fungicides (e.g., fosetyl-aluminum, mandipropamid, metalaxyl, oxathiapiprolin, propamocarb hydrochloride) are available for downy mildew control. Systemic fungicides can provide good control with fewer sprays per lettuce crop in most climates. The use of systemic fungicides is expensive for growers, however, and often induces the development of insensitive isolates of B. lactucae. B. lactucae is genetically highly variable, particularly when sexual recombination occurs. Isolates with insensitivity to the fungicide metalaxyl had become widespread by the 1990s. As a result, metalaxyl became ineffective, and it has rarely been applied since that time. Fosetyl- aluminum and maneb have been used since the failure of metalaxyl to control downy mildew. Subsequently, the majority of isolates of B. lactucae collected in California between 1997 34
and 2000 were found to have reduced sensitivity to fosetyl- aluminum. In humid climates, fungicides must be applied regularly to prevent or curb the development of epidemics. Research has demonstrated that some phosphites (i.e., potassium phosphite) have also proven to be somewhat effective in controlling downy mildew. While using these products exclusively is not recommended, using them as part of a comprehensive management program may increase efficacy and help avoid the development of fungicide resistance. In some climates, disease-warning systems can be used to minimize the number of fungicide applications and to optimize the timing of applications relative to infection periods. Several warning systems for lettuce downy mildew have been developed based primarily on the end of morning leaf wetness duration and temperature, and some systems also consider the night conditions for sporulation of B. lactucae. Applying fungicides based on the recommendations of these models, instead of a calendar-based schedule, can reduce the number of fungicide applications and achieve similar disease control. When lettuce is produced under irrigation, practices can be adjusted to reduce the risk of downy mildew development. Surface and subsurface drip irrigation produce a less conducive environment for downy mildew than furrow and sprinkler irrigation. If sprinkler irrigation is used, sprinklers should be operated in the afternoon to prevent extending the natural leaf wetness period that occurs in the morning. Other cultural practices focused on field hygiene may also help to control downy mildew—for example, maintaining a lettuce-free period, rotating crops, removing debris and sporulating plants, and destroying possible weed hosts. Selected References Brown, S., Koike, S. T., Ochoa, O. E., Laemmlen, F., and Michelmore, R. W. 2004. Insensitivity to the fungicide fosetyl-aluminum in California isolates of the lettuce downy mildew pathogen, Bremia lactucae. Plant Dis. 88:502-508. Cohen, Y., Rubin, E., and Gottlieb, D. 2008. Activity of carboxylic acid amide (CAA) fungicides against Bremia lactucae. Eur. J. Plant Pathol. 122:169-183. Crute, I. R. 1992. The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica 63:95-102. Crute, I. R., and Johnson, A. G. 1976. The genetic relationship between races of Bremia lactucae and cultivars of Lactuca sativa. Ann. Appl. Biol. 83:125-137. Fall, M. L., van der Heyden, H., Beaulieu, C., and Carisse, O. 2015. Bremia lactucae infection efficiency in lettuce is modulated by temperature and leaf wetness duration under Quebec field conditions. Plant Dis. 99:1010-1019. Hovius, M. H. Y., Carisse, O., Philion, V., and McDonald, M. R. 2007. Field evaluation of weather-based spray programs for the control of downy mildew of lettuce (Lactuca sativa), caused by Bremia lactucae, in Quebec and Ontario. Can. J. Plant Pathol. 29:9-17. Ilott, T. W., Hulbert, S. H., and Michelmore, R. W. 1989. Genetic analysis of the gene-for-gene interaction between lettuce (Lactuca sativa) and Bremia lactucae. Phytopathology 79:888-897. Judelson, H. S., and Michelmore, R. W. 1992. Temperature and genotype interactions in the expression of host resistance in lettuce downy mildew. Physiol. Molec. Plant Pathol. 40:233-245. Kushalappa, A. C. 2001. BREMCAST: Development of a system to forecast risk levels of downy mildew on lettuce (Bremia lactucae). Int. J. Pest Manag. 47:1-5. Lebeda, A., Petrzelová, I., and Maryška, Z.. 2008. Structure and variation in the wild-plant pathosystem: Lactuca serriola–Bremia lactucae. Eur. J. Plant Pathol. 122:127-146. Michelmore, R. W., and Wong, J. 2008. Classical and molecular genetics of Bremia lactucae, cause of lettuce downy mildew. Eur. J. Plant Pathol. 122:19. doi:10.1007/s10658-0 08-9305-2 Michelmore, R. W., Ochoa, O, and Wong, J. 2009. Bremia lactucae and lettuce downy mildew. Pages 241-262 in: Oomycete Genetics and Genomics: Diversity, Plant and Animal Interactions, and Toolbox. K. Lamour and S. Kamoun, eds. Wiley-Blackwell, New York.