Evaluation of Management Strategies for Clubroot Disease of Brassica Crops

Gideon Porth, Frank Mangan, Robert Wick, and Wesley Autio University of Massachusetts, Amherst, MA

Clubroot disease, caused by the pathogen brassicae, is the most devastating disease of Brassica crops worldwide. It is found throughout temperate climates and is especially significant in areas of intensive production of Brassica crops such as East Asia, Northern Europe, Australia, and North America. The disease can effect all types of cruciferous crops including vegetables (, , , , Chinese cabbage), oil crops (rape seed), fodder crops (swedes and fodder turnip), and ornamentals (stock and sweet alyssum), as well as weeds such as wild mustards. Disease occurs when the soil-borne club root pathogen invades the plant’s root system. The infected roots become swollen forming galls or “clubs” that interfere with the plant’s water and nutrient uptake. In mild cases wilting and stunting occurs, and in severe cases, the plant dies. Galls begin as small legions, often on lateral roots, and grow over time, often affecting the entire root system of the host (Figure 1).

Disease Management Many different strategies for managing clubroot have been researched and implemented since it was first reported by Woronin in 1878. One of the most documented treatments is raising the soil pH to 7.1- 7.2. This creates an unfavorable soil environment for the pathogen, most likely by disrupting the release of zoospores. It is unclear whether the suppressive effects of this treatment are Figure 1: Healthy roots of Chinese cabbage grown in disease free soil due solely to an increase in (left) and clubbed roots of mustard greens grown in clubroot infested pH, the associated increase soil (right). in soil calcium and magnesium, or some interaction between these three factors. It is only a partial solution; however, since given optimal soil moisture, temperature, and inoculum, severe clubbing will develop even in alkaline soils. Application of boron to the soil has also been used to manage clubroot for more than 60 years. Research has shown a significant decrease in disease by applications of borax at 20kg/ha. Fungicides have been used for many years to treat fields infested with P. brassicae. Many fungicides have given inconsistent management of clubroot, and some that have shown promise needed to be used at high rates that made them prohibitively expensive. For these reasons, no single fungicide has emerged as a truly effective and practical management tool. Pentachloronitrobenzene (PCNB) is currently the recommended fungicide for control of clubroot (New England Vegetable Management Guide, 2002). PCNB has shown somewhat inconsistent performance and may cause phytotoxicity in high concentrations. However, when combined with liming it can provide effective control. For cultural control options, crop rotations are the most frequently recommended management strategy. Plasmodiophora brassicae is an obligate parasite, unable to complete its life cycle in the absence of a host plant. For this reason, it is recommended that infested fields be rotated out of Brassica family crops for a minimum of 5-7 years. This strategy is limited for several reasons. The pathogen is capable of infecting some cruciferous weed hosts, thereby completing its life cycle and maintaining a population of resting spores within the field even in the absence of a Brassica crop. In addition, the resiliency of P. brassicae resting spores allows them to remain dormant in a field for many years (up to 10-20 years), meaning that in cases of severe infection, a field may need to be permanently rotated out of Brassica crops. For these reasons, crop rotation is only an effective management strategy when combined with other treatments or in situations where continuous, intensive production of Brassica crops is not a necessary part of the agricultural system. Another long-standing cultural control for clubroot is reducing soil moisture by increasing field drainage, deep plowing, sub-soiling, or using a raised-beds. An aquatic organism, P. brassicae thrives in saturated soil conditions where zoospores can swim freely to new hosts and resting spores are protected from desiccation. By reducing soil moisture, disease pressure can be significantly reduced. Disinfesting equipment is another common-sense and critical cultural management technique for the management of P. brassicae. As a soil-borne organism, this pathogen must be physically moved in order to enter new fields, and this can occur via tractor tires, implements, or even shoes of farm workers. Plowing or cultivating infested fields last can limit carry-over to new sites. All farm equipment should be thoroughly washed down after working infested fields. These practices will not eliminate clubroot, but can prevent the movement to new areas. In recent years, many new approaches to clubroot management have been researched. One promising new management tool is the use of calcium cyanamide fertilizer. Calcium cyanamide fertilizer, a by-product of plastics manufacturing, is 19.8% nitrogen and 50% lime expressed as CaO. When incorporated into the soil with sufficient moisture, calcium cyanamide metabolizes into calcium dihydroxide (lime) and hydrogen cyanamide, which dissolves and distributes throughout the soil water. Hydrogen cyanamide exhibits two desirable properties. It has fungicidal and herbicidal effects, and can thereby significantly reduce fungal spores while also eliminating weed seeds. Furthermore, the degradation of hydrogen cyanamide results in urea, a nitrogen source, and dicyandiamide, which inhibits nitrification by Nitrosomonas bacteria. This action slows the breakdown of ammonia into nitrate in the soil over a period of 6-8 weeks, providing a slow release source of nitrogen. Another emerging chemical control for clubroot is the use of non-ionic surfactants, commonly used as wetting agents in greenhouse systems. The exact action of these products on the pathogen has not yet been determined but appears to be due to a lytic effect on zoospores. Surfactants are attractive due to their relatively low cost and ease of use, and have been tested by several researchers for control of clubroot. Several of these products have exhibited significant control in both field and greenhouse trials. They are available in both liquid and granular formulations, and both formulations have proven effective. However, none of these products are currently labeled for field use. An intriguing approach to clubroot management is the practice of “bait” or “trap” cropping. A bait crop, which stimulates germination of the pathogen but does not allow its lifecycle to become completed, is grown prior to the cash crop. The bait crop is tilled under after several weeks to insure that clubs and resting spores are not produced. Although this management strategy requires land to be taken out of production for a period of a growing season, it has shown significant results at both lowering inoculum densities (resting spore concentration in the soil) and reducing disease in the following crop. In Massachusetts, clubroot is a significant disease problem for growers of Brassica crops, especially for an increasing number of Asian farmers who devote a relatively large percentage of their acreage to Brassica species due to their importance in their cuisine. Since Brassica crops make up the majority of their crop mix and available land is often limited for these growers, crop rotation is not always an option and new alternatives need to be evaluated. Research was implemented in 2002 and 2003 to evaluate several strategies for management of clubroot. Data from our 2002 and 2003 field trials are summarized below.

Materials and Methods Plant materials Chinese cabbage ‘Rubicon’ (Johnny’s Selected Seeds, Albion, ME) was used as the clubroot-susceptible cultivar and ‘Chorus’ (American Takii Seed Co., Salinas, CA) was used as the clubroot-resistant cultivar. Transplants were planted in the field after seven weeks in a greenhouse.

Experimental sites The experiments were carried out at two commercial farms in Western Massachusetts on land with a history of Brassica cultivation and clubroot disease. Farm 1 represented a conventional production system and Farm 2 an organic production system. Only the organic treatments were trialed at Farm 2, whereas all treatments were trialed at Farm 1 (Table 1). In each case the farmer prepared the fields, fertilized, irrigated, and managed insect pests according to their respective practices. The experimental area at Farm 1 had a soil pH of 7.1 as a result of heavy liming the previous year for management of clubroot. Farm 2 had a soil pH of 6.2.

Treatments Four field trials were conducted over two years, 2002 and 2003 (Table 1). In each trial, replicated plots were established. The treatments evaluated were: 1. boron: 15ppm solution, 75ml/plant applied as a transplant drench at planting 2. calcium cyanamide fertilizer: broadcasted and incorporated at 1000kg/ha, 7 days prior to planting 3. PCNB fungicide: 0.38% v/v solution, 237ml/plant applied as a transplant drench at planting 4. AquaGro 2000G non-ionic surfactant: banded and incorporated in the rows at 10g/m just before planting 5. leafy daikon (cv. ‘CR-1’) bait crop: broadcast-seeded at 14g/m_, grown for 4 weeks, and incorporated into the soil 1 week before planting 6. clubroot resistant Chinese cabbage (cv. ‘Chorus’) 7. interplanting of resistant and susceptible cultivars (planted at 2:1 ratio) 8. Messenger biochemical pesticide (harpin protein): applied at rate of 6.7 g/L as a soil drench at seeding and as a foliar spray every 2 weeks after 9. Rootshield granules (Trichoderma harzianum Rifai strain KRL-AG2): mixed into potting medium at 590mg/L before seeding 10. control

Data collection After 7 weeks, the plants were harvested and data was collected. Whole plants were removed from the soil, and the roots were cut off, washed and scored for disease severity. Clubroot severity was assessed on a scale of 0-3, with 0 = no clubbing; 1 = lateral roots only clubbed; 2 = <50% of tap root clubbed; and 3 = >50% of tap root clubbed. The remainder of the plant was weighed to assess the affect of clubbing on plant growth.

Results Significant differences in clubroot severity were found among the different treatments in all four trials (Table 1). In all trials, the resistant cv. Chorus was found to be the most effective at reducing disease severity. The interplanting treatment showed significantly less disease than the control in all four trials, as well. The surfactant, bait crop, calcium cyanamide, and PCNB all showed intermediate disease suppression in the summer 2002 (farm 1) and fall 2003 trials only. Boron, Messenger, and Rootshield were not significantly different from the control. Significant differences in fresh weight were also observed (Table 2), although less consistently than clubroot severity. The resistant cultivar showed significantly higher weights than the control in the summer 2002 (farm 1), summer 2002 (farm 2), and fall 2002 trials. The interplant treatment showed significantly higher weights in the summer 2002 (farm 2) trial only. Calcium cyanamide showed significantly higher weights in fall 2002 only. Rootshield showed significantly higher weights in the fall 2003 trial only. All other treatments did not weigh significantly more than the control.

Discussion At both farm sites, the resistant cultivar showed good promise for management of clubroot with very low disease severity scores and high relative weights. This cultivar was selected after it was shown to be the most resistant among four cultivars screened in greenhouse tests during winter 2002. Genetic resistance has proven to be somewhat unstable for this pathogen; however, as repeated cultivation of a resistant cultivar will select for virulent strains within a field population of the pathogen. This, coupled with the small number of resistant Asian Brassica cultivars available, may limit the effectiveness of this treatment. However, it would certainly be of use as part of a comprehensive management plan, especially if used in conjunction with crop rotation. The calcium cyanamide treatment also showed promising results. As other researchers have reported, some phytotoxicity was observed in this trial which may account for the somewhat reduced weights seen with this treatment. As a relatively hard to find product, it is also quite expensive in the U.S., so targeting the minimum application rate necessary would also be important. In addition, calcium cyanamide is not labeled as a pesticide for control of clubroot; however, it is a legal source of fertilizer. The surfactant treatment also showed positive results and is worthy of further refinement. Prior research has shown that as a granular product, AquaGro 2000G seems to have a longer period of activity than some of the liquid formulations. The granular product, in combination with a liquid surfactant applied during the crop growth, might show even more improved performance. One complication will be getting these products labeled for field use as they are currently only labeled for greenhouse production. The bait crop treatment also showed some potential for disease management, but was inconsistent from trial to trial. One possible reason for this may have been differing soil conditions in each of the four trials. In the fall 2002 trial, the field site was very wet with very high inoculum rates (due to intense clubroot disease in that part of the grower’s field for many years). These field conditions may have decreased the efficacy of the bait crop treatment in that particular trial. The PCNB, calcium cyanamide, and surfactant treatments may have also been limited by the soil conditions in fall 2002. At the Farm 2 site, soil pH was significantly lower (6.2) than at Farm 1 (7.1) and the soils were generally less fertile. This also may have influenced the bait crop treatment by providing more optimal conditions for clubroot infection and placing additional stress on the plants making them more prone to disease. Differing field conditions may also account for the less significant weight differences (and the lack of a strong correlation between disease severity and weight) observed at the farm 1 site compared to the farm 2 site. Very high inputs (high to excessive fertilization and irrigation) at farm 1 may have enabled the infected plants to grow well, in spite of high disease severity; whereas poorer soils with no irrigation at farm 2 did not enable the infected plants to grow well .

Management recommendations for club root 1. Lime to bring the soil pH up to 7.1 to 7.2 2. Avoid planting cruciferous plants in soil known to contain the clubroot organism. 3. Do not raise transplants in soil known to contain the clubroot organism. 4. If planting into contaminated soil, ask your seed source if they have resistant cultivars. Resistant cultivars are available for most Brassica crops. 5. Use resistant cultivars in rotation with non-host crops. 6. Chisel plow and use raised beds if drainage is poor. 7. Apply PCNB fungicide in accordance with the label. 8. Apply calcium cyanamide fertilizer at 1000lbs./acre at least 7 days before planting. Be sure to account for the liming effect and N contribution of this fertilizer. 9. When working in fields known to be contaminated, hose down equipment before moving into new fields. **Clubroot is a disease that requires a multi-faceted approach to management. Several of the above management recommendations may be necessary to obtain acceptable disease suppression. Contact your vegetable Extension specialist for specific recommendations Table 1: Clubroot severity data in four field trials Clubroot severity_ Farm 1 Farm 2 Fall Fall Treatment Summer 2002 2002 2003 Summer 2002 control 2.57 a_ 2.96 a 2.55 a 2.92 a boron 2.57 a 2.91 a 2.63 a 3.00 a PCNB 1.92 ab 2.35 b 1.55 bc bait crop 1.65 b 3.00 a 1.58 bc 3.00 a interplant 1.35 b 1.71 c 1.19 c 1.54 b Aqua-Gro 2000G 1.32 b 2.75 a 1.04 c calcium cyanamide 1.17 b 2.85 a 1.58 bc resistant cultivar 0.17 c 0.13 d 0.00 d 0.11 c Messenger 2.50 a Rootshield 2.30 a

_Clubroot severity assessed on a scale of 0-3 with 0 = no clubbing; 1 = lateral roots only clubbed; 2 = <50% of tap root clubbed; and 3 = >50% of tap root clubbed (Dixon and Williamson, 1985). _within each column, values followed by the same letter are not significantly different at P=0.05, DNMRT

Table 2: Fresh weight data in four field trials

Fresh weight (kg) Farm 1 Farm 2 Summer Fall Treatment 2002 2002 Fall 2003 Summer 2002 control 1.53 ab_ 0.36 c 0.72 b 0.10 c boron 1.49 ab 0.45 c 0.69 b 0.10 c PCNB 1.52 ab 0.73 bc 0.67 b bait crop 1.86 ab 0.53 c 1.04 ab 0.02 c interplant 1.44 b 0.83 bc 0.97 ab 0.89 b Aqua-Gro 2000G 2.04 ab 1.06 abc 0.95 ab calcium cyanamide 1.69 ab 1.68 a 0.98 ab resistant cultivar 2.13 a 1.53 ab 1.12 ab 1.57 a Messenger 0.90 ab Rootshield 1.26 a _within each column, values followed by the same letter are not significantly different at P=0.05, DNMRT