Effect of Host Resistance and Fungicide Application on Clubroot Pathotype 6 in Green Cabbage and Napa Cabbage

in HortTechnology

Field trials were conducted to evaluate resistance to clubroot (Plasmodiophora brassicae, pathotype 6) in green cabbage (Brassica oleracea var. capitata) and napa cabbage (Brassica rapa ssp. pekinensis) at sites in southern Ontario in 2009 and 2010. The reaction of green cabbage cultivars Kilaton, Tekila, Kilaxy, and Kilaherb and the commercial standard cultivars, Bronco or Atlantis, were evaluated on organic (two site-years) and mineral soils (two site-years) that were naturally infested with the clubroot pathogen. In addition, fluazinam fungicide was drench applied to one treatment of the commercial standard cultivar immediately after transplanting. The napa cabbage cultivars Yuki, Deneko, Bilko, and Mirako (in 2009) and Emiko, Mirako, Yuki, and China Gold (in 2010) were evaluated only on organic soils (two site-years). At harvest, the roots of each plant were assessed for clubroot incidence and severity. Also, plant and head characteristics of the resistant green cabbage cultivars were evaluated at one site in 2010. The green cabbage cultivars Kilaton, Tekila, Kilaxy, and Kilaherb were resistant to pathotype 6 (0% to 3.8% incidence), but ‘Bronco’ was susceptible (64% to 100% incidence). Application of fluazinam reduced clubroot severity on ‘Bronco’ by 6% at one of three sites. Resistance was more effective in reducing clubroot than application of fluazinam. Plant and head characteristics of the resistant cultivars were similar to those of ‘Bronco’ treated with fluazinam. Napa cabbage cultivars Yuki, Deneko, Bilko, Emiko, and China Gold were resistant to clubroot (0% to 13% incidence), and ‘Mirako’ was highly susceptible (87% to 92% incidence). We conclude that the clubroot resistance available in several cultivars of green and napa cabbage was effective against P. brassicae pathotype 6.

Abstract

Field trials were conducted to evaluate resistance to clubroot (Plasmodiophora brassicae, pathotype 6) in green cabbage (Brassica oleracea var. capitata) and napa cabbage (Brassica rapa ssp. pekinensis) at sites in southern Ontario in 2009 and 2010. The reaction of green cabbage cultivars Kilaton, Tekila, Kilaxy, and Kilaherb and the commercial standard cultivars, Bronco or Atlantis, were evaluated on organic (two site-years) and mineral soils (two site-years) that were naturally infested with the clubroot pathogen. In addition, fluazinam fungicide was drench applied to one treatment of the commercial standard cultivar immediately after transplanting. The napa cabbage cultivars Yuki, Deneko, Bilko, and Mirako (in 2009) and Emiko, Mirako, Yuki, and China Gold (in 2010) were evaluated only on organic soils (two site-years). At harvest, the roots of each plant were assessed for clubroot incidence and severity. Also, plant and head characteristics of the resistant green cabbage cultivars were evaluated at one site in 2010. The green cabbage cultivars Kilaton, Tekila, Kilaxy, and Kilaherb were resistant to pathotype 6 (0% to 3.8% incidence), but ‘Bronco’ was susceptible (64% to 100% incidence). Application of fluazinam reduced clubroot severity on ‘Bronco’ by 6% at one of three sites. Resistance was more effective in reducing clubroot than application of fluazinam. Plant and head characteristics of the resistant cultivars were similar to those of ‘Bronco’ treated with fluazinam. Napa cabbage cultivars Yuki, Deneko, Bilko, Emiko, and China Gold were resistant to clubroot (0% to 13% incidence), and ‘Mirako’ was highly susceptible (87% to 92% incidence). We conclude that the clubroot resistance available in several cultivars of green and napa cabbage was effective against P. brassicae pathotype 6.

Clubroot, caused by the soil-borne protist P. brassicae, is a limiting factor in the production of brassica crops worldwide (Dixon, 2006). The characteristic symptom of clubroot is the formation of root swellings (clubs) that disrupt the vascular tissue of the root. Severe symptoms can lead to delayed variable maturity, or both, wilting, and reduced yield (Cheah et al., 2006; Karling, 1968). In Canada, clubroot has been reported on brassica vegetables and canola (Brassica napus) in Ontario, Quebec, British Columbia, the Atlantic Provinces, Alberta (Cao et al., 2009; Howard et al., 2010; Tewari et al., 2005), and most recently in Saskatchewan (Dokken-Bouchard et al., 2010). Clubroot is endemic in many regions of Ontario where brassica crops are grown (Adhikari, 2010; Conners et al., 1956; McDonald and Westerveld, 2008). Numerous pathotypes of P. brassicae have been identified (Xue et al., 2008). Pathotype 6 is the predominant pathotype in Ontario (Reyes et al., 1974; Strelkov et al., 2006), but pathotypes 2 and 5 are also present.

Clubroot is a serious threat to the brassica vegetable industry in Ontario, which had a farm gate value of $54 million in 2010 [Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA), 2010a]. The major brassica vegetable crops grown in Ontario are cabbage, broccoli (Brassica oleracea var. italica), cauliflower (B. oleracea var. botrytis), and Asian vegetables including napa cabbage (Brassica rapa ssp. pekinensis), shanghai pak choy (B. rapa ssp. chinensis var. communis), and chinese flowering cabbage (B. rapa ssp. chinensis var. utilis). A relatively small number of growers produce these specialized crops, and it can be difficult for them to follow long crop rotations or get access to noninfested land. This has contributed to the buildup of the pathogen over time (McDonald and Westerveld, 2008).

P. brassicae survives in the absence of hosts as long-lived resting spores in the soil (Dixon, 1996; Karling, 1968). Infection and development of P. brassicae is favored by soil temperatures at or above 17 °C, with optimal soil temperatures between 20 and 26 °C (Gossen et al., 2011a; Sharma et al., 2011a, 2011b), slightly acid soil pH (Gossen et al., 2011b; Niwa et al., 2007) and low organic matter in soils (Colhoun, 1952, 1953). However, high levels of clubroot can occur in soils with organic matter of 60% or higher (McDonald and Westerveld, 2008).

Several strategies have been developed to reduce clubroot damage in the field. Among those are crop rotation with nonbrassica crops for at least 5 years, application of agricultural lime or soil amendments to raise soil pH above 7.2 (Dixon, 2009; Donald et al., 2006; OMAFRA, 2010b), improved drainage and avoiding production of susceptible crops on poorly drained sites (OMAFRA, 2010b), application of fungicides at seeding (Naiki and Dixon, 1987; OMAFRA, 2010b), use of biocontrol agents (Cheah et al., 2000, 2001)and use of resistant cultivars. Synthetic fungicides and biofungicides are used in various parts of the world for clubroot management (Mitani et al., 2003; Suzuki et al., 1995), but only pentachloronitrobenzene (Quintozene 75 WP; AMVAC Chemical Corp., Newport Beach, CA) and fluazinam (Allegro 500F; ISK Biosciences Corp., Concord, OH) are registered for management of clubroot on brassicae vegetable crops in Canada (Howard et al., 2010; OMAFRA, 2010b). There are no biofungicides registered in Canada for the suppression of clubroot, but a recent study on the biofungicides Bacillus subtilis (Serenade ASO; AgraQuast, Davis, CA) and Gliocladium catenulatum, (Prestop; Verdera OY, Luoteisrinne, Finland) show promise (Peng et al., 2011).

Use of resistant cultivars is one of the most effective ways of managing a wide range of diseases. Work to develop brassica crops with durable resistance to clubroot is ongoing and resistant cultivars of B. napus, B. oleracea, and B. rapa have recently been released (Diederichsen et al., 2009). However, the resistant genes that have been incorporated into these crops are not effective against all P. brassicae pathotypes. Syngenta Seeds (Boise, ID) and Bejo Seeds (Geneva, NY) have released cultivars of green cabbage and napa cabbage for production in Canada that are purported to have resistance to clubroot. It is important to evaluate these resistant cultivars at several sites in Ontario to determine if they provide effective reductions in clubroot under various soil conditions and disease pressures. The main objective of this study was to assess clubroot development in these resistant green and napa cabbage cultivars. A secondary objective was to compare the efficacy of a drench application of fluazinam fungicide on a susceptible green cabbage cultivar to determine if fungicide application could reduce clubroot as effectively as the use of a resistant cultivar. A third objective was to compare the quality of the resistant green cabbage cultivars to that of the standard susceptible cultivar Bronco.

Materials and methods

Field sites.

One field trial was established each year on an organic soil (typic Hemic-Histosoil, 74% organic matter, pH 6.4) at the Muck Crops Research Station (MCRS), University of Guelph, on the Holland Marsh, ON, Canada (lat. 44°15′N, long. 77°35′W) in 2009 and 2010 (Site 1). A second field trial (Site 2) was conducted on a commercial field near the Simcoe Research Station, University of Guelph, Simcoe, ON, Canada (lat. 42°59′N, long. 80°17′W) on a mineral soil (typic Berrien clay to sandy loam, 2.8% organic matter, pH 6.8) in 2009. A third field trial (Site 3) was conducted on a commercial field near Site 2 (lat. 43°17′N, long. 80°6′W) on a mineral soil (a typic Grimsby sandy loam 2.2% organic matter, pH 7.4) in 2010.

Each site was naturally infested with P. brassicae pathotype 6. At Site 1 (organic soil), brassica crops have been cultivated for 4 years on the same site to provide a high level of inoculum. Before that, no brassica crops had been grown on that site for at least 5 years. At Sites 2 and 3 (mineral soils), brassica crops have been cultivated for 8 to 10 years in two to three rotations with cereals.

Each trial was laid out in a randomized complete block design with four replications. Fertilization, weeds and insects were managed according to recommended commercial practices (OMAFRA, 2010b). Mean air temperatures and rainfall data were collected each year during the growing period (July to October) at automated weather stations located near the research trials at the MCRS for Site 1 (McDonald et al., 2009, 2010) and the Simcoe Research Station for Sites 2 and 3 (Environment Canada, 2011).

Green cabbage.

The green cabbage cultivars Kilaton, Tekila, Kilaxy, Kilaherb (Syngenta Seeds) and the clubroot-susceptible standard cultivar Bronco (Bejo Seeds) were evaluated at Site 1 (2009 and 2010) and Site 3 (2010). At Site 2, the susceptible cultivar Atlantis (Stokes Seeds, Thorold, ON, Canada) was used as the susceptible standard in place of ‘Bronco’, and assessed against ‘Kilaherb’ and ‘Tekila’. In addition, the fungicide fluazinam was applied at a rate of 0.025 g per plant in 100 mL of water at the base of each plant of the susceptible standard cultivar immediately after transplanting. Because the number of plants per hectare varied, the rate of fluazinam was 1.0 kg·ha−1 (Site 1, 2009), 0.7 kg·ha−1 (Site 1, 2010), 0.8 kg·ha−1 (Site 2, 2009), and 0.7 kg·ha−1 (Site 2, 2010).

At Site 1, each cultivar was seeded into 128-cell plug trays filled with a commercial soil-less mix on 8 May 2009 and 5 May 2010. Plants were grown in a greenhouse under ambient light and temperature conditions and were hand transplanted on 1 June 2009 and 8 June 2010. In 2009, each plot consisted of three 7.5-m-long rows, with 55 cm between rows and 45 cm in-row spacing. In 2010, each plot consisted of two 7.5-m-long rows with 86 cm between rows and 45-cm in-row spacing.

At Site 2, each cultivar was seeded on 4 June 2009 and transplanted using a mechanical transplanter into one 7-m-long row with 90 cm between rows and 35 cm between plants on 6 July. At Site 3, each cultivar was seeded on 21 May 2010 into 200-cell plug trays. Seedlings were hand transplanted on 29 June 2010 into one 8.6-m-long row per plot, with 81 cm between rows and plants within the row spaced 43 cm apart.

Cabbage heads were harvested when each cultivar achieved marketable size and firmness. At Site 1 in 2009, 20 mature cabbage heads per plot were harvested on 6 Aug. (‘Bronco’, ‘Bronco’ + fluazinam), 12 Aug. (‘Tekila’), and 27 Aug. (‘Kilaton’, ‘Kilaxy’, ‘Kilaherb’). In 2010, 20 heads were harvested on 11 Aug. (‘Tekila’, ‘Kilaherb’) and 24 Aug. (‘Bronco’, ‘Kilaton’, ‘Kilaxy’). Heads were harvested consecutively within a row from the center of each plot, such that seven, six, and seven heads were harvested per row. At Site 2, a 3.5-m section of the center row (10 heads) was harvested on 23 Sept. (‘Kilaherb’, ‘Tekila’) and 20 Oct. 2009 (‘Atlantis’), starting at a random spot. At Site 3, a 7-m length of row (15 to 18 heads) in each plot was harvested on 22 Sept. (‘Bronco’, ‘Kilaherb’, ‘Tekila’) and 21 Oct. 2010 (‘Kilaton’, ‘Kilaxy’), starting at the third head in the row.

Cabbage heads were weighed and graded into marketable and unmarketable categories. At Site 3, cultivars were evaluated at harvest for stock uniformity, length of stalk, growth habit, head protection, and savoying (the extent of leaf rugosety) of leaf. In addition, five randomly selected marketable cabbage heads per plot were evaluated for head shape and external color, and cut in half longitudinally to assess internal color, core size, core width, core length, and internal breakdown. These plant and cabbage head characteristics were evaluated using the rating system developed by Loughton and Baker, (1994).

Napa cabbage.

The napa cabbage cultivars Mirako (Bejo Seeds) and Yuki (Sakata Seed America, Morgan Hill, CA) were evaluated in both years at Site 1; cultivars Bilko and Deneko (Bejo Seeds) were evaluated in 2009, but replaced with ‘Emiko’ (Bejo Seeds) and ‘China Gold’ (Sakata Seed America) in 2010.

Each cultivar was seeded into 128-cell plug trays on 8 May 2009 and 6 May 2010, and maintained in the greenhouse under ambient light and temperature conditions. Seedlings were hand transplanted on 1 June 2009 and 8 June 2010. Each plot consisted of three 7.5-m-long rows with 55 cm between rows and 30 cm in-row spacing. To determine yield, 24 mature heads per plot were harvested and weighed on 17 and 20 July 2009 and 15 July 2010.

Clubroot.

Roots of all of the harvested plants in each plot were dug, washed, air dried for 1 h, and assessed for clubroot incidence and severity. Clubroot severity was rated using a 0–3 scale (Kuginuki et al., 1999), where roots were separated into classes of: 0 = no galling, 1 = a few small galls (small galls on less than 1/3 of roots), 2 = moderate galling (small to medium-sized galls on one-third to two-thirds of roots), and 3 = severe galling (medium to large-sized galls on more than two-thirds of roots). Clubroot severity ratings were used to calculate a disease severity index (DSI) to transform the ratings to a 0–100 scale, using the following equation (Kobriger and Hagedorn, 1983):

DE1

To determine the concentration of clubroot resting spores in the soil, soils samples were collected at Site 1 before planting in 2009 and 2010, and at Site 3 before planting and after harvest in 2010. The quantification of resting spores was conducted using a modification of the method of Dhingra and Sinclair (1985). Briefly, a 25 g sample of dried soil was mixed with 100 mL of 2% sodium hexametaphosphate and shaken vigorously for 1 min. The suspension was kept overnight and filtered through eight layers of cheesecloth. The filtrate was centrifuged for 10 min and the supernatant was discarded. The pellet was resuspended in distilled water and the centrifugation process was repeated to collect the fine particles. The fine particles were suspended in enough distilled water to bring the mixture to a final weight equal to the original weight of the soil sample. The suspension was centrifuged and the supernatant was poured off, then the pellet was dispersed in 50 mL of 40% sucrose. The resulting suspension was placed into a 100 mL beaker and stored for 2 d at 3 °C to allow the mineral component to settle. The supernatant was then poured off and the pellet was diluted with an equal volume of distilled water and centrifuged for 1 h. The supernatant was discarded and the pellet was resuspended in 5 mL of distilled water. The number of resting spores in the suspension was determined using a hemocytometer.

In 2010, a sample of clubbed roots from Sites 1 and 3 was collected and sent to the Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada, for determination of the P. brassicae pathotype(s).

Data analysis.

The data from each trial were analyzed using analysis of variance in SAS (Proc GLM, version 9.2; SAS Institute, Cary, NC). Each data set was tested for normality using the Shapiro-Wilk test and outliers were identified using Lund’s test of standardized residuals (Lund, 1975). Each of the data sets was normally distributed and no outliers were identified. Data from 2009 and 2010 were combined when there was no cultivar by location or cultivar by year interactions. When the interactions were significant, the analysis was done separately by year and location. Means were separated using Tukey’s Studentized range (hsd) test at P = 0.05. Differences are significant at P = 0.05 unless otherwise indicated.

Results

Weather

The mean air temperatures during the growing season were substantially lower in 2009 than in 2010. The only exception was temperatures in September at Sites 2 and 3, where mean temperatures were essentially the same in both years, but below the long-term average. In both years, rainfall at Site 1 was substantially higher for July and above the long-term average. At Sites 2 and 3, rainfall was substantially higher in Aug. 2009 and Oct. 2010 and was higher overall for the 2009 growing season. Rainfall in 2009 was above the long-term average and below average in 2010 (Table 1).

Table 1.

Mean air temperature and rainfall during the growing period of green cabbage and napa cabbage grown on organic soil at the Holland Marsh, ON, Canada (Site 1), and on mineral soils near Simcoe, ON, Canada (Sites 2 and 3), in 2009 and 2010.

Table 1.

Pathotype and disease pressure

P. brassicae pathotype 6 was the sole pathotype identified in clubbed roots from Sites 1 and 3 (S. Strelkov, personal communication). The average concentration of resting spores before planting at Site 1 (organic soil) was 1.3 × 106 spores per gram of soil in 2009 and 9.0 × 106 spores per gram in 2010. The average concentration of resting spores at Site 3 (mineral soil) in 2010 was 1.7 × 105 spores per gram of soil before planting and 1.2 × 105 spores per gram after harvest. Spore concentrations were not determined at the mineral soil site in 2009.

Green cabbage

Site 1 (organic soil).

The resistant cultivars developed very few clubroot symptoms relative to ‘Bronco’ (susceptible) in both years. However, there was a year × cultivar interaction at this site for incidence (P = 0.0015), for DSI (P = <0.0001), and cabbage head weight (P = <0.0001), so the data for each year are presented separately (Table 2). In 2009, clubroot incidence and severity in the four resistant cultivars (incidence = 0% to 4%, DSI = 0 to 3) were significantly lower (P < 0.0001) than in the susceptible ‘Bronco’ (incidence = 86%, DSI = 42). Fungicide application did not reduce clubroot incidence or severity on ‘Bronco’ or affect head weight (Table 2). Cabbage head weights were highest in ‘Kilaherb’ (3.7 kg), intermediate in ‘Kilaton’, ‘Tekila’, and ‘Bronco’ with and without fungicide (2.4 to 2.6 kg), and lowest in ‘Kilaxy’ (1.8 kg) (Table 2).

Table 2.

Clubroot incidence and severity [disease severity index (DSI)] and yield of clubroot-resistant green cabbage cultivars and the susceptible cultivar Bronco with and without fluazinam fungicide, grown in organic soil at the Holland Marsh, ON, Canada, in 2009 and 2010.

Table 2.

In 2010, the results showed a similar pattern; clubroot incidence and severity of the four resistant cultivars (incidence = 0% to 1%, DSI = 0 to 1) were significantly lower (P < 0.0001) than in ‘Bronco’ (incidence = 100%, DSI = 98). Again, fungicide application did not reduce incidence or severity, or increase head weight (Table 2). High levels of clubroot in ‘Bronco’ were reflected in the weight of heads, which were generally higher in the resistant cultivars (1.7 to 2.3 kg) than in ‘Bronco’ (1.0 to 1.2 kg). However, there was no significant difference in head weight between ‘Kilaxy’ and ‘Bronco’ treated with fungicide.

Sites 2 and 3 (mineral soil).

There were differences among some of the cabbage cultivars evaluated in 2009 and 2010 on mineral soil (Sites 2 and 3), so results from each year are presented separately (Table 3). In 2009 (Site 2), clubroot levels were low and there were no significant differences in clubroot incidence or severity or head weights among the cultivars assessed. In 2010 (Site 3), no clubroot developed in ‘Kilaherb’, ‘Tekila’, ‘Kilaxy’, and ‘Kilaton’, but incidence was 100% on the susceptible ‘Bronco’ with or without fungicide. Fungicide application reduced DSI in ‘Bronco’ by 6% and there was a numerical, but not statistically significant increase in yield from 0.8 to 1.5 kg per head (Table 3). Only ‘Kilaton’ had a higher head weight than ‘Bronco’ treated with fungicide. ‘Bronco’ without fluazinam had significantly lower head weight than all of the resistant cultivars (Table 3).

Table 3.

Clubroot incidence and severity [disease severity index (DSI)] and yield of clubroot-resistant green cabbage cultivars and susceptible cultivars Atlantis and Bronco untreated and treated with fluazinam fungicide grown on mineral soil near Simcoe, ON, Canada, in 2009 and 2010.

Table 3.

The plant and head characteristics evaluated in Site 3 (2010) differed among the cabbage cultivars. The resistant cultivars and ‘Bronco’ + fluazinam had more uniform stocks than ‘Bronco’ alone. ‘Tekila’, ‘Kilaherb’, and ‘Bronco’ with or without fungicide, had more compact heads than ‘Kilaton’ or ‘Kilaxy’ (Table 4). All of the cultivars had smooth leaves and intermediate stalk length. ‘Bronco’ was pale green relative to ‘Kilaxy’, ‘Kilaherb’, ‘Kilaton’, and ‘Tekila’, which were dark green. ‘Kilaton’ and ‘Kilaxy’ exhibited the best head protection, ‘Tekila’, ‘Kilaherb’ and ‘Bronco’ + fluazinam had intermediate head protection, and nontreated ‘Bronco’ had the poorest head protection. The head shape of ‘Kilaherb’ was slightly flat, ‘Tekila’ and ‘Kilaton’ were intermediate, and ‘Kilaton’, ‘Kilaxy’, and ‘Bronco’ were globe-shaped (Table 4). The internal color of each cultivar varied from white to yellow white, with no internal breakdown or tip burn symptoms, as shown in Fig. 1. Core size was largest in ‘Tekila’, slightly smaller in ‘Kilaherb’, intermediate in the other cultivars, and smallest in nontreated ‘Bronco’. Core width was highest on ‘Kilaton’ and ‘Kilaxy’, intermediate in ‘Tekila’, ‘Kilaherb’, and ‘Bronco’+ fluazinam, and smallest on nontreated ‘Bronco’. Core height was longest in the resistant cultivars, intermediate in ‘Bronco’+ fluazinam, and shortest in the nontreated ‘Bronco’. Cabbage head weights of the resistant cultivars and ‘Bronco’ + fluazinam were higher than in the nontreated ‘Bronco’ (Table 4).

Table 4.

Evaluation of cabbage plant and head characteristics of clubroot-resistant green cabbage cultivars and the susceptible cultivar Bronco untreated and treated with the fluazinam fungicide grown in mineral soil naturally infected with Plasmodiophora brassicae (Site 3) near Simcoe, ON, Canada, in 2010.

Table 4.
Fig. 1.
Fig. 1.

Comparison of cabbage head characteristics: head shape, width, core size, core width and length, internal color of clubroot-resistant green cabbage cultivars and the susceptible cultivar Bronco untreated and treated with fluazinam fungicide, grown on mineral soils, near Simcoe in 2010. The fungicide fluazinam was applied at a rate of 0.025 g (0.00088 fl oz) per plant in 100 mL (3.38 fl oz) of water at the base of each plant of the susceptible standard cultivar Bronco immediately after transplanting. The rate of fluazinam was 0.7 kg·ha−1 (0.62 lb/acre).

Citation: HortTechnology hortte 22, 3; 10.21273/HORTTECH.22.3.311

Napa cabbage

In 2009, no clubroot symptoms were observed on cultivar Yuki. Clubroot levels on ‘Deneko’ and ‘Bilko’ were low (incidence = 4% to14%, DSI = 2 to 6), and high levels of clubroot developed in the susceptible standard ‘Mirako’ (incidence = 88%, DSI = 43) (Table 5). Despite differences in clubroot severity among the cultivars, head weights were not significantly different and were 2.1 to 2.6 kg per head. In 2010, the putative resistant cultivars, China Gold and Emiko, were assessed in place of ‘Deneko’ and ‘Bilko’. The pattern was similar to 2009: ‘Mirako’ had high levels of clubroot, and there were no symptoms on ‘China Gold’ and ‘Emiko’ (Table 5). Head weights were not significantly different for all cultivars and ranged from 1.4 to 1.7 kg per head.

Table 5.

Incidence and severity [disease severity index (DSI)] of clubroot and yield of clubroot resistant and susceptible napa cabbage cultivars grown in organic soil at the Holland Marsh, ON, Canada, in 2009 and 2010.

Table 5.

Discussion

Over a 2-year period, multiple green and napa cabbage cultivars that are being marketed as resistant to clubroot showed very low levels of clubroot when exposed to P. brassicae pathotype 6 on organic and mineral soils at sites in Ontario. The standard commercial cultivars included as susceptible controls had high levels of clubroot, except at the mineral soil site (Site 2) in 2009. Although none of the resistant cultivars were completely immune at all of the sites, several had no symptoms of clubroot at one or more sites, even though disease pressure was high.

The source of clubroot resistance in the cultivars evaluated in this study is proprietary information. Knowing the source of resistance would be useful because the specific clubroot-resistance gene(s) in a cultivar and the P. brassicae pathotype in a field can influence clubroot incidence and severity. Clubroot resistance in B. oleracea is frequently based on a few genes for resistance derived initially from turnip [B. rapa (Hirai, 2006; Hirai et al., 2003)]. Clubroot resistance from this source is generally race-specific and breakdown of resistance has been reported (Crete and Chiang, 1980; Diederichsen et al., 2009; Dixon, 2006; Manzanares-Dauleux et al., 2001; Piao and Ramchiary, 2009). Examples of resistance breakdown include the green cabbage cultivars Kilaton and Tekila (included in the present study). Soon after these cultivars were introduced in Germany, Poland, and France in 2005, there were reports of medium to severe clubroot severity at some sites (Diederichsen et al., 2009). Similarly, clubroot control failures on chinese cabbage ‘Yuki’ were reported in Australia (Donald and Porter, 2009). In the current study, green cabbage cultivars Kilaton and Tekila, and napa cabbage cultivar Yuki were resistant, but developed slight symptoms of clubroot.

The green cabbage cultivars were tested in two soil types that differed substantially in organic matter content and pH. The organic soil at Site 1 had far more organic matter (74%) than the mineral soils at Sites 2 and 3 (3%). Soils with high organic matter, or where additional organic matter was incorporated, have been reported to reduce clubroot by bringing soil pH to neutral levels (Niwa et al., 2007). Soils with high organic matter also have high soil moisture retention that induces constant release of hydrogen cations (H+), thus, rendering the soils more acidic, and consequently, lowering the soil pH (Kroetsch et al., 2011). Therefore, based on organic matter content (but not pH) lower levels of clubroot would be expected at Site 1 than at Site 3. This was not the case, but high clubroot incidence was expected and has been reported from this region before (McDonald and Westerveld, 2008).

Previous studies to determine the pH required to reduce clubroot severity were not conclusive. Low soil pH generally favors the development of clubroot (Myers and Campbell, 1985; Tremblay et al., 2005). However, there are a number of reports of control failures at or above pH 7.2 (Myers et al., 1981; Wellman, 1930). Indeed, a recent controlled environment study demonstrated that clubroot incidence of at least 40% developed in sand at pH 8.0 when temperature and soil moisture were optimum (Gossen et al., 2011b).

The concentration of resting spores in soil is an important factor in clubroot incidence and severity (Hildebrand and McRae, 1998). The concentration of P. brassicae resting spores was high at the three sites where it was assessed, ranging from 105 to 106 spores per gram of soil. This is well above the minimum threshold level of 103 spores per gram of soil required for clubroot symptom development (Donald and Porter, 2004; Faggian and Strelkov, 2009).The incidence and severity of clubroot was generally lower in 2009 than in 2010. This may have been caused solely by a higher concentration of resting spores at the organic soil site in 2010 (1.3 × 106 spores per gram in 2009 and 9.0 × 106 spores per gram in 2010).

However, weather conditions can also affect the development of clubroot. Recent studies under controlled conditions (Gossen et al., 2011a; Sharma et al., 2011a, 2011b) have confirmed previous field observations (Chupp, 1917; Colhoun, 1952, 1953; Einhorn and Bochow, 1990; McDonald and Westerveld, 2008; Monteith, 1924; Wellman, 1930) that infection and development of P. brassicae are inhibited at temperatures below 17 °C and above 26 °C. Soil moisture also influences clubroot. Clubroot incidence and severity are highest at soil moisture content of 70% to 80% of the maximum water holding capacity in acid soils (Monteith, 1924). Also, cumulative rainfall (especially early in the season) is positively correlated with clubroot severity (Adhikari, 2010; Thuma et al., 1983).

In the present study, the mean temperature and rainfall at Site 1 were higher in 2010 than in 2009. In the studies on mineral soil, July was 4.0 °C cooler and August was 1.9 °C cooler in 2009 (Site 2) than in 2010 (Site 3). The cooler temperatures in 2009 may have reduced clubroot development. However, rainfall was higher in July and Aug. 2009 than in 2010, and higher in total for the growing season, so rainfall does not appear to be an important limiting factor in this study.

Application of fluazinam fungicide to ‘Bronco’ did not reduce incidence or DSI or increase yield at Site 1 in either year and only slightly reduced clubroot severity at Site 3. However, the roots of nontreated ‘Bronco’ plants at harvest were clubbed and decayed, while the roots of the fungicide-treated ‘Bronco’, although clubbed, remained intact and had a few healthy feeding roots at Site 3, based on visual observation. The healthier root system of the fungicide-treated ‘Bronco’ cabbage may explain the trend toward higher yield in comparison with nontreated ‘Bronco’ on mineral soil. This difference in yield was not statistically significant, but was large enough (almost 2×) to merit consideration by producers. The relative efficacy of the fungicide fluazinam in controlling clubroot on broccoli grown on mineral soils was reported by Donald et al., (2006). When comparing different clubroot control methods, the researchers found that the drench application of the fungicide soon after crop transplant reduced clubroot on sandy soils. Broccoli yield was further increased when the fungicide was applied in conjunction with soil lime treatments to increase the soil pH. The efficacy of the fungicide was in part attributed to the sandy soils profile and porosity, which enables fungicide movement in soil.

Yield of the green cabbage cultivars Kilaherb, Kilaton, Kilaxy, and Tekila was similar at the organic and mineral soil sites. ‘Kilaxy’ had smaller heads and lower head weights than the other resistant cultivars and the fungicide-treated ‘Bronco’ in 1 of 2 years. This lower yield may have resulted from its long growth cycle. Even though it was among the last cultivars harvested, it was probably not yet at full maturity. In general, yields of the green and napa cabbage cultivars were higher in 2009 than in 2010, likely in response to lower clubroot pressure in 2009.

Plant and head characteristics of ‘Kilaherb’, ‘Kilaton’, ‘Kilaxy’, and ‘Tekila’ were generally similar to those of ‘Bronco’ treated with fungicide. However, some plant stunting (short stalk length) caused by clubroot was observed in ‘Bronco’ treated with fungicide, and severe stunting was observed in nontreated ‘Bronco’. The late maturity of ‘Kilaxy’ resulted in sprawling heads that required more trimming to bring to marketable acceptance. Trimming reduced head width and weight, and together with late maturity, resulted in the lowest yield among the resistant cultivars.

There were no differences in yield among the resistant and susceptible cultivars of napa cabbage, even though very high clubroot severity developed on the susceptible ‘Mirako’. This indicates that napa cabbage may be more tolerant to clubroot, in terms of maintaining yield, than green cabbage.

In conclusion, the green cabbage cultivars Kilaherb, Kilaton, Kilaxy, and Tekila, and the napa cabbage cultivars, China Gold, Emiko, Yuki, Deneko, and Bilko, were highly resistant to pathotype 6 of P. brassicae, the causal agent of clubroot disease of brassica crops in Ontario. The resistance in green cabbage was consistent on two very different soil types. A single drench application of fluazinam fungicide did not provide effective clubroot control. Thus, the use of resistant cultivars is currently a more effective clubroot management strategy. Very low levels of clubroot symptoms were observed on the resistant cultivars, which indicate that they are not immune to P. brassicae. The resistant cultivars of green cabbage have most of the desirable plant and head characteristics of ‘Bronco’, and as such can be easily adopted by growers as a clubroot management tool. Cultivar resistance should be used as part of an integrated pest management strategy that includes crop rotation and maintaining an alkaline soil pH, so that the resistance will remain stable in the future.

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Literature cited

  • AdhikariK.K.C.2010Effect of temperature biofungicides and fungicides on clubroot of selected Brassica crops. University of Guelph Guelph ON Canada Master’s Thesis

  • CaoT.ManoliiV.P.HwangS.F.HowardR.J.StrelkovS.E.2009Virulence and spread of Plasmodiophora brassicae (clubroot) in Alberta, CanadaCan. J. Plant Pathol.31321329

    • Search Google Scholar
    • Export Citation
  • CheahL.H.GowersS.MarshA.T.2006Clubroot control using brassica break cropsActa Hort.706329332

  • CheahL.H.KentG.GowersS.2001Brassica crops and a Streptomyces sp. as potential biocontrol for clubroot of brassicasN.Z. Plant Prot. Sci.548083

    • Search Google Scholar
    • Export Citation
  • CheahL.H.VeerakoneS.KentG.2000Biological control of clubroot on cauliflower with Trichoderma and Streptomyces sppN.Z. Plant Prot. Sci.531821

    • Search Google Scholar
    • Export Citation
  • ChuppC.1917Studies on clubroot of cruciferous plantsBul. Cornell Univ. Agr. Expt. Sta.387419452

  • ColhounJ.1952Factors affecting the incidence of club root disease of BrassicaeNature1692122

  • ColhounJ.1953A study of the epidemiology of club-root disease of BrassicaeAnn. Appl. Biol.40262283

  • ConnersI.L.ShoemakerR.A.CreelmanD.W.1956Thirty-sixth annual report of the Canadian plant disease surveyCan. Plant Dis. Surv.365253

  • CreteR.ChiangM.S.1980Screening brassicas for resistance to clubroot, Plasmodiophora brassicae WorCan. Plant Dis. Surv.601719

  • DhingraO.D.SinclairJ.B.1985Basic plant pathology methods. CRC Press Boca Raton FL

  • DiederichsenE.FrauenM.LindersE.G.A.HatakeyemaK.HiraiM.2009Status and perspectives of clubroot resistance breeding in crucifer cropsJ. Plant Growth Regul.28265281

    • Search Google Scholar
    • Export Citation
  • DixonG.R.1996Repression of the morphogenesis of Plasmodiophora brassicae Wor. by boron. A reviewActa Hort.407393401

  • DixonG.R.2006The biology of Plasmodiophora brassicae Wor. A review of recent advancesActa Hort.706271282

  • DixonG.R.2009Plasmodiophora brassicae in its environmentJ. Plant Growth Regul.28212228

  • Dokken-BouchardF.L.BouchardA.J.IppolitoJ.PengG.StrelkovS.E.KirkhamC.L.KutcherH.R.2010Detection of Plasmodiophora brassicae in Saskatchewan, 2008Can. Plant Dis. Surv.90126

    • Search Google Scholar
    • Export Citation
  • DonaldE.C.PorterI.J.2004A sand-solution culture technique used to observe the effect of calcium and pH on root hair and cortical stages of infection by Plasmodiophora brassicae. AustralPlant Pathol.33585589

    • Search Google Scholar
    • Export Citation
  • DonaldE.C.PorterI.J.2009Integrated control of clubrootJ. Plant Growth Regul.28289303

  • DonaldE.C.PorterI.J.FaggianR.LancasterR.A.2006An integrated approach to the control of clubroot in vegetable brassica cropsActa Hort.706283300

    • Search Google Scholar
    • Export Citation
  • EinhornG.BochowH.1990The effects of temperature and pH value on the pathogenesis of Plasmodiophora brassicae Wor., the causal agent of clubrootArch. Phytopathol. Pflanzenschutz26131138

    • Search Google Scholar
    • Export Citation
  • Environment Canada2011Canadian Weather. 27 Dec. 2011. <http://www.weatheroffice.gc.ca/canada_e.html >

  • FaggianR.StrelkovS.E.2009Detection and measurement of Plasmodiophora brassicaeJ. Plant Growth Regul.28282288

  • GossenB.D.AdhikariK.K.C.McDonaldM.R.2011aEffects of temperature on infection and subsequent development of clubroot under controlled conditionsPlant Pathol.60doi: 10.1111/j.1365-3059.2011.02536.x (in press)

    • Search Google Scholar
    • Export Citation
  • GossenB.D.KasinathanH.AdhikariK.K.C.HwangS.F.McDonaldM.R.2011bImpact of temperature and pH on symptom development of Plasmodiophora brassicae in canola. Proc. 13th Intl. Rapeseed Congr. Prague Czech Republic 5–9 June 2011. p. 1218–1221

  • HildebrandP.D.McRaeK.B.1998Control of clubroot caused by Plasmodiophora brassicae with non-ionic surfactantsCan. J. Plant Pathol.20111

    • Search Google Scholar
    • Export Citation
  • HiraiM.2006Genetic analysis of clubroot resistance in brassica cropsBreed. Sci.56223229

  • HiraiM.HarudaT.KuboN.TsukadaM.SuwabeK.MatsumotoS.2003A novel locus for clubroot resistance in Brassica rapa and its linkage markersTheor. Appl. Genet.108639643

    • Search Google Scholar
    • Export Citation
  • HowardR.J.StrelkovS.E.HardingM.W.2010Clubroot of cruciferous crops – New perspective on an old diseaseCan. J. Plant Pathol.324357

  • KarlingJ.S.1968The Plasmodiophorales: Including a complete host index bibliography and a description of diseases caused by species of this order. 2nd ed. Hafner New York

  • KobrigerK.M.HagedornD.J.1983Determination of bean root rot potential in vegetable production fields of Wisconsin’s Central SandsPlant Dis.67177178

    • Search Google Scholar
    • Export Citation
  • KroetschD.J.GengX.ChangS.X.SauretteD.D.2011Organic soils of Canada: Part 1. Wetland organic soilsCan. J. Soil Sci.91807822

  • KuginukiY.YoshikawaH.HiraiM.1999Variation in virulence of Plasmodiophora brassicae in Japan tested with clubroot-resistant cultivars of chinese cabbage (Brassica rapa L. ssp. pekinensis)Eur. J. Plant Pathol.105327332

    • Search Google Scholar
    • Export Citation
  • LoughtonA.BakkerR.1994Cruciferae family cultivar trials. Horticultural Experimental Station (H.R.I.O.), Simcoe, ON, CanadaVegetable Cultivar Trials1272429

    • Search Google Scholar
    • Export Citation
  • LundR.E.1975Tables for an approximate test for outliers in linear modelsTechometrics17473476

  • Manzanares-DauleuxM.J.DivaretL.BaronF.ThomasG.2001Assessment of biological and molecular variability between field isolates of Plasmodiophora brassicaePlant Pathol.50165173

    • Search Google Scholar
    • Export Citation
  • McDonaldM.R.WesterveldS.M.2008Temperature prior to harvest influences the incidence and severity of clubroot on two Asian brassica vegetablesHortScience4315091513

    • Search Google Scholar
    • Export Citation
  • McDonaldM.R.JanseS.Vander KooiK.2009Muck vegetable cultivar and research reports—Weather data. 59:9–16. 31 Jan. 2011. <http://www.uoguelph.ca/muckcrop>

  • McDonaldM.R.JanseS.Vander KooiK.2010Muck vegetable cultivar and research reports—Weather data. 60:9–16. 31 Jan. 2011. <http://www.uoguelph.ca/muckcrop>

  • MitaniS.SugimotoK.HayashiH.TakiiY.OhshimaT.MatsuoN.2003Effects of cyazofamid against Plasmodiophora brassicae Woronin on chinese cabbagePest Manag. Sci.59287293

    • Search Google Scholar
    • Export Citation
  • MonteithJ.1924Relation of soil temperature and soil moisture to infection by Plasmodiophora brassicaeJ. Agric. Res.28549561

  • MyersD.F.CampbellR.N.1985Lime and the control of clubroot of crucifers: Effects of pH, calcium, magnesium, and their interactionsPhytopathology75670673

    • Search Google Scholar
    • Export Citation
  • MyersD.F.CampbellR.N.GreatheadA.S.1981Clubroot of brassicas in California: Soils respond differently to lime for clubroot controlPhytopathology7110051006

    • Search Google Scholar
    • Export Citation
  • NaikiT.DixonG.R.1987The effects of chemicals on developmental stages of Plasmodiophora brassicae (clubroot)Plant Pathol.36316327

  • NiwaR.KumeiT.NomuraY.YoshidaS.OsakiM.EzawaT.2007Increase in soil pH due to Ca-rich organic matter application causes suppression of the clubroot disease of crucifersSoil Biol. Biochem.39778785

    • Search Google Scholar
    • Export Citation
  • Ontario Ministry of Agriculture Food and Rural Affairs2010aVegetables: Area Production and Farm Value of Specified Commercial Vegetable Crops Ontario 2009. 27 Dec. 2011. <http://www.omafra.gov.on.ca/english/stats/hort/veg_all09-10.pdf>

  • Ontario Ministry of Agriculture Food and Rural Affairs2010bVegetable production recommendations 2010–2011. Publ. 363 Queen's Printer for Ontario Toronto ON Canada

  • PengG.McGregorL.LahlaliR.GossenB.G.HwangS.F.AdhikariK.K.C.StrelkovS.E.McDonaldM.R.2011Potential biocontrol of clubroot on canola crucifer vegetable cropsPlant Pathol.60566574

    • Search Google Scholar
    • Export Citation
  • PiaoZ.RamchiaryN.2009Genetics of clubroot resistance in Brassica speciesJ. Plant Growth Regul.28252264

  • ReyesA.A.DavidsonT.R.MarksC.F.1974Races, pathogenicity and chemical control of Plasmodiophora brassicae in OntarioPhytopathology64173177

    • Search Google Scholar
    • Export Citation
  • SharmaK.GossenB.D.McDonaldM.R.2011aEffect of temperature on primary infection by Plasmodiophora brassicae and initiation of clubroot symptomsPlant Pathol.60830838

    • Search Google Scholar
    • Export Citation
  • SharmaK.GossenB.D.McDonaldM.R.2011bEffect of temperature on cortical infection by Plasmodiophora brassicae and clubroot severityPhytopathology10114241432

    • Search Google Scholar
    • Export Citation
  • StrelkovS.E.TewariJ.P.SmithE.Smith-DegenhardtE.2006Characterization of Plasmodiophora brassicae populations from Alberta, CanadaCan. J. Plant Pathol.28467474

    • Search Google Scholar
    • Export Citation
  • SuzukiK.SugimotoK.HayashiH.KomyojiT.1995Biological mode of action of fluazinam, a new fungicide for chinese cabbage clubrootPhytopathol. Soc. Jpn.61395398

    • Search Google Scholar
    • Export Citation
  • TewariJ.P.StrelkovS.E.OrchardD.HartmanM.LangeR.M.TurkingtonT.K.2005Identification of clubroot of crucifers on canola (Brassica napus) in AlbertaCan. J. Plant Pathol.27143144

    • Search Google Scholar
    • Export Citation
  • ThumaB.A.RoweR.C.MaddenL.V.1983Relationships of soil temperature and moisture to clubroot (Plasmodiophora brassicae) severity on radish in organic soilPlant Dis.67758762

    • Search Google Scholar
    • Export Citation
  • TremblayN.BélecC.CoulombeJ.GodinC.2005Evaluation of calcium Cyanamid and liming for control of clubroot disease in cauliflowerCrop Protection24798803

    • Search Google Scholar
    • Export Citation
  • WellmanF.L.1930Clubroot of crucifers. U.S. Dept. Agr. Tech. Bul. No. 18

  • XueS.CaoT.HowardR.J.HwangS.F.StrelkovS.E.2008Isolation and variation in virulence of single-spore isolates of Plasmodiophora brassicae from CanadaPlant Dis.92456462

    • Search Google Scholar
    • Export Citation

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Contributor Notes

Funding was provided by the Agriculture Adaptation Council through the support of the Fresh Vegetable Growers of Ontario and by the Ontario Ministry of Agriculture, Food and Rural Affairs/University of Guelph Plant program.We thank Laura Riches, Cathy Bakker, and staff at Muck Crops Research Station and Simcoe Research Station for their assistance. Also, thanks to Stephen Strelkov (University of Alberta, Edmonton, AB, Canada) for conducting pathotype assessments and to Michael Tesfaendrias and Abhinandan Deora for clubroot resting spore quantifications.

Corresponding author. E-mail: mrmcdona@uoguelph.ca.

  • View in gallery

    Comparison of cabbage head characteristics: head shape, width, core size, core width and length, internal color of clubroot-resistant green cabbage cultivars and the susceptible cultivar Bronco untreated and treated with fluazinam fungicide, grown on mineral soils, near Simcoe in 2010. The fungicide fluazinam was applied at a rate of 0.025 g (0.00088 fl oz) per plant in 100 mL (3.38 fl oz) of water at the base of each plant of the susceptible standard cultivar Bronco immediately after transplanting. The rate of fluazinam was 0.7 kg·ha−1 (0.62 lb/acre).

  • AdhikariK.K.C.2010Effect of temperature biofungicides and fungicides on clubroot of selected Brassica crops. University of Guelph Guelph ON Canada Master’s Thesis

  • CaoT.ManoliiV.P.HwangS.F.HowardR.J.StrelkovS.E.2009Virulence and spread of Plasmodiophora brassicae (clubroot) in Alberta, CanadaCan. J. Plant Pathol.31321329

    • Search Google Scholar
    • Export Citation
  • CheahL.H.GowersS.MarshA.T.2006Clubroot control using brassica break cropsActa Hort.706329332

  • CheahL.H.KentG.GowersS.2001Brassica crops and a Streptomyces sp. as potential biocontrol for clubroot of brassicasN.Z. Plant Prot. Sci.548083

    • Search Google Scholar
    • Export Citation
  • CheahL.H.VeerakoneS.KentG.2000Biological control of clubroot on cauliflower with Trichoderma and Streptomyces sppN.Z. Plant Prot. Sci.531821

    • Search Google Scholar
    • Export Citation
  • ChuppC.1917Studies on clubroot of cruciferous plantsBul. Cornell Univ. Agr. Expt. Sta.387419452

  • ColhounJ.1952Factors affecting the incidence of club root disease of BrassicaeNature1692122

  • ColhounJ.1953A study of the epidemiology of club-root disease of BrassicaeAnn. Appl. Biol.40262283

  • ConnersI.L.ShoemakerR.A.CreelmanD.W.1956Thirty-sixth annual report of the Canadian plant disease surveyCan. Plant Dis. Surv.365253

  • CreteR.ChiangM.S.1980Screening brassicas for resistance to clubroot, Plasmodiophora brassicae WorCan. Plant Dis. Surv.601719

  • DhingraO.D.SinclairJ.B.1985Basic plant pathology methods. CRC Press Boca Raton FL

  • DiederichsenE.FrauenM.LindersE.G.A.HatakeyemaK.HiraiM.2009Status and perspectives of clubroot resistance breeding in crucifer cropsJ. Plant Growth Regul.28265281

    • Search Google Scholar
    • Export Citation
  • DixonG.R.1996Repression of the morphogenesis of Plasmodiophora brassicae Wor. by boron. A reviewActa Hort.407393401

  • DixonG.R.2006The biology of Plasmodiophora brassicae Wor. A review of recent advancesActa Hort.706271282

  • DixonG.R.2009Plasmodiophora brassicae in its environmentJ. Plant Growth Regul.28212228

  • Dokken-BouchardF.L.BouchardA.J.IppolitoJ.PengG.StrelkovS.E.KirkhamC.L.KutcherH.R.2010Detection of Plasmodiophora brassicae in Saskatchewan, 2008Can. Plant Dis. Surv.90126

    • Search Google Scholar
    • Export Citation
  • DonaldE.C.PorterI.J.2004A sand-solution culture technique used to observe the effect of calcium and pH on root hair and cortical stages of infection by Plasmodiophora brassicae. AustralPlant Pathol.33585589

    • Search Google Scholar
    • Export Citation
  • DonaldE.C.PorterI.J.2009Integrated control of clubrootJ. Plant Growth Regul.28289303

  • DonaldE.C.PorterI.J.FaggianR.LancasterR.A.2006An integrated approach to the control of clubroot in vegetable brassica cropsActa Hort.706283300

    • Search Google Scholar
    • Export Citation
  • EinhornG.BochowH.1990The effects of temperature and pH value on the pathogenesis of Plasmodiophora brassicae Wor., the causal agent of clubrootArch. Phytopathol. Pflanzenschutz26131138

    • Search Google Scholar
    • Export Citation
  • Environment Canada2011Canadian Weather. 27 Dec. 2011. <http://www.weatheroffice.gc.ca/canada_e.html >

  • FaggianR.StrelkovS.E.2009Detection and measurement of Plasmodiophora brassicaeJ. Plant Growth Regul.28282288

  • GossenB.D.AdhikariK.K.C.McDonaldM.R.2011aEffects of temperature on infection and subsequent development of clubroot under controlled conditionsPlant Pathol.60doi: 10.1111/j.1365-3059.2011.02536.x (in press)

    • Search Google Scholar
    • Export Citation
  • GossenB.D.KasinathanH.AdhikariK.K.C.HwangS.F.McDonaldM.R.2011bImpact of temperature and pH on symptom development of Plasmodiophora brassicae in canola. Proc. 13th Intl. Rapeseed Congr. Prague Czech Republic 5–9 June 2011. p. 1218–1221

  • HildebrandP.D.McRaeK.B.1998Control of clubroot caused by Plasmodiophora brassicae with non-ionic surfactantsCan. J. Plant Pathol.20111

    • Search Google Scholar
    • Export Citation
  • HiraiM.2006Genetic analysis of clubroot resistance in brassica cropsBreed. Sci.56223229

  • HiraiM.HarudaT.KuboN.TsukadaM.SuwabeK.MatsumotoS.2003A novel locus for clubroot resistance in Brassica rapa and its linkage markersTheor. Appl. Genet.108639643

    • Search Google Scholar
    • Export Citation
  • HowardR.J.StrelkovS.E.HardingM.W.2010Clubroot of cruciferous crops – New perspective on an old diseaseCan. J. Plant Pathol.324357

  • KarlingJ.S.1968The Plasmodiophorales: Including a complete host index bibliography and a description of diseases caused by species of this order. 2nd ed. Hafner New York

  • KobrigerK.M.HagedornD.J.1983Determination of bean root rot potential in vegetable production fields of Wisconsin’s Central SandsPlant Dis.67177178

    • Search Google Scholar
    • Export Citation
  • KroetschD.J.GengX.ChangS.X.SauretteD.D.2011Organic soils of Canada: Part 1. Wetland organic soilsCan. J. Soil Sci.91807822

  • KuginukiY.YoshikawaH.HiraiM.1999Variation in virulence of Plasmodiophora brassicae in Japan tested with clubroot-resistant cultivars of chinese cabbage (Brassica rapa L. ssp. pekinensis)Eur. J. Plant Pathol.105327332

    • Search Google Scholar
    • Export Citation
  • LoughtonA.BakkerR.1994Cruciferae family cultivar trials. Horticultural Experimental Station (H.R.I.O.), Simcoe, ON, CanadaVegetable Cultivar Trials1272429

    • Search Google Scholar
    • Export Citation
  • LundR.E.1975Tables for an approximate test for outliers in linear modelsTechometrics17473476

  • Manzanares-DauleuxM.J.DivaretL.BaronF.ThomasG.2001Assessment of biological and molecular variability between field isolates of Plasmodiophora brassicaePlant Pathol.50165173

    • Search Google Scholar
    • Export Citation
  • McDonaldM.R.WesterveldS.M.2008Temperature prior to harvest influences the incidence and severity of clubroot on two Asian brassica vegetablesHortScience4315091513

    • Search Google Scholar
    • Export Citation
  • McDonaldM.R.JanseS.Vander KooiK.2009Muck vegetable cultivar and research reports—Weather data. 59:9–16. 31 Jan. 2011. <http://www.uoguelph.ca/muckcrop>

  • McDonaldM.R.JanseS.Vander KooiK.2010Muck vegetable cultivar and research reports—Weather data. 60:9–16. 31 Jan. 2011. <http://www.uoguelph.ca/muckcrop>

  • MitaniS.SugimotoK.HayashiH.TakiiY.OhshimaT.MatsuoN.2003Effects of cyazofamid against Plasmodiophora brassicae Woronin on chinese cabbagePest Manag. Sci.59287293

    • Search Google Scholar
    • Export Citation
  • MonteithJ.1924Relation of soil temperature and soil moisture to infection by Plasmodiophora brassicaeJ. Agric. Res.28549561

  • MyersD.F.CampbellR.N.1985Lime and the control of clubroot of crucifers: Effects of pH, calcium, magnesium, and their interactionsPhytopathology75670673

    • Search Google Scholar
    • Export Citation
  • MyersD.F.CampbellR.N.GreatheadA.S.1981Clubroot of brassicas in California: Soils respond differently to lime for clubroot controlPhytopathology7110051006

    • Search Google Scholar
    • Export Citation
  • NaikiT.DixonG.R.1987The effects of chemicals on developmental stages of Plasmodiophora brassicae (clubroot)Plant Pathol.36316327

  • NiwaR.KumeiT.NomuraY.YoshidaS.OsakiM.EzawaT.2007Increase in soil pH due to Ca-rich organic matter application causes suppression of the clubroot disease of crucifersSoil Biol. Biochem.39778785

    • Search Google Scholar
    • Export Citation
  • Ontario Ministry of Agriculture Food and Rural Affairs2010aVegetables: Area Production and Farm Value of Specified Commercial Vegetable Crops Ontario 2009. 27 Dec. 2011. <http://www.omafra.gov.on.ca/english/stats/hort/veg_all09-10.pdf>

  • Ontario Ministry of Agriculture Food and Rural Affairs2010bVegetable production recommendations 2010–2011. Publ. 363 Queen's Printer for Ontario Toronto ON Canada

  • PengG.McGregorL.LahlaliR.GossenB.G.HwangS.F.AdhikariK.K.C.StrelkovS.E.McDonaldM.R.2011Potential biocontrol of clubroot on canola crucifer vegetable cropsPlant Pathol.60566574

    • Search Google Scholar
    • Export Citation
  • PiaoZ.RamchiaryN.2009Genetics of clubroot resistance in Brassica speciesJ. Plant Growth Regul.28252264

  • ReyesA.A.DavidsonT.R.MarksC.F.1974Races, pathogenicity and chemical control of Plasmodiophora brassicae in OntarioPhytopathology64173177

    • Search Google Scholar
    • Export Citation
  • SharmaK.GossenB.D.McDonaldM.R.2011aEffect of temperature on primary infection by Plasmodiophora brassicae and initiation of clubroot symptomsPlant Pathol.60830838

    • Search Google Scholar
    • Export Citation
  • SharmaK.GossenB.D.McDonaldM.R.2011bEffect of temperature on cortical infection by Plasmodiophora brassicae and clubroot severityPhytopathology10114241432

    • Search Google Scholar
    • Export Citation
  • StrelkovS.E.TewariJ.P.SmithE.Smith-DegenhardtE.2006Characterization of Plasmodiophora brassicae populations from Alberta, CanadaCan. J. Plant Pathol.28467474

    • Search Google Scholar
    • Export Citation
  • SuzukiK.SugimotoK.HayashiH.KomyojiT.1995Biological mode of action of fluazinam, a new fungicide for chinese cabbage clubrootPhytopathol. Soc. Jpn.61395398

    • Search Google Scholar
    • Export Citation
  • TewariJ.P.StrelkovS.E.OrchardD.HartmanM.LangeR.M.TurkingtonT.K.2005Identification of clubroot of crucifers on canola (Brassica napus) in AlbertaCan. J. Plant Pathol.27143144

    • Search Google Scholar
    • Export Citation
  • ThumaB.A.RoweR.C.MaddenL.V.1983Relationships of soil temperature and moisture to clubroot (Plasmodiophora brassicae) severity on radish in organic soilPlant Dis.67758762

    • Search Google Scholar
    • Export Citation
  • TremblayN.BélecC.CoulombeJ.GodinC.2005Evaluation of calcium Cyanamid and liming for control of clubroot disease in cauliflowerCrop Protection24798803

    • Search Google Scholar
    • Export Citation
  • WellmanF.L.1930Clubroot of crucifers. U.S. Dept. Agr. Tech. Bul. No. 18

  • XueS.CaoT.HowardR.J.HwangS.F.StrelkovS.E.2008Isolation and variation in virulence of single-spore isolates of Plasmodiophora brassicae from CanadaPlant Dis.92456462

    • Search Google Scholar
    • Export Citation
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