Management of clubroot (Plasmodiophora brassicae) on canola (Brassica napus) in western Canada

Abstract

Clubroot, caused by Plasmodiophora brassicae, has emerged as a serious disease threatening the canola production industry in western Canada. This review summarizes results from studies, conducted since 2007, on the development of effective strategies for the management of clubroot in canola. Several options have been proposed for the control of this disease in infested fields, including liming the soil to increase soil pH, crop rotation with non-hosts and bait crops, manipulating the sowing date, sanitization of farm equipment, and the deployment of resistant cultivars, all aimed at reducing the severity of infection. Research began by assessing existing clubroot treatments, originally developed for the cole crop vegetable industry, for their applicability to canola production systems. Although these treatments provide good levels of clubroot reduction for the intensive production of short-season brassica vegetables, most are not economically feasible for the large-scale production of canola, which requires protection over a greater field acreage. Genetic resistance to P. brassicae has been shown to be a practical option for the management of clubroot on canola, but resistance stewardship, coupled with crop rotation and appropriate cultural practices, will be required to maintain the performance and durability of genetic resistance. Pathogen resting spores can be disseminated on infested soil carried on both machinery and seed. Efforts to minimize spread of the pathogen between canola fields have focused largely on the sanitization of field equipment and seed.

Résumé

La hernie, causée par Plasmodiophora brassicae, s’est révélée une maladie grave qui menace la production du canola dans l’Ouest canadien. Cette revue résume les résultats d’études menées depuis 2007 sur l’élaboration de stratégies efficaces visant la gestion de la hernie sur le canola. Diverses options ont été proposées pour lutter contre cette maladie dans les champs infestés, y compris le chaulage des sols pour en accroître le pH, la rotation des cultures avec des cultures non hôtes et des cultures-appâts, la modification des dates de semis, le nettoyage de l’équipement agricole et l’utilisation de cultivars résistants, options qui toutes visent à réduire la gravité de l’infection. La recherche s’est d’abord concentrée sur l’évaluation des traitements courants contre la hernie, originalement développés pour la culture du chou, pour vérifier dans quelle mesure ils étaient applicables à la production du canola. Bien que ces traitements permettent de réduire significativement la hernie chez les légumes à cycle court du genre Brassica, la majorité n’est pas économiquement réalisable à grande échelle pour des cultures comme le canola qui requiert une protection sur des superficies beaucoup plus grandes. La résistance génétique à P. brassicae s’est avérée pratique en tant que solution visant la gestion de la hernie chez le canola, mais l’intendance de la résistance, associée à la rotation des cultures et aux pratiques culturales appropriées, sera nécessaire pour en maintenir la performance et la longévité. Les spores de repos des agents pathogénes peuvent être disséminées par le sol infesté transporté par la machinerie et les semences. Les efforts déployés pour minimiser la propagation des agents pathogénes entre les champs de canola ont surtout porté sur le nettoyage de l’équipement agricole et des semences.

Keywords:

• baiting crops
• crop rotation
• fumigants
• fungicides
• resistance
• sanitization
• seeding date
• soil amendments

Mots clés:

• Cultures-appâts
• rotation des cultures
• fumigants
• agents fongicides
• résistance
• nettoyage
• date des semis
• amendements des sols

Introduction

Clubroot, caused by Plasmodiophora brassicae Woronin (Fig. 1), has recently become an economically important disease of canola (Brassica napus L.) on the Canadian Prairies (Hwang et al. 2012b). The disease has spread from an original outbreak near Edmonton in 2003 (Tewari et al. 2005) to more than 1000 fields throughout the province of Alberta by 2012, and has also been confirmed in canola fields in the neighbouring provinces of Saskatchewan (Strelkov et al. 2012) and Manitoba (Cao et al. 2009; S.E. Strelkov unpublished data). This has led to concerns that clubroot will spread across the Prairies and could have a huge negative impact on Canadian canola production, since estimated yield losses in severely infected canola crops have ranged from 30% to 100% (Strelkov et al. 2007; Hwang et al. 2011a). Also, each infected canola plant has the potential to return up to 8 × 10⁸ resting spores to the soil (Hwang et al. 2012a), with a half-life for the resting spores of about 4 years (Wallenhammar 1996; Hwang et al. 2013). This epidemic has resulted in legislation in Alberta for the control of P. brassicae under the Agricultural Pests Act (Alberta Clubroot Management Committee 2010). In response to this significant disease threat, a coordinated research effort was launched in Canada aimed at developing a better understanding of the strategies needed for the effective management of clubroot in the canola production systems of the Prairies.

Fig. 1. (Colour online) A, Clubroot foliar symptoms on young susceptible canola plants, showing stunting, wilting and premature yellowing caused by Plasmodiophora brassicae infection; B, susceptible plant at the flowering stage showing wilting; and C, galls on severely infected roots.

Crop rotations based on standard agronomic recommendations for western Canada (one year of canola in every four) are unlikely to have a substantial impact on resting spore populations of P. brassicae (Strelkov et al. 2006) because viable propagules can persist in the soil for more than 15 years (Wallenhammar 1996). Even substantially longer rotations may not be effective because the 330 genera and 3700 species of the family Brassicaceae are all potential hosts of P. brassicae (Dixon 2009). Many common weed species in the region are susceptible to infection by this parasite, including wild mustard (B. kaber (DC.) L.C. Wheeler), shepherd’s purse (Capsella bursa-pastoris (L.) Medik.), stinkweed (Thlaspi arvense L.), and white mustard (B. hirta Moench) (Howard et al. 2010).

The density of viable clubroot resting spores in the soil affects the progress of initial infections, the timing of symptom onset and development, and the probability of multiple infections. High concentrations of resting spores contribute to earlier development of larger galls. Large galls have a more deleterious effect on crop production than small galls due to increased disruption of water and nutrient flows in the host. Also, older plants are thought to be less susceptible to clubroot (Horiuchi & Hori 1980); therefore, delaying infection and symptom development may reduce the impact of clubroot on crop production, which warrants more research.

Several approaches have been recommended for the management of clubroot in infested fields, including the application of lime to increase soil pH (Murakami et al. 2002), bait crops to reduce the concentration of pathogen resting spores (Kroll et al. 1984; Ikegami 1985; Murakami et al. 2001), manipulation of seeding date to minimize infection (Gossen et al. 2009, 2012), and deployment of resistant cultivars (Diederichsen et al. 2009). Also, sanitization of field equipment/machinery to prevent initial infestation of fields has been proposed (Howard et al. 2010), because the field-to-field spread of P. brassicae is usually initiated outwards from the field entrance. This could be related to the movement of infested soil and plant debris on farming equipment (Cao et al. 2009) or by cattle that are fed near gateways (Dixon, personal communication). Several of these management options, which historically have been used in the production of vegetable crops, are not practical nor cost effective in the extensive cropping systems used for canola (Strelkov et al. 2011; Gossen et al. 2013b), especially when the concentrations of resting spores in the soil are high. Crop rotation, which is already an important component of most crop disease management systems for the Canadian Prairies, is complicated by the fact that the pathogen can survive as resting spores in the soil for long periods (Wallenhammar 1996), and many common Brassica weed species on the Canadian Prairies may act as hosts for the pathogen. Also, large-scale agriculture and scattered land tenure, which necessitates that individual producers move farming equipment over long distances, and tight crop rotation schedules, have promoted the proliferation and dispersal of P. brassicae.

This review focuses on recent studies on clubroot management in canola, including the application of soil amendments, soil fumigation, seed treatments, cultural practices such as bait crops, the manipulation of seeding dates, sanitization of machinery, and the development of P. brassicae – resistant cultivars.

Soil amendments

Lime

Clubroot development is often favoured by acidic soil conditions (Karling 1968; Myers & Campbell 1985; Rastas et al. 2012). Thus, maintaining a pH of 7.2 or higher with application of various soil amendments, especially forms of lime, has been used as a strategy aimed at reducing clubroot in high-value horticultural crops (Murakami et al. 2002). Research into methods to manage clubroot on canola initially focused on the application of soil amendments that increased soil pH.

Lime is available in various forms: agricultural lime (calcium carbonate and calcitic lime), dolomitic lime (calcium and magnesium carbonate), hydrated lime (calcium hydroxide) and quicklime (calcium oxide). Agricultural and dolomitic limes are relatively slow-acting, whereas hydrated lime and quicklime are more reactive and so act much more quickly to raise the soil pH. Application of slow-acting forms of lime should be made in the autumn months (September to December in western Canada) to allow time for the amendments to disperse into the soil profile prior to spring planting. Also, substantial quantities have to be applied because a large proportion of the material applied will not yet have dispersed or dissolved into an active form. Fast-acting limes are more suitable for spring application. Finely ground amendments are potentially more reactive than coarse formulations and so they alter the pH more rapidly. Annual applications of soil amendments may be required to raise the pH and to maintain it at desirable levels during the growing season (Hwang et al. 2011c).

The impact of soil amendment with lime, wood ash and calcium cyanamide on clubroot severity and seed yield was assessed in field trials on canola in central Alberta over several growing seasons. Applications of calcium carbonate at 5.0 or 7.5 t ha⁻¹ or wood ash at 7.5 t ha⁻¹ increased plant cover and height, even under heavy inoculum pressure (Hwang et al. 2008). Calcium carbonate reduced clubroot severity and increased yield compared with the non-treated control, but the disease reduction and yield increase were too small to justify the expense of lime application (Hwang et al. 2011c). Moreover, the results were not consistent across years and soil types. Other researchers also concluded that this option is not practical or cost effective for use in canola production, because several tons of lime per hectare are required to increase the pH of an acidic soil to a level at which clubroot severity is reduced (Myers & Campbell 1985; Webster & Dixon 1991; Murakami et al. 2002). The enormous quantities of lime or wood ash needed to treat the thousands of hectares of clubroot-infested fields in Alberta would be impractical to source, transport and apply. Finally, assessments of the soil pH in infested canola fields in Alberta demonstrated that there was only a weak correlation between soil pH and clubroot severity (Gossen et al. 2014, 2013a). Moreover, an early study, which has been largely overlooked, indicated that application of lime might not be effective if temperature and soil moisture conditions are favourable for infection by P. brassicae (Colhoun 1953). A recent study on the interaction of soil pH and temperature on clubroot development under controlled conditions supported this conclusion. It demonstrated that, although alkaline pH suppressed clubroot infection, substantial levels of clubroot could still develop where soil temperature and moisture conditions were conducive to infection (Gossen et al. 2013a). Highly conducive conditions for infection, such as warm, wet soils and high inoculum density (Colhoun 1953), might be the cause for failures in clubroot reduction that are occasionally associated with liming (Webster & Dixon 1991; McDonald et al. 2004; Kasinathan 2012).

Calcium cyanamide

Calcium cyanamide is a synthetic nitrogen fertilizer, which has been associated with the amelioration of clubroot of brassicas for many years (Walker & Larson 1935;  Karling 1968). The granulated form of this fertilizer, containing 19.8% N and >50% lime as CaO, is regularly used in many parts of the European Union where it has been sold as a nitrogen fertilizer (Klasse 1996). Calcium cyanamide, when in contact with soil moisture, decomposes to hydrogen cyanamide and hydrated lime. Following this process, the hydrogen cyanamide further decomposes to urea and dicyandiamide. The intermediate, hydrogen cyanamide, is known to possess properties associated with reductions in the activity of fungal pathogens; however, the lime and calcium components of the product also have reported effects on P. brassicae (Klasse 1996). More importantly, the application of calcium cyanamide increases the soil microbial populations, which might act as antagonists, thus suppressing P. brassicae populations (Dixon 2012a, 2012b).

Dixon (2009) summarized extensive research that has been done on the interactions between calcium cyanamide, P. brassicae and other soil microbes, demonstrating that calcium cyanamide and its degradation products – calcium and nitrate nitrogen – are associated with the reduced viability of P. brassicae. In Canada, Hwang et al. (2011c) studied the effect of calcium cyanamide on clubroot severity in canola under field conditions, and reported no benefit of calcium cyanamide on the reduction of clubroot severity, or in increasing seedling emergence or yield. The effect of calcium cyanamide is influenced by the particle size, methods of application and depth. In the study by Hwang et al. (2011c), calcium cyanamide was spread on the soil surface at a rate of 0.5 or 1.0 t/ha and then incorporated into the soil to a depth of 8 cm with a rototiller; additional studies, examining different methods and rates of application, may be warranted to fully explore the potential of this product for the management of clubroot on canola.

Boron

Boron has been recommended for the reduction of clubroot severity on vegetable crops for more than 70 years (O’Brien & Dennis 1936; Dixon 2009). It inhibits the development from plasmodium to sporangium during root hair infection (Webster & Dixon 1991), in addition to having positive effects on the growth of many Brassica species, which have high requirements for boron. A significant reduction in clubroot severity on canola was observed when boron was applied at a rate of 4 kg ha⁻¹ in a field trial; however, higher rates, while effectively reducing clubroot severity, were also phytotoxic (Deora et al. 2011). Subsequent field assessments across a wide range of soil types and environments indicated that reduction in clubroot severity was more consistent in soils with very high organic matter content than in the typical mineral soils found on the Canadian Prairies (B.D. Gossen, unpublished data). The effects of boron on clubroot management are discussed in more detail in a paper on clubroot risk that appears in this volume (Gossen et al. 2014).

Soil fumigants

There may be situations where eradicating resting spore populations at a field entrance or at newly established infection foci in a field may eliminate P. brassicae from a new site and thereby prevent it from becoming established in a region. Therefore, soil fumigants are currently being evaluated for efficacy against clubroot on canola under field conditions in central Alberta. Application of Vapam, a commercial aqueous formulation of metham-sodium (dithiocarbamate; sodium N-methyldithiocarbamate), and several other fumigants has been shown to reduce clubroot severity on cabbage (B. oleracea L. var. capitata) (White & Buczacki 1977). When in contact with moist soil, Vapam is largely converted to methyl isothiocyanate, a volatile compound that diffuses as a gaseous fumigant through the soil and has considerable nematicidal, fungicidal and phytocidal activity (Smelt & Leistra 1974). Preliminary tests conducted in Alberta showed that the application of Vapam HL^® (metam sodium 42%) one week prior to planting reduced clubroot severity on canola (Fig. 2). In trials under controlled conditions, application of Vapam HL^® at 0.4–1.6 mL L⁻¹ soil resulted in a 12–16-fold reduction in primary and secondary infection and clubroot severity in canola seedlings (S.F. Hwang unpublished data; Fig. 2). Moreover, the residual effect of Vapam HL^® at the higher rates (0.8 and 1.6 mL L⁻¹ soil) reduced clubroot development and improved plant health in a subsequent crop compared with the non-treated control. Soil moisture influences the efficacy of Vapam. Application of Vapam HL^® at soil moisture levels in the range of 10–30% had a larger effect on both clubroot severity and plant growth than at lower soil moisture levels. Therefore, it appears that Vapam HL^® at a higher rate has potential utility for the eradication of isolated clubroot infestations in commercial canola fields. A downside of the application of metam-sodium, however, is that it may cause localized air pollution (Saeed et al. 2000). Thus, a standard method of application that limits the evaporation of the vapour (methyldithiocarbamate) will be required before any recommendation can be made to farmers.

Fig. 2. (Colour online) Effects of fumigation of clubroot-infested soil with three different concentrations of Vapam HL®, compared with an unfumigated control, on growth of canola under greenhouse conditions (top panel). Effects of soil fumigation at 1000 L ha⁻¹ on growth of canola under field conditions near Edmonton, AB (bottom panel). Note stunting, sparse growth and delayed flowering of plants grown in the unfumigated soil where clubroot infection was severe.

Seed cleaning and fungicidal treatments

Seed contaminated with soil containing spores of P. brassicae may represent a mechanism for long-distance spread of this pathogen (Warne 1943). A recent study demonstrated the potential for dissemination of P. brassicae resting spores as external contaminants on the seed of canola and other crops, including seed of spring wheat (Triticum aestivum L.) and tubers of potato (Solanum tuberosum L.) harvested from clubroot-infested fields. Seed cleaning removed lumps of soil, crop residue and shrivelled seed, and thereby reduced the risk of transmission of clubroot with seed (Rennie et al. 2011).

The impact of fungicidal seed treatments on clubroot of canola was also investigated under greenhouse and field conditions in western Canada. Many of the fungicides assessed, including Dynasty^® 100FS (azoxystrobin), Helix Xtra^® (thiamethoxam + difenconazole + metalaxyl + fludioxonil), Prosper^™ FX (clothianidin + carbathiin + trifloxystrobin + metalaxyl), Vitavax^® RS (carbathiin + thiram) and Nebijin^® (flusulfamide), reduced infection on canola seedlings under greenhouse conditions, but had no effect on clubroot severity in heavily infested fields (Hwang et al. 2011c). It is possible that the amounts of these products on the seeds were insufficient to eliminate the large numbers of resting spores in the surrounding soil environment, which would still have been available to infect the seedlings after emergence. By contrast, Rod (1992) reported that fungicidal seed treatment may delay infection by P. brassicae and thereby reduce the severity of clubroot symptoms on affected plants. The author concluded, however, that seed treatments were not sufficiently active to reduce the impact of clubroot in heavily infested fields. Nonetheless, a prudent containment strategy for seed harvested from a clubroot-infested field would include seed cleaning and treatment with an effective fungicide.

Soil fungicides

Reductions in clubroot severity are also possible with the application of fungicides to the soil (Mitani et al. 2003). The use of fungicides for the control of clubroot on canola and other crops is discussed in more detail in an accompanying review (Peng et al. 2014). Nevertheless, a brief mention is made here of the studies undertaken in western Canada to assess the efficacy of chemical fungicides in reducing the severity of clubroot on canola, with the aim of providing farmers with additional disease management options. In field trials conducted in Alberta, pentachloronitrobenzene (PCNB, Terraclor® 75% WP) was incorporated into the soil prior to seeding, and shown to result in a significant reduction in clubroot severity (Hwang et al. 2008, Fig. 3). However, health concerns, the persistence of this product in the soil, and the costs associated with its application make it unlikely that PCNB will ever be an option for clubroot management in the large-scale field production of canola (Hwang et al. 2011c).

Fig. 3. (Colour online) Effects of calcium cyanamide, Terraclor® and Ranman® on growth of canola plots in a clubroot-infested field near Edmonton, AB. The superior performance of Terraclor® is indicated by more robust foliar growth compared with the other two soil treatments.

The efficacy of cyazofamid (Ranman® 400SC Agricultural Fungicide), which has a direct effect on resting spore germination, root hair infection and the formation of clubroot galls (Mitani et al. 2003), was also evaluated in Alberta (Hwang et al. 2008). Like PCNB, cyazofamid, when incorporated into the soil prior to seeding, significantly reduced the severity of clubroot in less heavily infested soils (Fig. 3). The application rates found to be effective, however, would be prohibitively expensive for treatment of canola crops in a commercial field setting.

Cultural controls

Disease avoidance

The most effective cultural control for management of clubroot is to ensure that fields remain free of the pathogen. Any activity that results in transport of soil or crop residues infested with P. brassicae from one point to another has the potential to disseminate the pathogen (Strelkov et al. 2011). A study on the distribution of infected plants within clubroot-infested fields showed that the incidence of infected plants was highest at the field entrances, and lower at distances of 150 m and 300 m from the entrance (Cao et al. 2009). This indicates that farm equipment laden with infested soil and crop debris was likely to be responsible for introducing the pathogen, so sanitization of infested equipment (discussed below) is a critically important component of disease avoidance strategies.

Another potential mechanism for the long-distance dissemination of P. brassicae is seed and tubers harvested from infested fields, which have been shown to carry detectable levels of resting spores (Rennie et al. 2011). Field trials which assessed the frequency of seed-to-seedling transmission of clubroot from resting spores inoculated onto canola seed have not resulted in clubroot symptoms in the susceptible canola crop or on highly susceptible hosts sown on the same site the following year (B.D. Gossen unpublished data). However, the success of transmission under greenhouse conditions (Rennie et al. 2011) still raises concerns that dissemination of the pathogen on seed may represent a viable mechanism for dispersal of clubroot disease. It is important to note that the movement of infested soil and crop residues on farm equipment, machinery and vehicles is a much more common and consistent mechanism of spread than seed-borne transmission. The amount of soil, and therefore the number of resting spores, carried on equipment far exceeds that found on even the most heavily infested seed lots. Nevertheless, transmission of resting spores on seed and tubers could lead to the dissemination of P. brassicae over longer distances than might typically be associated with the movement of farm machinery. This could also result in the introduction of novel races or pathotypes to a region where previously they were absent. The existence of multiple strains or pathotypes of P. brassicae is discussed in detail in an accompanying review (Strelkov & Hwang 2014). As such, the possibility of seed-borne transmission should not be ignored in the development of clubroot-containment strategies, and farmers should avoid planting self-saved/farm-saved common, untreated seeds harvested from clubroot-infested fields (Alberta Clubroot Management Committee 2010).

Another important potential mechanism of P. brassicae dispersal is irrigation water pumped from canals, creeks and reservoirs contaminated with runoff from clubroot-infested fields. Contaminated water could infest large areas of non-infested fields and should not be applied to plantings of cruciferous vegetables (Howard et al. 2010) or other susceptible crops such as canola. In fact, it could be argued that this practice should be discouraged for all agricultural fields given the longevity of clubroot resting spores in soil and the possibility that susceptible rotational crops could eventually be grown in these fields.

Similarly, resting spores can survive passage through livestock, so application of raw manure from animals that have been fed or pastured on clubroot-infected fodder onto clean fields should be avoided (Howard et al. 2010). Temperature and moisture content were shown to be important for the successful eradication of P. brassicae resting spores from composted residues infested with clubroot (Noble & Roberts 2004;  Fayolle et al. 2006; Wilchuk et al. 2011), although research on the effects of the composting process is limited and questions have been raised as to how the temperatures achieved in composting could destroy all of P. brassicae resting spores (G.R. Dixon personal communication).

Bait crops

Induction of resting spore germination in the absence of host plants has been proposed as a possible tool in the management of clubroot (Friberg et al. 2005). Resting spores of P. brassicae can survive for many years in the soil environment. However, following germination, they must quickly infect a host in order to ensure continued survival (Suzuki et al. 1992; Takahashi 1994). Also, the concentration of viable resting spores in the soil is an important factor in the subsequent development of P. brassicae epidemics (Murakami et al. 2002). For example, reduction of viable spore density to approximately 10⁴–10⁵ spores mL⁻¹ of soil was required to reduce the clubroot disease index to 50% of that observed at 10⁸ spores mL⁻¹ (Hwang et al. 2011b). However, extremely long rotations may be needed to reduce high inoculum concentrations to a level below a disease-causing threshold (Wallenhammar 1996; Donald & Porter 2009). Therefore, inducing resting spore germination in the absence of host plants to accelerate reduction in spore populations could be a useful component of an integrated clubroot management programme (Friberg et al. 2006).

Many plants can induce germination of resting spores of P. brassicae without becoming infected. A crop that stimulates resting spore germination (i.e. a bait crop) could be planted to reduce pathogen populations in heavily infested fields. Host crops, if they are killed before the formation of clubs and resting spores, could also act as bait crops. Root hair infection by P. brassicae has been reported in a wide range of non-brassica plant species, including common velvet-grass (Holcus lanatus L.), perennial ryegrass (Lolium perenne L.), Indian Cress (Tropaeolum majus L.) (Webb 1949; MacFarlane 1952) and strawberry (Fragaria ananassa Duch.) (Lugauskas et al. 2003). Subsequent cortical infection and development of resting spores have been reported in several non-cruciferous plant species, such as T. majus and beet (Beta vulgaris L.) (Ludwig-Müller et al. 1999). Root exudates of perennial ryegrass (Rod & Robak 1994), lettuce (Lactuca sativa L.) (Ikegami 1985; Robak 1996), leek (Allium ampeloprasum var. porrum (L.) Gay), rye (Secale cereale L.) and red clover (Trifolium pratense L.) induce resting spore germination (Friberg et al. 2006). Perennial ryegrass was effective in reducing the resting spore numbers in one study (Rod & Robak 1994), but was not effective in another (Robak 1996).

Studies in northern Europe using bait crops to stimulate germination of resting spores did not result in effective reductions in clubroot (Friberg et al. 2005, 2006). Moreover, the benefits of using non-host plants for baiting or in crop rotations came under question when fallow treatments without bait plants reduced resting spore levels to an extent similar to the most promising non-host crops (Ikegami 1985; Robak 1996). By contrast, a 5-year fallow period or the continuous cultivation of a clubroot-resistant Japanese radish (Raphanus sativus var. longipinnotu Bailey) resulted in a substantial decrease in resting spore populations (Ikegami 1985).

On the Canadian Prairies, the extensive scale of the clubroot epidemic on canola necessitates approaches that can be implemented across a large area, and bait crops were one of the few potential management options that met this requirement. However, environmental conditions and production systems on the Canadian Prairies are quite different from those in northern Europe or Japan, so information directly applicable to the Canadian situation was required to evaluate the potential for use of bait crops for clubroot management.

In a heavily infested commercial field in Alberta, clubroot incidence and severity on canola were lower following a cruciferous bait crop versus a non-cruciferous crop or a cereal (Ahmed et al. 2011). Similarly, when sequences of bait crops (canola, ryegrass and fallow treatments) were assessed, clubroot severity in the subsequent canola crop was lowest in the canola–fallow sequence. Clubroot severity was consistently high in the fallow–fallow sequence, but the results of the other sequences with canola were not as consistent across two repetitions of the experiment. The assessment of a bait crop at two other field sites in Alberta only had a small impact on resting spore populations and there was no effect on subsequent clubroot severity (Hwang et al. 2011b). Resting spore concentrations at these sites were about 1 × 10⁶ spores per g soil, so a small reduction in the spore load was difficult to detect and would not be expected to affect clubroot severity. Resistant cultivars also stimulate the germination of resting spores, but few or no viable spores are produced, and so this may result in a reduction in inoculum pressure (Hwang et al. 2011b). Long-term studies are needed to detect significant reductions in clubroot inoculum and severity in heavily infested field sites, and to evaluate whether bait crops could be useful at locations where inoculum levels are low to moderate. Nevertheless, Canadian results appear to support the conclusion of Friberg et al. (2006) that the impact of bait crops on inoculum potential and clubroot severity is too small and inconsistent to be useful for managing this disease in commercial fields.

Seeding date

Clubroot development is strongly favoured by high soil moisture (Karling 1968) and temperatures near 25 °C (Feng et al. 2010; Sharma et al. 2011). Hence, a key means of avoiding infection in canola and other long-season brassicas may be through the manipulation of the timing of seeding to minimize infection. Cool soil temperatures have been shown to inhibit pathogen development (Hwang et al. 2011a). Older plants have been shown to be less susceptible to infection, and the infection that does occur is less likely to affect yield (Hwang et al. 2011a). Early seeding dates reduced clubroot severity by 10–50% (only statistically significant at one of two sites) and increased yield by 30–58% (Gossen et al. 2012). Similar results were obtained by manipulating seeding date to minimize clubroot in Shanghai pak choy (B. rapa subsp. chinensis var. communis Tsen & Lee) and Chinese flowering cabbage (B. rapa subsp. chinensis var. utilis Tsen & Lee) over several years at sites in central Canada (McDonald & Westerveld 2008; Gossen et al. 2009; Adhikari et al. 2012). A study by Hwang et al. (2012a) reported that early seeding of canola reduced clubroot severity and increased yield, although it also reduced emergence. Previous research has indicated that younger canola seedlings are more susceptible to infection than older seedlings (Hwang et al. 2011a). A resistant cultivar exhibited few or no symptoms of clubroot when inoculated 10–25 days after seeding, but some plants became infected when they were inoculated at 5 days after seeding. The susceptibility of canola roots to infection by P. brassicae declines with increasing age, perhaps as a result of the thickening of cell walls (Mellano et al. 1970) and formation of other barriers that limit pathogen colonization. However, the manipulation of seeding dates alone is not sufficient to manage clubroot. Although additional research in this area is still required, it is likely that early seeding may be a useful tool for clubroot management on canola when used along with other crop management options, including host plant resistance, soil amendment and fungicide application.

Sanitization

As noted earlier, any activity that moves P. brassicae-infested soil or infected crop residues from one field to another has the potential to spread clubroot (Strelkov et al. 2011). Sanitization (sanitation) is the process of cleaning and disinfecting or otherwise decontaminating hard surfaces (machinery, equipment, vehicles, tools, footwear), seeds, plant materials, water and/or soil infested with pathogens. In a plant agriculture setting, such practices are meant to eradicate pathogens, eliminate the risk of introducing them, or slow their spread from infested to non-infested fields or beyond localized areas within already infested fields. To prevent the transfer of clubroot-infested soil and infected crop residues to new sites, field equipment, tools, vehicles and the like should be cleaned and, where possible, disinfected prior to moving them from infested to clubroot-free fields. This process has been recommended for use on vegetable farms for many years (Miller et al. 1996; Tremblay et al. 1999; Donald 2006), but its use in canola production systems has been a relatively recent application.

Sanitization involves three key steps: (i) rough cleaning using scraping, brushing or blowing to remove bulk soil and crop debris from contaminated surfaces; (ii) fine cleaning using pressure washing, scrubbing or compressed air to remove any remaining residues; and (iii) disinfection by applying an effective biocide to the cleaned surfaces and allowing at least 20 minutes of contact time to ensure that any remaining spores are killed (Canola Council of Canada 2011).

Unfortunately, many farmers find rigorous sanitization protocols to be excessively time consuming and labour intensive, since field equipment typically has many internal and external surfaces that may be exposed to soil or to spore-bearing dust and infected crop residues. Similar challenges are faced by petroleum, construction and transportation companies, which often work in clubroot-infested fields in areas such as central Alberta. The Canadian Association of Petroleum Producers (CAPP) has recognized the challenges faced by its members and has produced a plan for mitigating the spread of clubroot through petroleum industry-related activities (CAPP 2008).

The most critical steps in sanitizing clubroot-infested farm machinery, equipment and vehicles are the rough and fine cleaning, which should aim to remove up to 99% of the clubroot contamination (Canola Council of Canada 2011). At this point, the surfaces should be free of visible soil and plant material. The application of a disinfectant, such as 1–2% active ingredient sodium hypochlorite solution, on pre-cleaned surfaces will serve to kill or inactivate residual resting spores. A contact time of 20–30 minutes is required to achieve adequate spore mortality. In on-farm demonstration trials in southern Alberta, it took at least 2 hours to clean and disinfect a 12 m wide field cultivator and up to 4 hours for a large tractor (R.J. Howard unpublished data). This work was done using a mobile sanitation unit that contained a commercial pressure washer, air compressor and other equipment that would typically be used by farmers for cleaning machinery, field equipment and vehicles such as farm trucks.

Tractors and tillage equipment generally carry the heaviest loads of infested soil (Canola Council of Canada 2011). For example, a 12 m wide cultivator that had worked in a moist, clubroot-infested field in southern Alberta had c. 50 kg of soil on its shovels, shanks and tires, whereas the large tractor used to pull it had c. 150 kg of soil on the tires and frame (Fig. 4). Heavy soil loads were also observed on a double disc unit working in the same field. At harvest time in an infested canola field, swathers and combines were observed to carry large amounts of crop debris in the form of straw, chaff and seed (Howard et al. unpublished data). Like soil, infested crop debris can be transported over long distances on machinery, vehicles and equipment and may serve to spread clubroot into new areas.

Fig. 4. (Colour online) A, Clubroot-infested soil adhered to tires, shanks and shovels of a 12 m-wide field cultivator – over 50 kg of soil was removed from this implement. B, Clubroot-infested soil on the frame and tires of a large field tractor – over 150 kg of soil was removed from this machine. C, Pressure washing clubroot-infested soil from the tires of a field tractor.

While chlorine has been shown to be useful for disinfesting water containing P. brassicae resting spores (Datnoff et al. 1987), it is highly corrosive and therefore may not be desirable for repeated applications to bare metal on tools and field equipment. Likewise, sensitive electronic equipment, electrical systems and panels may also be damaged by water and/or corrosive disinfectants, thus compromising equipment warranties and longevity. In such cases, it is recommended to use brushes or compressed air to remove loose dust and debris (Canola Council of Canada 2011).

A few studies have compared the relative efficacy of chemical disinfectants against the resting spores of P. brassicae. Donald et al. (2002) reported that none of the nine commercial disinfectants they tested completely inactivated clubroot resting spores and, in fact, most were ineffective. Hypochlorite was the only treatment that resulted in a significant reduction in clubroot severity when treated spores were used to inoculate broccoli seedlings. Howard et al. (unpublished data) evaluated the efficacy of 10 commercial disinfectants (Table 1) against clubroot resting spores obtained from diseased canola roots. Infectivity declined sharply as disinfectant concentration increased over the range of dosages tested for the following products: General Storage Disinfectant, Hyperox^®, KleenGrow^™, EcoClear^™, SaniDate^®, Thymox^™, Virkon^® and Industrial Bleach.

Table 1. Disinfectants evaluated for efficacy against resting spores of Plasmodiophora brassicae in laboratory trials.

Biocide	Supplier	Active ingredients	Recommended concentration^1
Dutrion^®	Dutrion, Ferintosh, AB	Chlorine dioxide 0.2%	50 ppm
EcoClear^™	Ecoval Corp., Toronto, ON	Acetic acid 25%	1:3 or 1:2.25^2
Anostel®/CR-7	Biostel, Olds, AB	Hypochlorous acid (<60 mg/L) and other biocidal ions	90% (v/v) of anolyte:catholyte
General Storage Disinfectant	Ag- Services Inc., Brampton, ON	Alkyl dimethyl benzyl ammonium chloride 10.0%	0.6% (v/v)
Hyperox^®	Vetoquinol, Lavaltrie, QC	Peracetic acid 5% + hydrogen peroxide 25%	0.78% (v/v)
Industrial bleach	Brenntag, Winnipeg, MB	Sodium hypochlorite 10.8%	1% (w/v)
KleenGrow^™	Pace Chemicals, Burnaby, BC	Didecyl dimethyl ammonium chloride 7.5%	0.8% (v/v)
SaniDate^®	Brenntag, Winnipeg, MB	Hydrogen peroxide 27.11% Peracetic acid 2.0%	2% (v/v)
Thymox^™	Laboratoire M2, Sherbrooke, QC	Thymol 23%	1% (v/v)
Virkon^®	Vetoquinol, Lavaltrie, QC	Potassium peroxomonosulphate 21.4%	1% (w/v)

¹Manufacturer’s recommendation for general disinfection of hard surfaces. Trials were conducted at the Crop Diversification Centre South, Brooks, Alberta.

²Product registered for weed control. Used 1 : 3 (v/v; concentrated product/water) for control of actively growing young weeds, or 1 : 2.25 for control of larger weeds and suppression of perennial weeds. In this study 0, 10, 20, 40 and 100% aqueous solutions were used.

Donald et al. (2002) noted that clubroot resting spores subjected to pressurized heat (autoclaved at 121 °C, 20 min) or dry heat (oven at 80 °C, 12 h) exhibited gross changes in their pathogenic activity and caused reduced disease in broccoli and Chinese cabbage seedlings. However, neither treatment resulted in 100% inactivation of the resting spores. Howard et al. (unpublished data) subjected aqueous suspensions of resting spores to seven temperature regimes (40, 50, 60, 70, 80, 90 and 100 °C) for various lengths of time and then inoculated canola seedlings with the treated spores to determine if they were still infective. All treatments reduced infectivity in direct proportion to the exposure times, which ranged from 30 min to 72 h in increments of 0.5 or 1.0 h. The sharpest declines occurred at 80, 90 and 100 °C, after which most spores were rendered non-viable after as little as 30 min of treatment. At 40 and 50 °C, spores remained infective following 48 h of thermal treatment.

Donald et al. (2002) investigated the use of ultraviolet light and calcium, boron and potassium salts for their ability to inactivate clubroot spores in water solutions. Exposure to UV light resulted in reduced pathogenic activity. This was correlated (r = 0.80) with reductions in the severity of root galling on vegetable seedlings that had been inoculated with treated spores. By contrast, the ionic treatments resulted in relatively small reductions in pathogenic activity and there was no correlation with the degree of symptom expression.

Genetic resistance to clubroot

Sources and types of resistance

Genotypes with resistance to one or more of the pathotypes of P. brassicae have been reported in all of the major brassica crops, except B. juncea (L.) Czern. and B. carinata Braun (Diederichsen et al. 2009). Both qualitative (Wit & van de Weg 1964; Crute 1986)  and quantitative (Chiang & Crête 1970; Figdore et al. 1993; Grandclément & Thomas 1996; Voorrips et al. 1997) types of resistance have been reported. Most of these sources of resistance, however, are pathotype or race-specific.

In B. napus, most studies have reported oligogenic control of resistance to P. brassicae (Crute 1986). This would make the pyramiding of resistance genes in B. napus genotypes more practical than in other species. Models based on three, four and five resistance genes have been proposed, and the most favoured model was based on four genes (Gustafsson & Fält 1986). A complex type of inheritance, with dominant genes from B. rapa and recessive genes from B. oleracea, was expected in a re-synthesized B. napus, with resistance from both ancestral species (Diederichsen & Sacristan 1996). Segregation analysis indicated that resistance in re-synthesized B. napus was controlled by at least two dominant and unlinked genes (Diederichsen & Sacristán 1996). One major gene (Pb-Bn1) for resistance against two P. brassicae isolates is located on chromosome N03 and additional minor QTL for each isolate on chromosomes N12 and N19 (Manzanares-Dauleux et al. 2000). Previous reports indicate that P. brassicae resistance in canola is controlled by a combination of major genes and quantitative trait loci (Matsumoto et al. 1998; Suwabe et al. 2003, 2006; Hirai et al. 2004; Piao et al. 2009).

Accessions of B. oleracea with pathotype-independent resistance to P. brassicae have also been reported (Voorrips 1996). Most studies on the C genome indicate that P. brassicae resistance in B. oleracea is quantitative and under the polygenic control of one or two major QTLs and some QTLs with minor effects (Landry et al. 1992; Figdore et al. 1993; Grandclément & Thomas 1996; Voorrips et al. 1997; Moriguchi et al. 1999; Rocherieux et al. 2004; Nomura et al. 2005). A few studies, however, indicated that P. brassicae resistance in B. oleracea is qualitative and controlled by either dominant (Chiang & Crête 1983) or recessive (Yoshikawa 1993) genes. It is possible that both quantitative and qualitative resistance mechanisms may be at play in this species.

Resistance genes from fodder turnip (B. rapa) have been used in resistance breeding of various brassica crops, including Chinese cabbage, oilseed rape and B. oleracea. Although most turnip lines carry more than one resistance gene, cultivars of the other brassica crops with resistance derived from turnip generally carry a single, dominant resistance gene that is pathotype-specific. While important to clubroot management, genetic resistance has generally been race- or pathotype-specific (Diederichsen et al. 2009) and can break down when virulent races increase in the pathogen population. Therefore, genetic resistance should be carefully managed in combination with other methods of clubroot control.

Effect of resistance on pathogen development

Infection of root hairs by P. brassicae occurs in a broad range of plants, not only in susceptible host cultivars but also in resistant cultivars (Diederichsen et al. 2009) and even non-host plants (Feng et al. 2012). Root hairs serve as a niche for pathogen increase prior to invasion of the root cortex, but also provide an opportunity for close interaction between host and pathogen, which facilitates the evolution of mechanisms by which P. brassicae can break down basal resistance to cortical infection (Feng et al. 2013). In susceptible plants, both root hair infection and clubroot severity increase with higher inoculum density (Hwang et al. 2011b, 2011c).

Root hair infection occurs more frequently with a compatible isolate (susceptible reaction) compared with an incompatible isolate (resistant reaction) and, subsequently, fewer cells within the root become infected when the host is resistant (Tanaka et al. 2006). The compatible isolate forms secondary plasmodia with many nuclei and eventually resting spores are formed in the host root tissue. In contrast, plasmodia formed by the incompatible isolate remain immature with only a small number of nuclei and do not produce resting spores (Hwang et al. 2011b; Deora et al. 2013). These results suggest that resistance in host species is associated with a small amount of suppression of infection during primary infection, but a much greater suppression of secondary infection and subsequent plasmodial development in the root cortex. One important difference between the resistant and susceptible host reactions is that in a resistant host, the secondary thickening of the cell walls in the xylem are not degraded and there are fewer cell wall breakages (Donald et al. 2008).

The influence of cultivar resistance on root hair infection was studied across a range of inoculum densities in canola in one resistant and one susceptible cultivar (Hwang et al. 2011b). A subsequent study assessed root hair infection in two resistant and three susceptible canola cultivars (Hwang et al. 2012a). Infection and clubroot severity were higher and plant height was reduced in the susceptible cultivars relative to the resistant cultivars. Root hair infection and the amount of P. brassicae DNA (assessed using qPCR analysis) increased in both resistant and susceptible cultivars over time, but the increases were greater in the susceptible cultivars. Also, there was a strong linear relationship between root infection and the amount of DNA of P. brassicae in the root hairs. The slow increase in the amount of pathogen DNA and root hair infection observed in the resistant cultivars, and the sharp increases observed between 4 and 10 days after inoculation in the susceptible cultivars, indicate that secondary infection and pathogen development are occurring quickly in the susceptible cultivars. However, sharp declines in detectable levels of pathogen DNA in the seedling roots occurred during the transition from zoospore development in the root hairs to secondary infection (Hwang et al. 2012a). These levels quickly rebounded as the pathogen spread into the root cortex after secondary infection (Gludovacz 2013).

The rate of infection and pathogen development is most rapid in susceptible canola lines (Deora et al. 2012 2013). However, resistant plants showed reduced growth and delayed development when inoculated with resting spores of an avirulent pathotype (Hwang et al. 2012a; Deora et al. 2013), which indicates that resistance is an active process. In at least one vegetable brassica line, microscopic analysis has revealed substantial levels of pathogen infection in inoculated roots of symptomless plants (Gludovacz 2013; Gludovacz et al. 2013). The mechanism for this response has not yet been determined, but it is possible that it involves genes for tolerance to P. brassicae.

Successful management of P. brassicae through the deployment of genetically resistant cultivars will require very careful control of susceptible weeds and canola volunteers to maximize the impact of resistant cultivars on reducing resting spore levels in the soil and to prevent the build-up of virulent populations.

Deployment of resistance

Clubroot-resistant canola cultivars have been the dominant component of the clubroot management strategy in western Canada in recent years (Figs 5, 6). The first resistant cultivar for western Canada, Pioneer ‘45H29’, was registered in 2009 and its release was quickly followed by several other resistant cultivars (Strelkov et al. 2011; Gossen et al. 2013b). However, the durability of this resistance is not known. Also, the genetic basis for the resistance in these cultivars is proprietary knowledge that is not available to the public. This has complicated efforts aimed at resistance stewardship, since it is not possible to develop rational strategies for the rotation of resistance sources in infested fields. Also, the number of resistance genes that are currently available to breeders is limited (Hirai 2006). Recent studies indicated that there were no detectable differences in pathotype reactions among clubroot-resistant canola cultivars available in western Canada (Deora et al. 2012, 2013). This represents one line of evidence that resistance genes in all of these lines originated from a similar source. In contrast, another recent study by LeBoldus et al. (2012) revealed that pathogen populations that had been repeatedly cycled on and become adapted to one brassica host did not exhibit a similar adaptation to other hosts, when the cycled populations were inoculated on the latter, indicating that distinct sources of resistance may occur in at least some genotypes. Regardless of the relationships between resistance sources, there is substantial genetic and pathotype variation present in the P. brassicae populations in western Canada (Strelkov et al. 2006; Xue et al. 2008; Cao et al. 2009), and the deployment of a cultivar with single-gene resistance against a genetically diverse pathogen on a large scale imposes a strong selection pressure for pathogen genotypes that are able to overcome this resistance.

Fig. 5. (Colour online) A, Resistant and B, susceptible canola genotypes grown in clubroot-infected soil in a field near Edmonton, AB. Note that under severe clubroot pressure, a poor canopy is produced and canola plants ripen prematurely. C, Roots on the resistant plants appear normal and healthy, while those on the susceptible plants (D) are severely galled.

Fig. 6. (Colour online) Mature susceptible canola plants infected by Plasmodiophora brassicae in a field near Edmonton, AB showing premature seed pod formation; resistant plants are unaffected by clubroot.

Erosion or breakdown of resistance

Resistance to P. brassicae has broken down in various cruciferous crops, including oilseed rape and vegetable brassicas (Seaman et al. 1963; Kuginuki et al. 1999; Oxley 2007; Diederichsen et al. 2009). While P. brassicae-resistant cultivars of B. napus, B. oleracea and B. rapa are available, their use is often limited by the short durability and the pathotype-specificity of the resistance (Voorrips 1995; Diederichsen et al. 2009). Each of the resistant canola cultivars available for production in western Canada will develop small galls under high inoculum pressure, and repeated cycles of inoculation can result in a rapid decline in the level of resistance (LeBoldus et al. 2012). The effective and sustainable deployment of genetically resistant cultivars to manage clubroot disease requires that the use of these cultivars be integrated with various other approaches for control (Diederichsen et al. 2009; Donald & Porter 2009). As such, regardless of the nature of the resistance, it is prudent to ensure that resistance is carefully managed to maximize its durability.

Resting spore populations in soil

In principle, cropping of resistant cultivars should result in a reduction in the population of resting spores in the soil by stimulating spore germination. Also, few or no resting spores are produced in the resistant plants. However, fields cropped to resistant crops are not necessarily free of susceptible plants. Susceptible weed species are endemic, susceptible canola volunteers will continue to be present in infested fields for many years, and there may be a small percentage of susceptible siblings or off-types in seed lots. Each of these factors may offset the benefits that can be derived from a resistant cultivar (Hwang et al. 2012a).

The effects of growing resistant and susceptible canola genotypes on resting spore populations were assessed under greenhouse and field conditions (Hwang et al. 2012a). One crop of susceptible canola contributed 1.4 × 10⁸ resting spores mL⁻¹ soil in a mini-plot experiment, and 1.0 × 10¹⁰ spores per g gall under field conditions. Repeated cropping of susceptible canola over four, 6-week cycles increased clubroot severity over time, while severity declined slightly in continuously fallow soil and where a resistant cultivar was repeatedly grown. When a resistant canola cultivar was included in the field study, the susceptible cultivar produced much larger galls. Moreover, galls in the resistant cultivar produced only 60% of the number of spores per g of gall mass than in the susceptible cultivar, which further reduced the relative contribution of inoculum by the resistant cultivar (Hwang et al. 2012a).

Resting spore concentrations in the soil increased following the cultivation of both resistant and susceptible canola cultivars in heavily infested soil, although the increase was greatest with a susceptible cultivar (Hwang et al. 2012a). In Sweden, partially resistant cultivars of oilseed turnip rape (B. rapa var. oleifera) grown on moderately infested soils produced a slight decrease in inoculum levels (Wallenhammar 1996). Taken together, these results indicate that production of resistant cultivars may reduce inoculum levels in lightly or moderately infested soils, but will not appreciably reduce clubroot infestations in heavily infested fields. Further research, including a long-term study, is required to confirm this view.

A number of studies have examined the effect of susceptible weeds and volunteers on resting spore populations by growing mixtures of resistant and susceptible plants. In a recent trial, repeated cropping of a resistant cultivar reduced resting spore populations compared with a susceptible cultivar, and also reduced clubroot severity in the subsequent susceptible canola crop (Hwang et al. 2012a). However, soil inoculum loads were similar following resistant canola and continuous fallow. This indicates that while the resistant cultivar does not increase soil inoculum loads, it also does not act as a bait crop, i.e. it does not appear to significantly stimulate the germination of resting spores. However, in another study, resistant crucifers reduced the numbers of residual resting spores after 4 years of continuous cultivation (Yamagishi et al. 1986). Colonization and gall formation also were reduced when susceptible and resistant radish (Raphanus sativus L.) cultivars were grown together, relative to the susceptible cultivar alone (Kroll et al. 1984). In Canada, clubroot severity was lower in a susceptible canola crop following a mixed crop (resistant + susceptible) relative to a susceptible cultivar only, but was higher than following fallow or a resistant cultivar only (Hwang et al. 2013). This indicates that susceptible volunteer canola may play an important role in the persistence of resting spore populations in infested fields. No empirical data are available, however, on the number of resting spores contributed by volunteers in infested fields where resistant canola is grown.

Conclusions

Since clubroot was first identified on canola in Alberta in 2003, intensive research has been conducted into the management and containment of this disease. Several clubroot management strategies that are recommended for high-value horticultural crops proved to be impractical for large-scale canola production. Soil amendments to increase soil pH may reduce clubroot severity slightly, but not sufficiently to have an impact on clubroot proliferation. The costs and environmental concerns associated with soil-applied fungicides make them impractical for use in the large-scale production of field crops. Crop rotations can be used to reduce resting spore populations, but very long intervals are required between susceptible canola crops, and bait crops are unlikely to be an important component of an integrated management programme for clubroot. Soil fumigants have potential for elimination or reduction of small-scale infestations near field entrances, but more research is required to optimize their efficacy and minimize environmental risk before they are likely to be used in commercial situations.

Resistant cultivars have become the main means for management of clubroot. Unfortunately, few resistance genes are available for deployment, and single-gene resistance to P. brassicae has been quickly eroded in the past. Also, substantial genetic and virulence variation exists within the P. brassicae population in western Canada. Production of canola lines with single-gene resistance against a genetically diverse pathogen on a large hectarage will impose a strong selection pressure favouring pathogen genotypes that are able to overcome this resistance. As a result, a breakdown in the resistance of the current clubroot-resistant cultivars seems likely if their use is not properly managed. Genetic resistance should be considered as just one component in the integrated management of clubroot disease in canola on the Canadian Prairies. In infested fields in western Canada, the cropping of clubroot-susceptible canola cultivars will result in an increase in P. brassicae resting spore populations in the soil over time, while cropping of clubroot-resistant cultivars is equivalent to leaving the land fallow, although the biology of the fallow land would not be the same. However, it is likely that this effect will be offset by susceptible off-types, susceptible canola volunteers, and cruciferous weeds, which will continue to increase resting spore populations if they are not managed with adequate attention and care.

G. Peng

Agriculture and Agri-Food Canada, Saskatoon Research Centre, Saskatoon, SK S7N 0X2, Canada

B. D. Gossen

Agriculture and Agri-Food Canada, Saskatoon Research Centre, Saskatoon, SK S7N 0X2, Canada

S. E. Strelkov

Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB T6G 2P5, Canada

R. J. Howard

Crop Diversification Centre South, Alberta Agriculture and Rural Development, Brooks, AB T1R 1E6, Canada

S. F. Hwang

Crop Diversification Centre North, Alberta Agriculture and Rural Development, Edmonton, AB T5Y 6H3, Canada

Correspondence to: S.F. Hwang. E-mail: [email protected]

Acknowledgements

Financial support from the Agriculture and Agri-Food Canada/Canola Council of Canada Clubroot Risk Mitigation Initiative, the Alberta Crop Industry Development Fund, the Alberta Canola Producers Commission, SaskCanola, and the Manitoba Canola Growers Association is gratefully acknowledged.