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Plantwise Technical Factsheet

club root (Plasmodiophora brassicae)

Host plants / species affected
Brassica
Brassica napus var. napobrassica (swede)
Brassica napus var. napus (rape)
Brassica oleracea (cabbages, cauliflowers)
Brassica oleracea var. botrytis (cauliflower)
Brassica oleracea var. capitata (cabbage)
Brassica oleracea var. gemmifera (Brussels sprouts)
Brassica oleracea var. gongylodes (kohlrabi)
Brassica oleracea var. italica (broccoli)
Brassica oleracea var. viridis (collards)
Brassica rapa cultivar group Caixin
Brassica rapa cultivar group Mizuna
Brassica rapa cultivar group Taatsai (Chinese flat cabbage)
Brassica rapa subsp. chinensis (Chinese cabbage)
Brassica rapa subsp. oleifera (turnip rape)
Brassica rapa subsp. pekinensis
Brassicaceae (cruciferous crops)
Capsella bursa-pastoris (shepherd's purse)
Eutrema wasabi (Wasabi)
Matthiola
Nasturtium officinale (watercress)
Raphanus sativus (radish)
Rosaceae
List of symptoms/signs
Roots  -  galls along length
Roots  -  soft rot of cortex
Roots  -  stubby roots
Symptoms

Clubroot is known by many other names including, most commonly, finger and toe, knolvoet, hernie du chou, kohlhernie, klomprot and kapoustnaja kila (Dixon, 2009a). The root malformation produced is most commonly confused with the symptoms of insect damage, especially that of the turnip gall weevil (Ceutorhyncus pleurostigma) and on swedes and turnips, with the hard swellings of uncertain origin, termed 'hybridisation nodules'.

The disease rarely kills plants but induces them to wilt when under slight water stress. Initial foliar wilting is followed by reddening of the leaves which become chlorotic and eventually necrotic. Plants may become stunted, flowering is accelerated with the formation of small poor quality curds or spears in cauliflower and calabrese (green broccoli) and especially in large, heavy plants such as Brussels sprout become physically unstable. Crop efficiency is impaired as a consequence of erratic maturity and the failure to produce uniform high quality products. Clubroot deforms and reduces the market value of root crops and where these are used as stock fodder there is a loss of palatability and storability. Land infested by P. brassicae losses its capital asset value since rotations involving brassicas are prevented. Methods for the assessment of clubroot disease and for infection for experimental purposes were described by Dixon (1976a, b, respectively).

Prevention and control

The soil-borne nature of P. brassicae along with the durable nature of its resting spores means this pathogen, once present, can be particularly difficult to manage. Despite some resting spores appearing able to remain viable for over 15 years the average half-life of these structures is 3.6 years (Wallenhammar, 1996) meaning the use of crop rotations which avoid members of the Brassicaceae depressing soil-borne inoculum potential is advocated as a longer term disease management technique. Fungicides generally provide inconsistent to ineffectual control of P. brassicae resulting in limited wide spread use in disease management programmes.  Raising soil pH above 7.0 using forms of lime is a traditional method for combating clubroot disease and has been examined by numerous workers worldwide not infrequently producing conflicting results due to application of varying calcium compounds, rates of application, differing soil types and climates Myers and Campbell (1985). Application of fertilizers such as calcium cyanamide (Trembaly et al., 2005) and calcium nitrate (Dixon and Page, 1998) are associated with reduced clubroot incidence although disease control conferred by these products can be inconsistent (McGrann et al., 2016).

P. brassicae resistant varieties of most brassica crops have been developed. However, in most of these cases resistance is based on a single dominant resistance gene. Widespread use of oligogenic resistance against clubroot is likely to lead to evolutionary changes in the pathogen population resulting is isolates that can overcome the resistance source (Diederichsen et al., 2009). This has been observed in European oilseed rape where clubroot resistance is based on a single resistance source, ‘Mendel’, (Diederichsen et al., 2006) which has been used heavily and is now being overcome by virulent P. brassicae isolates (McGrann et al., 2016). 

Due the difficulties associated with managing this disease preventing the introduction of P. brassicae is essential. Resting spores of the pathogen can be easily spread in soil that adheres to farm machinery, workers footwear and livestock grazing in infested fields.  Infested soil attached to plant material or for use as potting media can also be a means through which the pathogen can be spread long distances. Ensuring machinery and workers footwear is cleaned after entering infested fields will reduce the risk of transferring P. brassicae to uncontaminated areas. Importing brassica plants that are free from infection will also reduce the risk of introducing the pathogen to previously uninfested areas.

Cultural Control

Raising soil pH above 7.0 using forms of lime is a traditional method for combating clubroot disease and has been examined by numerous workers worldwide not infrequently producing conflicting results due to application of varying calcium compounds, rates of application, differing soil types and climates (Myers and Campbell, 1985). Application of fertilizers such as calcium cyanamide (Trembaly et al., 2005) and calcium nitrate (Dixon and Page, 1998) are associated with reduced clubroot incidence although disease control conferred by these products can be inconsistent (McGrann et al., 2016).

The use of crop rotations which avoid members of the Brassicaceae depressing soil-borne inoculum potential is advocated as a longer term technique. Studies of rotational components, the effects on resting spore viability and germination, stimulation of soil suppressiveness and interactions with soil physical factors or other microbial components are typified by the results of Rouxel et al. (1987), Suzucki et al. (1992), Osozawa et al. (1994), Tsushima et al. (1996), Wallenhammar (1996), Worku and Gerhardson (1996) and Arie (1998). Where applicable soil sterilization could be used to lower soil inoculum levels (Borges et al., 1996).

Chemical Control

Numerous molecules have been screened for activity against P. brassicae reviewed by Pen et al. (2014) with very limited success. The compounds: trichlamide, flusulfamide and fluazinam are effective against weakly virulent P. brassicae isolates (Tanaka et al., 1999). Quintozene (Smieton, 1939) and dazomet (soil sterilant, releasing methyl iso thiocyanate) are available more widely. Unfortunately, the prohibitively expensive cost of some of these products combined with inconsistent performance means they are not likely to be used in broad acre oilseed rape production (Peng et al., 2014).

Host-Plant Resistance

Oligogenic dominant forms of resistance exist in B. rapa and B. napus (Wit and van de Weg, 1964; Wit, 1965; Lammerink, 1967) whereas B. oleracea contains recessive, possibly additive resistance systems (Chiang and Crete, 1970). Resistance in B. oleracea has been examined by Dixon and Robinson (1986), Crisp et al. (1989), Figdore et al. (1993), Granclement et al. (1996), Grandclement and Thomas (1996), Vorrips and Kane (1997), Vorrips et al. (1997) and in B. napus by Diederichsen and Sacristan (1996) and Bradshaw et al. (1997). Resistance in B. rapa has been exploited commercially to produce cultivars of stubble turnip and Japanese cultivars of Chinese cabbage (Dixon, 1974; Mattusch, 1976; Ashizawa et al., 1978) and in B. oleracea producing calabrese (green broccoli) cultivars (Dixon et al., 1986).

An extensive survey of resistance of accessions taken from across the Brassicaceae is reported by Scholtze and Hammer (1998). Fuchs and Sacristan (1996) report resistance in Arabidopsis thaliana associated with a hypersensitive reaction. Resistance in radish (Raphanus spp.) may be utilised to produce commercial cultivars of Daikon (R. sativus var. longipinnatus) (Bunin and Yoshikawa, 1991) and in the amphidiploid Raphanobrassica (McNaughton, 1973). Transfers of resistance between Brassica spp and wild relatives are envisaged by Sjodin and Glimelius (1988). Widespread use of oligogenic resistance against clubroot is likely to lead to evolutionary changes in the pathogen population resulting is isolates that can overcome the resistance source (Diederichsen et al., 2009). This has been observed in European oilseed rape where clubroot resistance is based on a single resistance source, ‘Mendel’, (Diederichsen et al., 2006) which has been used heavily and is now being overcome by virulent P. brassicae isolates (McGrann et al., 2016).  

Information Sources

The International Clubroot Working Group (ICWG) operates a Discussion Site at: http://cvu.strath.ac.uk/HyperNews/get/clubroot.html The ICWG Chairman is Professor GR Dixon, Department of Bioscience and Biotechnology, University of Strathclyde, Glasgow, UK. Meetings are arranged in conjunction with Brassica Symposia arranged by the International Society for Horticultural Science (ISHS) and Crucifer Genetics Workshops, International Congresses of Plant Pathology, International Horticultural Congresses and at national meetings of societies of plant pathology. Information gathered at these meetings is reported in the Cruciferae Newsletter published by Institut National de la Recherche Agronomique (INRA), Rennes, France.

Impact

Introduction

Brassica clubroot was considered the economically most important disease of cultivated crucifers by Karling (1968). His review cites more than 300 species and varieties within 61 genera of the Cruciferae that have been reported as susceptible to clubroot disease.

Early Observations

Early observations from the 13th century are supposed to relate to clubroot disease (Böhner, 1922). Disease symptoms of cabbage were well known in Spain in the 16th century, and the occurrence was reported in 1736 in England, and later in Norway in 1855 and then in Scotland in 1870 (see Karling, 1968; Dixon, 2009a). Reports from Finland date back to the 1860s (Jamalainen, 1936). However, it was not until 1869, when cabbage fields outside St Petersburg were devastated, that Woronin (1878) described the pathogen as a fungus. Clubroot was thereafter observed and described throughout Europe and was reported in Denmark (Christensen et al., 1909) and Sweden (Eriksson, 1906). It was first reported in Japan for cabbage in 1892 (Yoshikiawa and Buczacki, 1978), and caused severe losses for cabbage in the USA (Halsted, 1894). P. brassicae is now recognised as a protist and not a fungus.

Geographical Spread and Field Surveys

Clubroot disease is distributed throughout the temperate region, and is also prevalent in tropical and subtropical areas. In several countries it has been estimated that clubroot infestation exceeds 10% of the land on which crucifer crops are grown (Buczacki, 1983). 

In oilseed rape crops this level of observation normally does not occur and the severity of the disease is underestimated (Krostitz, 1991; Wallenhammar, 1999). However, in the UK, the incidence of clubroot has steadily risen with more than 50% of the sites surveyed across England, Scotland and Wales between 2007 and 2010 infected with P. brassicae (McGrann et al., 2016). 

In Finland, P. brassicae was detected in vegetable Brassica crops all over the country with 375 (65%) of the sampled plants showing clubroot symptoms (Linnasalmi and Tovianen, 1991). In Finnish oilseed/turnip rape fields, clubroot was detected in 10-20% of the fields yearly from 1982 to 1987, but it was not reported to have caused severe yield losses (Hannukakala, 1988).

P. brassicae was detected in 40% of vegetable Brassica fields surveyed in Taiwan (Hsieh and Yang, 1985). In Poland and the Czech Republic, a number of pathotypes have been identified that are associated with crop damage (Řičařová et al., 2016). Clubroot was reported to occur in oilseed rape crops in Rostock and Schwerin, Germany (Daebler et al., 1980) and in Schlesweig-Holstein, Germany (Krostitz, 1991). In Canada, P. brassicae has spread since 2003 and is now considered a serious threat to brassica cultivation (Hwang et al., 2012). Clubroot was reported as a new dangerous disease of yellow sarson (B. campestris var. yellow sarson) from several districts in West Bengal in 1983-85 (Laha et al., 1985). Chattopadhyay and Bagchi (1989) reported severe attacks in all of the cultivated varieties of rapeseed mustard (B. campestris var. yellow sarson, B. campestris var. toria, B. juncea) in West Bengal, India.

Soil sampled for the presence of clubroot in Swedish fields destined for oilseed cropping in 1987 to 1993 revealed a widespread occurrence of inoculum with 217 (57%) positive tests (Engqvist, 1994). In an area of central Sweden, Örebro county, soil from 190 fields on farms where clubroot was detected revealed the presence of clubroot in 148 (78%) of the fields (Wallenhammar, 1996). Field surveys are continuously carried out by observing symptoms in randomly selected fields of spring oilseed rape and spring oilseed turnip rape in Örebro. During the period 1984-98, infected plants were assessed in 235 (30%) of the fields investigated. These outbreaks are related to an oilseed rape area covering an average 3935 ha/year (Wallenhammar, 1999). 

Measurement of Yield Loss

There are numerous reports from the late 1800s and from early in the twentieth century of 50 to 100% destruction of turnips, swedes and cabbages in Germany, the UK, the USA, the USSR and other countries in Europe, Asia and South Africa (Colhoun, 1958; Karling, 1968). The impact has never been greater than it is today because of the wide variety of cruciferous crops being grown (Buczacki, 1983). In Japan, clubroot occurs with increasing severity throughout the country (Yoshikawa and Buczacki, 1978). Extensive disease surveys are reported from some countries, for example, Australia where annual losses of crucifer crops caused by P. brassicae are estimated at least 10% (Faggian et al., 1999). In recent years considerable yield losses have been reported on mustard, Szechuan mustard, Chinese cabbage and Pak-choi from Taiwan (Hsieh and Yang, 1985). A yield loss of 32.5% was estimated by experimental cutting in mustard in India (Laha et al., 1985).

In Swedish field experiments where increasing amounts of infested soil were applied as soil inoculum prior to planting, linear relationships between yield of spring oilseed rape and disease incidence (R²=0.90), and between yield and soil infestation (R²=0.94) were found. A clear positive linear relationship between disease incidence and degree of infestation was also found (R²=0.87). Results from a field experimental site, naturally contaminated with P. brassicae, showed an equally linear relationship (R²=0.82). A yield reduction of 1620 tonnes/ha (50%) at the highest level of infestation (91% infected plants) was measured, while at <20% plants infected, yield reductions were estimated at about 10% (0.3 tonnes/ha) (Wallenhammar, 1998).

The magnitude of yield loss caused by infections of P. brassicae depends not only on soil infestation level, but also on other soil factors. A very important factor is the time of infection, determining the part of the growing season available after infection. An early attack on a field with high inoculum density could probably lead to complete crop failure. In field experiments where disease incidence was 100%, yields were 583 kg/ha of spring oilseed rape (Wallenhammar, 1998) and 264 kg/ha of spring oilseed turnip rape (Wallenhammar, 1999). These reductions correspond to a yield loss of 72 and 85 % related to the average yield of spring oilseed rape and spring oilseed turnip rape in Sweden 1999 (Anon., 1999). A late attack in a field with lower inoculum density may pass undetected. Field experimental data in spring oilseed rape show a yield decrease of 263 kg/ha (9%) with a corresponding disease incidence of 17%, while at 7% infected plants, no significant yield reduction was recorded (Wallenhammar, 1998). When disease incidence is low <20% infected plants), the level of yield loss in summer oilseed turnip rape appears to be the same as for summer oilseed rape. Yield loss ranged between 5-8% with a corresponding disease incidence of 17% (Wallenhammar et al., 2000).

Experimental data from Germany in winter oilseed rape show a yield reduction of 47% at medium infestation levels, and of 78% at high infestation levels where the plant density was also reduced by 73% (Daebler et al., 1980).

In UK field trials yield losses in winter oilseed rape were demonstrated at 0.03 t ha-1 for every 1% increase in clubroot severity in the susceptible variety Kommando indicating that losses in severely infected crops can equate to over 50% of potential yield (McGrann et al., 2016).

Assessment of inoculum distribution in one infested field clearly showed a patchy occurrence (Wallenhammar, 1998) indicating that yield loss is seldom total in a whole field.

The more recent introduction of P. brassicae in Canada has seen economic losses to oilseed rape in the region of 30-90% yield losses dependent of the region affected. In some instances complete crop failures have been reported (Hwang et al., 2012).

Related treatment support
Plantwise Factsheets for Farmers
Cambodia, General Directorate of Agriculture; CABI, 2014, English language
Somachandra, K. P.; Perera, M. S. K. K.; Thanabalasingam, K.; Hadji, T. K. A. I.; CABI, 2013, English language
Somachandra, K. P.; Perera, M. S. K. K.; Thanabalasingam, K.; Hadji, T. K. A. I.; CABI, 2013, Sinhalese language
Somachandra, K. P.; Perera, M. S. K. K.; Thanabalasingam, K.; Hadji, T. K. A. I.; CABI, 2013, Tamil language
Bwalya, C.; CABI, 2017, English language
 
Pest Management Decision Guides
Cambodia, General Directorate of Agriculture; CABI, 2015, English language
Adhikari, S.; Aryal, S.; Pokhrel, M.; CABI, 2014, English language
Adhikari, S.; Aryal, S.; Pokhrel, M.; CABI, 2014, Bengali language
Somachandra, K. P.; CABI, 2014, English language
CABI; CABI, 2015, Spanish language
 
External factsheets
HGCA On-Farm Information, Home-Grown Cereals Authority (HGCA), 2006, English language
RHS Gardening Advice Factsheets, Royal Horticultural Society, 2012, English language
Pestnet Factsheets, Pestnet, 2016, English language
Cornell University Factsheets, Cornell University Plant Pathology Department, 2012, English language
East West Seed Crop Disease Factsheets, East West Seed, 2013, English language
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