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Belowground Defence Strategies Against Clubroot (Plasmodiophora brassicae)

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Belowground Defence Strategies in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

The clubroot disease is one of the most devastating root-borne diseases of brassica crops. While breeding of resistant cultivars is still a method of choice, the control of clubroot by either biocontrol agents or even plant strengtheners could be improved. More environmentally friendly alternatives or additional means to make the resistance response of crop plants more durable are needed. Chemical control of clubroot is in many cases not successful; only liming has been used traditionally with good success. In some cases, the model plant Arabidopsis thaliana has been used; a plethora of work however has been done on oilseed rape/canola (in this chapter, the common name for Brassica napus will be chosen according to the name in the respective publications, mainly canola in Canada and oilseed rape in Europe) (Brassica napus). The clubroot pathogen is called Plasmodiophora brassicae and constitutes an obligate biotrophic protist that lives in close relationship with its host cell. The roots of the host plants are colonized, and the plant growth is altered upon infection. While shoots can be stunted and show wilt symptoms after longer infection periods, the root system is converted to a tumorous root tissue, called “clubroot” by alterations of plant hormones and metabolic pathways essential for pathogen nutrition. In this chapter, the major focus will, however, be on biocontrol of clubroot by either endophytic organisms or by plant strengtheners or plant growth regulators; and some mechanisms behind it, independent of which host plant was employed, will be discussed.

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References

  • Agarwal A, Kaul V, Faggian R, Rookes JE, Ludwig-Müller J, Cahill DM (2011) Analysis of global host gene expression during the primary phase of the Arabidopsis thalianaPlasmodiophora brassicae interaction. Funct Plant Biol 38:462–478

    Article  CAS  Google Scholar 

  • Ahmed HU, Hwang SF, Strelkov SE, Gossen BD, Peng G, Howard RJ, Turnbull GD (2011) Assessment of bait crops to reduce inoculum of clubroot (Plasmodiophora brassicae) of canola. Can J Plant Sci 91:545–551

    Article  Google Scholar 

  • Aist JR, Williams PH (1971) The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae Wor. Can J Bot 49:2023–2034

    Article  Google Scholar 

  • Arie T, Kobayashi Y, Kono Y, Gen O, Yamaguchi I (1999) Control of clubroot of crucifers by Phoma glomerata and its product epoxydon. Pestic Sci 55:602–604

    Article  CAS  Google Scholar 

  • Arnold DL, Blakesley D, Clarkson JM (1996) Evidence for the growth of Plasmodiophora brassicae in vitro. Mycol Res 100:535–540

    Article  CAS  Google Scholar 

  • Auer S, Ludwig-Müller J (2014) Effects of the endophyte Acremonium alternatum on oilseed rape (Brassica napus) development and clubroot progression. Albanian J Agric Sci 13:15–20

    Google Scholar 

  • Buczacki ST, Moxham SE (1979) A triple stain for differentiating resin-embedded sections of Plasmodiophora brassicae in host tissues under light microscope. Trans Br Mycol Soc 72:311–347

    Article  Google Scholar 

  • Chai AL, Xie XW, Shi YX, Li BJ (2014) Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Can J Plant Pathol 36(S1):142–153

    Article  Google Scholar 

  • Cheah L-H, Kent G, Gowers S (2001) Brassica crops and a Streptomyces sp. as potential biocontrol for clubroot of brassicas. N Z Plant Prot 54:80–83

    Google Scholar 

  • Cheah L-H, Gowers S, Marsh AT (2006) Clubroot control using Brassica break crops. Acta Hortic 706:329–332

    Article  Google Scholar 

  • Choe S (2004) Brassinosteroid biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic, Dordrecht, pp 156–178

    Google Scholar 

  • Christian M, Steffens B, Schenck D, Burmester S, Böttger M, Lüthen H (2006) How does auxin enhance cell elongation? Roles of auxin-binding proteins and potassium channels in growth control. Plant Biol 8:346–352

    Article  CAS  PubMed  Google Scholar 

  • Clapperton MJ, Lee NO, Binet F, Conner RL (2001) Earthworms indirectly reduce the effects of take-all (Gaeumannomyces graminis var. tritici) on soft white spring wheat (Triticum aestivum cv. Fielder). Soil Biol Biochem 33:1531–1538

    Article  CAS  Google Scholar 

  • Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119

    Article  CAS  Google Scholar 

  • Deora A, Gossen BD, Walley F, McDonald MR (2011) Boron reduces development of clubroot in canola. Can J Plant Pathol 33:475–484

    Article  CAS  Google Scholar 

  • Devos S, Prinsen E (2006) Plant hormones: a key in clubroot development. Commun Agric Appl Biol Sci 71(3 Pt B):869–872

    CAS  PubMed  Google Scholar 

  • Diederichsen E, Frauen M, Ludwig-Müller J (2014) Clubroot disease management challenges from a German perspective. Can J Plant Pathol 36(S1):85–98

    Article  CAS  Google Scholar 

  • Dixon GR (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J Plant Growth Regul 28:194–202

    Article  CAS  Google Scholar 

  • Dixon GR (2014) Clubroot (Plasmodiophora brassicae Woronin)—an agricultural and biological challenge worldwide. Can J Plant Pathol 36(S1):5–18

    Article  CAS  Google Scholar 

  • Doan TT, Jäschke D, Ludwig-Müller J (2010) An endophytic fungus induces tolerance against the clubroot pathogen Plasmodiophora brassicae in Arabidopsis thaliana and Brassica rapa roots. Acta Hortic 867:173–180

    Article  Google Scholar 

  • Donald EC, Porter IJ (2004) A sand–solution culture technique used to observe the effect of calcium and pH on root hair and cortical stages of infection by Plasmodiophora brassicae. Australas Plant Pathol 33:585–589

    Article  CAS  Google Scholar 

  • Donald EC (2005) The influence of abiotic factors and host plant physiology on the survival and pathology of Plasmodiophora brassicae of vegetable brassicas. PhD thesis, University of Melbourne

    Google Scholar 

  • Donald C, Porter I (2009) Integrated control of clubroot. J Plant Growth Regul 28:289–303

    Article  CAS  Google Scholar 

  • Donald EC, Porter IJ (2014) Clubroot in Australia: the history and impact of Plasmodiophora brassicae in Brassica crops and research efforts directed towards its control. Can J Plant Pathol 36(S1):66–84

    Article  CAS  Google Scholar 

  • Donald EC, Lawrence JM, Porter IJ (2004) Influence of particle size and application method on the efficacy of calcium cyanamide for control of clubroot of vegetable brassicas. Crop Prot 23:297–303

    Article  CAS  Google Scholar 

  • Einhorn G, Bochow H (1990) Influence of temperature and soil pH value on the pathogenesis of clubroot Plasmodiophora brassicae Wor. Arch Phytopathol Pflanzen 26:131–138

    Article  Google Scholar 

  • Faggian R, Strelkov SE (2009) Detection and Measurement of Plasmodiophora brassicae. J Plant Growth Regul 28:282–288

    Article  CAS  Google Scholar 

  • Faggian R, Bulman SR, Lawrie AC, Porter IJ (1999) Specific polymerase chain reaction primers for the detection of Plasmodiophora brassicae in soil and water. Phytopathology 89:392–397

    Article  CAS  PubMed  Google Scholar 

  • Friberg H, Lagerlöf J, Hedlund K, Rämert B (2008) Effect of earthworms and incorporation of grass on Plasmodiophora brassicae. Pedobiologia 52:29–39

    Article  Google Scholar 

  • Gao Y, Xu G (2014) Development of an effective nonchemical method against Plasmodiophora brassicae on Chinese cabbage. Int J Agron 2014:Article ID 307367, http://dx.doi.org/10.1155/2014/307367

    Article  Google Scholar 

  • Gimsing AL, Kirkegaard JA (2009) Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil. Phytochem Rev 8:299–310

    Article  CAS  Google Scholar 

  • Gossen BD, Adhikari KKC, McDonald MR (2012) Effect of seeding date on development of clubroot in short-season brassica crops. Can J Plant Pathol 34:516–523

    Article  Google Scholar 

  • Gossen BD, Deora A, Peng G, Hwang S-F, McDonald MR (2014) Effect of environmental parameters on clubroot development and the risk of pathogen spread. Can J Plant Pathol 36(S1):37–48

    Article  CAS  Google Scholar 

  • Guo S, Mao Z, Wu Y, Hao K, He P, He Y (2013) Genome sequencing of Bacillus subtilis strain XF-1 with high efficiency in the suppression of Plasmodiophora brassicae. Genome Announc 1(2):e00066-13. doi:10.1128/genomeA.00066-13

    PubMed Central  Google Scholar 

  • Hartwig T, Corvalan C, Best NB, Budka JS, Zhu J-Y, Choe S, Schulz B (2012) Propiconazole is a specific and accessible brassinosteroid (BR) biosynthesis inhibitor for Arabidopsis and maize. PLoS One 7:e36625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hildebrand PD, McRae KB (1998) Control of clubroot caused by Plasmodiophora brassicae with nonionic surfactants. Can J Plant Pathol 20:1–11

    Article  CAS  Google Scholar 

  • Hirai M (2006) Genetic analysis of clubroot resistance in Brassica crops. Breeding Sci 56:223–229

    Article  Google Scholar 

  • Howard RJ, Strelkov SE, Harding MW (2010) Clubroot of cruciferous crops—new perspectives on an old disease. Can J Plant Pathol 32:43–57

    Article  Google Scholar 

  • Hwang SF, Cao T, Xiao Q, Ahmed HU, Manolii VP, Turnbull GD, Gossen BD, Peng G, Strelkov SE (2012) Effects of fungicide, seeding date and seedling age on clubroot severity, seedling emergence and yield of canola. Can J Plant Sci 92:1175–1186

    Article  CAS  Google Scholar 

  • Hwang SF, Ahmed HU, Zhou Q, Strelkov SE, Gossen BD, Peng G, Turnbull GD (2014a) Efficacy of Vapam fumigant against clubroot (Plasmodiophora brassicae) of canola. Plant Pathol 63:1374–1383

    Article  CAS  Google Scholar 

  • Hwang S-F, Howard RJ, Strelkov SE, Gossen BD, Peng G (2014b) Management of clubroot (Plasmodiophora brassicae) on canola (Brassica napus) in western Canada. Can J Plant Pathol 36(S1):49–65

    Article  CAS  Google Scholar 

  • Ikegami H (1985) Decrease of clubroot fungus by cultivation of different crops in heavily infested soil. Res Bull Fac Agric Gifu Univ 50:19–32

    Google Scholar 

  • Jahn L, Mucha S, Bergmann S, Horn C, Siemens J, Staswick P, Steffens B, Ludwig-Müller J (2013) The clubroot pathogen (Plasmodiophora brassicae) influences auxin signaling to regulate auxin homeostasis. Plants 2:726–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jäschke D, Dugassa-Gobena D, Karlovsky P, Vidal S, Ludwig-Müller J (2010) Suppression of clubroot (Plasmodiophora brassicae) development in Arabidopsis thaliana by the endophytic fungus Acremonium alternatum. Plant Pathol 59:100–111

    Article  CAS  Google Scholar 

  • Joo GJ, Kim YM, Kim JW, Kim WC, Rhee IK, Choi YH, Kim JH (2004) Biocontrol of cabbage clubroot by the organic fertilizer using Streptomyces sp. AC-3. Kor J Microbiol Biotechnol 32:173–178

    Google Scholar 

  • Kageyama K, Asano T (2009) Life cycle of Plasmodiophora brassicae. J Plant Growth Regul 28:203–211

    Article  CAS  Google Scholar 

  • Kammerich J, Beckmann S, Scharafat I, Ludwig-Müller J (2014) Suppression of the clubroot pathogen Plasmodiophora brassicae by plant growth promoting formulations in roots of two Brassica species. Plant Pathol 63:846–857

    Article  CAS  Google Scholar 

  • Kobelt P (2000) Die Verbreitung von sekundären Plasmodien von Plasmodiophora brassicae (Wor.) im Wurzelgewebe von Arabidopsis thaliana nach immunhistologischer Markierung des plasmodialen Zytoskeletts. Dissertation, Institut für Angewandte Genetik, Freie Universität Berlin, Germany

    Google Scholar 

  • Kofoet A, Fischer K (2007) Evaluation of plant resistance improvers to control Peronospora destructor, P. parasitica, Bremia lactucae and Pseudoperonospora cubensis. J Plant Dis Protect 114:54–61

    Article  CAS  Google Scholar 

  • Kowata-Dresch LS, May-De Mio LL (2012) Clubroot management of highly infested soils. Crop Prot 35:47–52

    Article  CAS  Google Scholar 

  • Kroll TK, Lacy GH, Moore LD (1983) A quantitative description of the colonization of susceptible and resistant radish plants by Plasmodiophora brassicae. J Phytopathol 108:97–105

    Article  Google Scholar 

  • Kuginuki Y, Hiroaki Y, Hirai M (1999) Variation in virulence of Plasmodiophora brassicae in Japan tested with clubroot-resistant cultivars of Chinese cabbage (Brassica rapa L. ssp. pekinensis). Eur J Plant Pathol 105:327–332

    Article  Google Scholar 

  • Kühne S, Burth U, Marx P (2006) Biologischer Pflanzenschutz im Freiland. Eugen Ulmer, Stuttgart

    Google Scholar 

  • Lahlali R, Peng G (2014) Suppression of clubroot by Clonostachys rosea via antibiosis and induced host resistance. Plant Pathol 63:447–455

    Article  CAS  Google Scholar 

  • Lahlali R, Peng G, McGregor L, Gossen BD, Hwang SF, McDonald MR (2011) Mechanisms of the biofungicide Serenade (Bacillus subtilis GST713) in suppressing clubroot. Biocontrol Sci Technol 21:1351–1362

    Article  Google Scholar 

  • Lahlali R, Peng G, Gossen BD, McGregor L, Yu FQ, Hynes RK, Hwang S-F, McDonald MR, Boyetchko SM (2013) Evidence that the biofungicide Serenade (Bacillus subtilis) suppresses clubroot on canola via antibiosis and induced host resistance. Phytopathology 103:245–254

    Article  CAS  PubMed  Google Scholar 

  • Lahlali R, McGregor L, Song T, Gossen BD, Narisawa K, Peng G (2014) Heteroconium chaetospira induces resistance to clubroot via upregulation of host genes involved in jasmonic acid, ethylene, and auxin biosynthesis. PLoS One 9(4):e94144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269

    Article  CAS  PubMed  Google Scholar 

  • Lee SO, Choi GJ, Choi YH et al (2008) Isolation and characterization of endophytic actinomycetes from Chinese cabbage roots as antagonists to Plasmodiophora brassicae. J Microbiol Biotechnol 18:1741–1746

    CAS  PubMed  Google Scholar 

  • Lovelock DA, Donald CE, Conlan XA, Cahill DM (2013) Salicylic acid suppression of clubroot in broccoli (Brassicae oleracea var. italica) caused by the obligate biotroph Plasmodiophora brassicae. Australas Plant Pathol 42:141–153

    Article  CAS  Google Scholar 

  • Ludwig-Müller J (2009) Plant defence—what can we learn from clubroots? Australas Plant Pathol 38:318–324

    Article  Google Scholar 

  • Ludwig-Müller J, Kasperczyk N, Schubert B, Hilgenberg W (1995) Identification of salicylic acid in Chinese cabbage and its possible role during root infection with Plasmodiophora brassicae. Curr Top Phytochem 14:39–45

    Google Scholar 

  • Ludwig-Müller J, Prinsen E, Rolfe S, Scholes J (2009) Metabolism and plant hormone action during the clubroot disease. J Plant Growth Regul 28:229–244

    Article  CAS  Google Scholar 

  • Ludwig-Müller J, Jülke S, Geiß K, Richter F, Sola I, Rusak G, Mithöfer A, Keenan S, Bulman S (2015) A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid. Mol Plant Pathol 16:349–364

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S, Azzarello E, Mugnai S, Briand X (2006) Marine bioactive substances (IPA extract) improve foliar ion uptake and water tolerance in potted Vitis vinifera plants. Adv Hortic Sci 20:156–161

    Google Scholar 

  • Metting W, Zimmerman J, Crouch IJ, Van Staden J (1990) Agronomic uses of seaweed and micro-algae. In: Akatsuka I (ed) Introduction to applied phycology. SPB, The Hague, pp 269–307

    Google Scholar 

  • Mithen R, Magrath R (1992) A contribution to the life history of Plasmodiophora brassicae: secondary plasmodia development in root galls of Arabidopsis thaliana. Mycol Res 96:877–885

    Article  Google Scholar 

  • Moody SA, Piearce TG, Dighton J (1996) Fate of some fungal spores associated with wheat straw decomposition on passage through the guts of Lumbricus terrestris and Aporrectodea longa. Soil Biol Biochem 28:533–537

    Article  CAS  Google Scholar 

  • Muday GK, Murphy AS (2002) An emerging model of auxin transport regulation. Plant Cell 14:293–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami H, Tsushima S, Akimoto T, Shishido Y (2001) Reduction of spore density of Plasmodiophora brassicae in soil by decoy plants. J Gen Plant Pathol 67:85–88

    Article  Google Scholar 

  • Murakami H, Tsushima S, Kuroyanagi Y, Shishido Y (2002) Reduction in resting spore density of Plasmodiophora brassicae and clubroot severity by liming. Soil Sci Plant Nutr 48:685–691

    Article  CAS  Google Scholar 

  • Myers DF, Campbell RN (1985) Lime and the control of clubroot of crucifers: effects of pH, calcium, magnesium and their interactions. Phytopathology 75:670–673

    Article  CAS  Google Scholar 

  • Naiki T, Dixon GR (1987) The effects of chemicals on developmental stages of Plasmodiophora brassicae clubroot. Plant Pathol 36:316–327

    Article  CAS  Google Scholar 

  • Nakamura Y, Itakura J, Matsuzaki I (1995) Influence of the earthworm Pheretima hilgendorfi (Megascolecidae) on Plasmodiophora brassicae clubroot galls of cabbage seedlings in pot. Edaphologia 54:39–41

    Google Scholar 

  • Narisawa K, Tokumasu S, Hashiba T (1998) Suppression of clubroot formation in Chinese cabbage by the root endophytic fungus, Heteroconium chaetospira. Plant Pathol 47:206–210

    Article  Google Scholar 

  • Narisawa K, Ohiki KT, Hashiba T (2000) Suppression of clubroot and Verticillium yellows in Chinese cabbage in the field by the root endophytic fungus, Heteroconium chaetospira. Plant Pathol 49:141–146

    Article  Google Scholar 

  • Narisawa K, Shimura M, Usuki F, Fukuhara S, Hashiba T (2005) Effects of pathogen density, soil moisture, and soil pH on biological control of clubroot in Chinese cabbage by Heteroconium chaetospira. Plant Dis 89:285–290

    Article  Google Scholar 

  • Niwa R, Nomura Y, Osaki M, Ezawa T (2008) Suppression of clubroot disease under neutral pH caused by inhibition of spore germination of Plasmodiophora brassicae in the rhizosphere. Plant Pathol 57:445–452

    Article  Google Scholar 

  • Päsold S, Ludwig-Müller J (2013) Clubroot (Plasmodiophora brassicae) formation in Arabidopsis is reduced after treatment with prohexadione-calcium, an inhibitor for oxoglutaric acid dependent dioxygenases. Plant Pathol 62:1357–1365

    Article  CAS  Google Scholar 

  • Päsold S, Siegel I, Seidel C, Ludwig-Müller J (2010) Flavonoid accumulation in Arabidopsis thaliana root galls caused by the obligate biotrophic pathogen Plasmodiophora brassicae. Mol Plant Pathol 11:545–562

    Article  PubMed  Google Scholar 

  • Peng G, Hwang SF, McDonald MR, Lahlali R, Gossen BD, Hynes RH, Boyetchko SM (2010) Management of clubroot (Plasmodiophora brassicae) with microbial and synthetic fungicides. Phytopathology 100:S99

    Google Scholar 

  • Peng G, McGregor L, Lahlali R, Gossen BD, Hwang SF, Adhikari KK, Strelkov SE, McDonald MR (2011) Potential biological control of clubroot on canola and crucifer vegetable crops. Plant Pathol 60:566–574

    Article  Google Scholar 

  • Peng G, Lahlali R, Hwang S-F, Pageau D, Hynes RK, McDonald MR, Gossen BD, Strelkov SE (2014) Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Can J Plant Pathol 36(S1):99–112

    Article  CAS  Google Scholar 

  • Rademacher W (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Physiol Plant Biol 51:501–531

    Article  CAS  Google Scholar 

  • Rennie DC, Holtz MD, Turkington TK, Leboldus JM, Hwang S-F, Howard RJ, Strelkov SE (2015) Movement of Plasmodiophora brassicae resting spores in windblown dust. Can J Plant Pathol. doi:10.1080/07060661.2015.1036362

    Google Scholar 

  • Robak J (1994) Crop rotation effect on clubroot disease decrease. Acta Hortic 371:223–226

    Article  Google Scholar 

  • Sakai R, Sato R, Niki H, Sakamura S (1970) Biological activity of phyllosinol, a phytotoxic compound isolated from a culture filtrate of Phyllosticta sp. Plant Cell Physiol 11:907–920

    CAS  Google Scholar 

  • Schuller A, Kehr J, Ludwig-Müller J (2014) Laser microdissection coupled to transcriptional profiling of Arabidopsis roots inoculated by Plasmodiophora brassicae indicates a role for brassinosteroids in clubroot formation. Plant Cell Physiol 55:392–411

    Article  CAS  PubMed  Google Scholar 

  • Schwelm A, Fogelqvist J, Knaust A, Jülke S, Lilja T, Bonilla-Rosso G, Karlsson M, Shevchenko A, Choi SR, Dhandapani V, Kim HG, Park JY, Lim YP, Ludwig-Müller J, Dixelius C (2015) The genome sequence of the plant pathogenic Rhizarian Plasmodiophora brassicae reveals insights in its biotrophic life cycle and ancestry of chitin synthases. Sci Rep. doi:10.1038/srep11153

    PubMed  PubMed Central  Google Scholar 

  • Sharma K, Gossen BD, McDonald MR (2011) Effect of temperature on primary infection by Plasmodiophora brassicae and initiation of clubroot symptoms. Plant Pathol 60:830–838

    Article  Google Scholar 

  • Siemens J, Nagel M, Ludwig-Müller J, Sacristán MD (2002) The interaction of Plasmodiophora brassicae and Arabidopsis thaliana: parameters for disease quantification and screening of mutant lines. J Phytopathol 150:592–605

    Article  Google Scholar 

  • Siemens J, Keller I, Sarx J, Kunz S, Schuller A, Nagel W, Schmülling T, Parniske M, Ludwig-Müller J (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol Plant Microbe Interact 19:480–494

    Article  CAS  PubMed  Google Scholar 

  • Siemens J, Gonzales M-C, Wolf S, Hofmann C, Greiner S, Du Y, Rausch T, Roitsch T, Ludwig-Müller J (2011) Extracellular invertase is involved in the regulation of the clubroot disease in Arabidopsis thaliana. Mol Plant Pathol 12:247–262

    Article  CAS  PubMed  Google Scholar 

  • Smelt JH, Leistra M (1974) Conversion of metham-sodium to methyl isothiocyanate and basic data on the behaviour of methyl isothiocyanate in soil. Pestic Sci 5:401–407

    Article  CAS  Google Scholar 

  • Strelkov SE, Hwang SF, Howard RJ, Hartman M, Turkington TK (2011) Progress towards the sustainable management of clubroot (Plasmodiophora brassicae) of canola on the Canadian Prairies. Prairie Soils Crops J 4:114–121

    Google Scholar 

  • Takahashi K, Yamaguchi T (1987) An improved method for estimating the number of resting spores of Plasmodiophora brassicae in soil. Ann Phytopathol Soc Jpn 53:507–515

    Article  Google Scholar 

  • Takahashi H, Takita K, Kishimoto T, Mitsui T, Hori H (2002) Ca2+ is required by clubroot resistant turnip cells for transient increases in PAL activity that follow inoculation with Plasmodiophora brassicae. J Phytopathol 150:529–535

    Article  CAS  Google Scholar 

  • Wakeham AJ, White JG (1996) Serological detection in soil of Plasmodiophora brassicae resting spores. Physiol Mol Plant Pathol 48:289–303

    Article  Google Scholar 

  • Wallenhammar AC (1996) Prevalence of Plasmodiophora brassicae in a spring oilseed rape growing area in central Sweden and factors influencing soil infestation levels. Plant Pathol 45:710–719

    Article  Google Scholar 

  • Wallenhammar A-C, Almquist C, Söderström M, Jonsson A (2012) In-field distribution of Plasmodiophora brassicae measured using quantitative real-time PCR. Plant Pathol 61:16–28

    Article  CAS  Google Scholar 

  • Wang L, Li B, Chen X, Shi Y, Zhou Q, Qiu H, Ibrahim M, Xie GL, Sun GC (2012) Effect of chitosan on seed germination, seedling growth and the clubroot control in Chinese cabbage. J Food Agric Environ 10:673–675

    CAS  Google Scholar 

  • Webster MA, Dixon GR (1991a) Calcium, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae. Mycol Res 95:65–73

    Google Scholar 

  • Webster MA, Dixon GR (1991b) Boron, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae. Mycol Res 95:74–79

    Article  CAS  Google Scholar 

  • Winding A, Rønn R, Hendriksen NB (1997) Bacteria and protozoa in soil microhabitats as affected by earthworms. Biol Fertil Soils 24:133–140

    Article  Google Scholar 

  • Wite D, Mattner SW, Porter IJ, Arioli T (2015) The suppressive effect of a commercial extract from Durvillaea potatorum and Ascophyllum nodosum on infection of broccoli by Plasmodiophora brassicae. J Appl Phycol. doi:10.1007/s10811-015-0564-y

    PubMed  PubMed Central  Google Scholar 

  • Woronin M (1878) Plasmodiophora brassicae Urheber der Kohlpflanzen—Hernie. Jahrb Wiss Bot 11:548–574 [translated by Chupp C (1934) Phytopathological classics no. 4. American Phytopathological Society, St. Paul, MN]

    Google Scholar 

  • Zhou L, Zhang L, He Y, Liu F, Li M, Wang Z, Ji G (2014) Isolation and characterization of bacterial isolates for biological control of clubroot on Chinese cabbage. Eur J Plant Pathol 140:159–168

    Article  CAS  Google Scholar 

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Acknowledgments

Work in the author’s laboratory was funded over the years by the State of Saxony (SMWK and SAB), the Deutsche Forschungsgemeinschaft (DFG), Bundesministerium für Bildung und Forschung (BMBF), Bundesministerium für Landwirtschaft und Ernährung (BLME), and the Deutsche Akademische Austauschdienst (DAAD). Apologies to all colleagues whose work could not be included even though they contributed significantly to the clubroot world.

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Ludwig-Müller, J. (2016). Belowground Defence Strategies Against Clubroot (Plasmodiophora brassicae). In: Vos, C., Kazan, K. (eds) Belowground Defence Strategies in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-42319-7_9

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