Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-26T23:47:43.730Z Has data issue: false hasContentIssue false
  • English
  • Français

Managing clubroot disease (caused by Plasmodiophora brassicae Wor.) by exploiting the interactions between calcium cyanamide fertilizer and soil microorganisms

Published online by Cambridge University Press:  17 October 2016

G. R. DIXON
G. R. DIXON*
Affiliation:
School of Agriculture, Policy and Development, Earley Gate, University of Reading, Reading, Berkshire RG6 6AR, UK
*
*To whom all correspondence should be addressed. Email: geoffrdixon@gmail.com/g.r.dixon@reading.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Calcium cyanamide is a nitrogenous fertilizer used predominantly for over a century in field and glasshouse vegetable and salad production. The current review draws together, for the first time, knowledge concerning the biological properties of the compound that benefit crop production by encouraging sustainable soil health and quality. This is achieved through the increase of microorganisms antagonistic to plant pathogens. The review also reports on the natural occurence and degradation of cyanamide. The literature survey provides a perspective of research from the early 1900s to current studies. This identifies that nitrogen is released steadily into the rhizosphere from this fertilizer. Calcium is also readily available for plant roots and promotes the alkaline soil conditions beneficial to benign microorganisms. Consequently, soil suppressiveness towards organisms such as Plasmodiophora brassicae, the cause of clubroot disease in brassicas, develops. The effects of calcium and accompanying changes in soil pH values are discussed in relation to the life-cycle stages of P. brassicae and the development of clubroot disease. Formulations of calcium cyanamide contain the dimeric form, dicyandiamide. This compound slows soil nitrification and subsequent nitrate leaching into ground waters, reducing potential pollution. Calcium cyanamide is normally used for growing specialized fresh produce and is not available in quantities comparable with ammoniacal fertilizers. It is contended, however, that it has properties deserving wider assessment because of their implications for sustainable cropping.

Type
Crops and Soils Review
Information
The Journal of Agricultural Science , Volume 155 , Issue 4 , May 2017 , pp. 527 - 543
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alix, K., Lariagon, C., Delourme, R. & Manzanares-Dauleux, M. J. (2007). Exploiting natural genetic diversity and mutant resources of Arabidopsis thaliana to study the A. thaliana-Plasmodiophora brassicae interaction. Plant Breeding 126, 218–221.Google Scholar
Allison, F. E. (1924). The effect of cyanamid and related compounds on the number of microorganisms in soil. Journal of Agricultural Research 28, 1159–1166.Google Scholar
Amberger, A. (1986). Potentials of nitrification inhibitors in modern N-fertilizer management. Zeitschrift für Pflanzenernährung und Bodenkunde 149, 469–484.Google Scholar
Amberger, A. (1989). Research on dicyandiamide as a nitrification inhibitor and future outlook. Communications in Soil Science and Plant Analysis 20, 1933–1955.Google Scholar
Anderson, A. (1855). Report of the disease of finger and toe in turnips. Transactions of the Highland and Agricultural Society of Scotland 3, 118–140.Google Scholar
Anon (1996). Federal Government Position Paper on the Decision of the Bundesrat on the Decree Amending Fertiliser Regulations. Berlin: Federal Ministry of Food, Agriculture and Forestry, Berlin letter of March 25th 1996, reference: 312–3132/23.Google Scholar
Anon (2008 a). 100 years of calcium cyanamide from Trostberg. Monatsschift Magazin für den Gartenbau-Profi (Magazine for Professional Horticulture). August 2008, 296–297.Google Scholar
Anon (2008 b). AGP – What is a Healthy Soil? Rome: FAO. Available from: http://www.fao.org/agriculture/crops/thematic-sitemap/theme/spi/soil-biodiversity/the-nature-of-soil/what-is-a-healthy-soil/en/ (verified 24 March 2016).Google Scholar
Anon (2012). Brassica Research News no 1. Stoneleigh, Warwickshire: Horticultural Development Company (HDC, now Agriculture & Horticulture Development Board AHDB – Horticulture) and Brassica (now British) Growers Association (BGA). June 2008, 3 pages.Google Scholar
Antille, D. L., Gallar, L., Miller, P. C. H. & Godwin, R. J. (2015). An investigation into the fertilizer particle dynamics off-the-disc. Applied Engineering in Agriculture 31, 49–60.Google Scholar
Apaydin, A., Deligöz, I., Kar, H., Kibar, B. & Karaagac, O. (2010). An investigation on clubroot disease (Plasmodiophora brassicae Wor.) races in the Black Sea Region of Turkey. Gaziosmanpaşa Üniversitesi (GOU). Zirat Fakültesi Dergisi 28, 57–60.Google Scholar
Arie, T., Kobayashi, G., Okada, G., Kono, Y. & Yamaguchi, I. (1998). Control of soilborne clubroot disease of cruciferous plants by epoxydon from Phoma glomerata . Plant Pathology 47, 743–748.Google Scholar
Ashby, S. F. (1905). Note on the fate of calcium cyanamide in the soil. Journal of Agricultural Science, Cambridge 1, 358–360.Google Scholar
Bauchhenb, J. (1994). Influence of Alzodef and Perlka on earthworms (Einfluß von Alzodef und Perlka auf Regenwürmer). Report KA-187. Freising, Germany: Bayerische Landesanstalt für Bodenkultur.und Planzenbau.Google Scholar
Belec, C., Trembaly, N. & Coulombe, J. (2004). Liming and calcium cyanamid for clubroot control in cauliflower. Acta Horticulturae 635, 41–46.Google Scholar
Bell, M. A., Fischer, R. A., Byerlee, D. & Sayre, K. (1995). Genetic and agronomic contribitions to yield gains: a case study for wheat. Field Crops Research 44, 55–65.Google Scholar
Benyue, Z. (1995). Research on efficacy of LN fertiliser with chemical function of controlling Chinese cabbage clubroot. Journal of Agricultural Science of Zheijang University 6, 300–301.Google Scholar
Bjälfve, G. (1957). The nitrification of calcium cyanamide and its effects on the soil microflora. Annals of the Agricultural College of Sweden (Kungliga Lantbrukshögskolans Annaler) 23, 423–456.Google Scholar
Bletsos, F. A. (2006). Grafting and calcium cyanamide as alternatives to methyl bromide for greenhouse eggplant production. Scientia Horticulturae 107, 325–331.Google Scholar
Borneman, J. & Triplett, E. W. (1997). Molecular microbial diversity in soil from Eastern Amazonia: evidence of unusual micro-organisms and microbial population shifts associated with deforestation. Applied and Environmental Microbiology 63, 2647–2653.Google Scholar
Bosch, M. & Amberger, A. (1983). Influence of long-term fertilizing with different forms of nitrogen fertilizer on pH, humic fractions, biological activity and dynamics of nitrogen of an arable brown earth. (Einfluß langjähriger Düngung mit verschiedenen N-formen auf pH-Wert, Humusfraktionen, bilogische Aktivität und Stickstoffdynamik einer Acker-Braunerde) Journal of Plant Nutrition and Soil Science (Zeitschrift fur Pflanzenernähr Bodenkde) 146, 714–724.Google Scholar
Bourbos, V. A., Skoudridakis, M. T., Darakis, G. A. & Koulizakis, M. (1997). Calcium cyanamide and soil solarisation for the control Fusarium solani f. sp. cucurbitae in greenhouse cucumber. Crop Protection 16, 383–386.Google Scholar
Brochado-Miranda, V. H. (1975). Influence of nitrogenous fertilizers upon some soil characteristics. Landwirtschaftliche Forschung 29, 21–27.Google Scholar
Bronick, C. J. & Lal, R. (2005). Soil structure and management: a review. Geoderma 124, 3–22.Google Scholar
Broughton, W. J. (1981). Nitrogen Fixation vol. 1: Ecology. Oxford, UK: The Clarendon Press.Google Scholar
Broughton, W. J. (1982). Nitrogen Fixation vol. 2: Rhizobium. Oxford, UK: The Clarendon Press.Google Scholar
Broughton, W. J. (1983). Nitrogen Fixation vol. 3: Legumes. Oxford, UK: The Clarendon Press.Google Scholar
Broughton, W. J. (1986). Nitrogen Fixation vol. 4: Molecular Biology. Oxford, UK: The Clarendon Press.Google Scholar
Buczacki, S. T. & Cadd, S. E. (1976). Glasshouse evaluation of systemic compounds, derivatives of dithiocarbamic acid and other fungicides for the control of clubroot. Annals of Applied Biology 84, 43–50.Google Scholar
Buczacki, S. T. & Moxham, S. E. (1983). Structure of the resting spore wall of Plasmodiophora brassicae revealed by electron microscopy and chemical digestion. Transactions of the British Mycological Society (now Mycological Research) 81, 221–231.Google Scholar
Burki, F., Kudryavtsev, A., Matz, M. V., Aglyamova, G. V., Bulman, S., Fiers, M., Keeling, P. J. & Pawlowski, J. (2010). Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evolutionary Biology 10, 377. DOI: 10.1186/1471-2148-10-377 Google Scholar
Burns, I. G., Hammond, J. P. & White, P. J. (2010). Precision placement of fertiliser for optimising the early nutrition of vegetable crops – a review of the implications for the yield and quality of crops and their nutrient use efficiency. Acta Horticulturae 852, 177–187.Google Scholar
Campbell, R. N., Greathead, A. S., Myers, D. F. & de Boer, G. J. (1985). Factors related to control of clubroot of crucifers in the Salinas Valley of California. Phytopathology 75, 665–670.Google Scholar
Chai, A. L., Xie, X. W., Shi, Y. X. & Li, B. J. (2014). Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Canadian Journal Plant Pathology 36, Suppl 1, 142–153.Google Scholar
Challinor, A. J., Watson, J., Lobell, D. B., Howden, S. M., Smith, D. R. & Chetri, N. (2014). A meta-analysis of crop yield under climate change and adaptation. Nature Climate Change 4, 287–291.CrossRefGoogle Scholar
Chupp, C. (1934). Plasmodiophora brassicae: The Cause of the Cabbage Hernia, 1878. A Translation by Charles Chupp; With a Biographical Sketch by the Translator. Phytopathological Classics, No. 4. St Paul, MN, USA: American Phytopathological Society.Google Scholar
Colhoun, J. (1958). Club Root Disease of Crucifers caused by Plasmodiophora brassicae Woron.: a Monograph. Phytopathological Paper no 3. Kew, Surrey, UK: The Commonwealth Mycological Institute.Google Scholar
Cook, W. R. I. (1933). A monograph of the Plasmodiophorales. Archive für Protistenkunde 80, 179–254.Google Scholar
Cornforth, I. S. (1971). Calcium cyanamide in agriculture. Soils and Fertilisers 34, 463–468.Google Scholar
Crookes, W. (1900). The Wheat Problem. London: John Murray.Google Scholar
Crowther, E. M. & Richardson, H. L. (1932). Studies on calcium cyanamide. 1. The decomposition of calcium cyanamide in the soil and its effects on germination, nitrification and soil reaction. Journal of Agricultural Science, Cambridge 22, 300–334.Google Scholar
Diederichsen, E., Frauen, M. & Ludwig-Muller, J. (2014). Clubroot disease management challenges from a German perspective. Canadian Journal of Plant Pathology 36, (Suppl. 1), 85–98.CrossRefGoogle Scholar
Dixon, G. R. (2006). The biology of Plasmodiophora brassicae Wor. – a review of recent advances. Acta Horticulturae 706, 271–282.CrossRefGoogle Scholar
Dixon, G. R. (2007). Vegetable Brassicas and Related Crucifers. Crop Production Science in Horticulture no 14. Wallingford, UK: CAB International.Google Scholar
Dixon, G. R. (2009 a). Calcium cyanamide - 100 years of successful integrated control. Plant Protection Science 45, 37–38.Google Scholar
Dixon, G. R. (2009 b). The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation 28, 194–202.Google Scholar
Dixon, G. R. (2009 c). Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation 28, 212–228.Google Scholar
Dixon, G. R. (2009 d). The impact of climate and global change on crop production. In Climate Change: Observed Impacts on Planet Earth (Ed. Letcher, T. M.), pp. 307–324. Oxford, UK: Elsevier.CrossRefGoogle Scholar
Dixon, G. R. (2010). Calcium and pH as parts of a coherent control strategy for clubroot disease (Plasmodiophora brassicae). Acta Horticulturae 867, 151–156.Google Scholar
Dixon, G. R. (2012 a). Calcium cyanamide-a synoptic review of an environmentally benign fertiliser which enhances soil health. Acta Horticulturae 938, 211–217.Google Scholar
Dixon, G. R. (2012 b). Climate change – impact on crop growth and food production, and plant pathogens. Canadian Journal of Plant Pathology 34, 362–379.CrossRefGoogle Scholar
Dixon, G. R. (2014). Clubroot (Plasmodiophora brassicae Woronin) – an agricultural and biological challenge worldwide. Canadian Journal of Plant Pathology 36, (Suppl. 1), 5–18.Google Scholar
Dixon, G. R. (2015). Water, Irrigation and Plant Diseases. CAB Reviews 2015, no. 10. Wallingford, UK: CABI.Google Scholar
Dixon, G. R. & Brokenshire, T. (1981). Chemical control of clubroot (Plasmodiophora brassicae). In Crop Protection in Northern Britain. Proceedings of a Conference held at Dundee University 17–19 March 1981 (Ed. Williams, G. H.), pp. 325–329. Farnham, UK: The British Crop Protection Council.Google Scholar
Dixon, G. R. & Tilston, E. L. (2010). Soil-borne pathogens and their interaction with the soil environment. In Soil Microbiology and Sustainable Crop Production (Eds Dixon, G. R. & Tilston, E. L.), pp. 197–272. Dordrecht, The Netherlands: Springer Publications.Google Scholar
Dixon, G. R. & Walsh, U. F. (1998). Suppression of plant pathogens by organic extracts – a review. Acta Horticulturae 469, 383–390.CrossRefGoogle Scholar
Dixon, G. R. & Webster, M. A. (1988). Antagonistic effects of boron, calcium and pH on pathogenesis caused by Plasmodiophora brassicae Woronin (clubroot) – a review of recent work. Crop Research 28, 83–95.Google Scholar
Dixon, G. R. & Williamson, C. J. (1985). Factors affecting the use of calcium cyanamide for control of Plasmodiophora brassicae . In Proceedings of the Better Brassicas 1984 Conference, St. Andrews (Eds Macfarlane Smith, W. H. & Hodgkin, T.), pp. 238–244. Dundee: Scottish Crop Research Institute.Google Scholar
Dixon, G. R. & Wilson, F. (1983). Evaluation of calcium cyanamide for control of Plasmodiophora brassicae (clubroot). Annals of Applied Biology 102, (Suppl), 50–51.Google Scholar
Dixon, G. R., Naiki, T., Webster, A. & Wilson, F. (1987). Integrated use of boron, calcium cyanamide and nitrogen for control of clubroot (Plasmodiophora brassicae). In Crop Protection in Northern Britain (compiler Ed. Williams, G. R.), pp. 399–404. Farnham: The British Crop Protection Council.Google Scholar
Donald, E. C. & Porter, I. J. (2014). Clubroot in Australia: the history and impact of Plasmodiophora brassicae in brassica crops and research efforts directed towards its control. Canadian Journal of Plant Pathology 36, (Suppl. 1), 66–84.Google Scholar
Donald, E. C. & Porter, I. J. (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 . Australasian Plant Pathology 33, 585–589.Google Scholar
Donald, E. C., Lawrence, J. M. & Porter, I. J. (2004). Influence of particle size and application method on the efficacy of calcium cyanamide for control of clubroot of vegetable brassicas. Crop Protection 23, 297–303.Google Scholar
Donald, E. C., Porter, I. J., Faggian, R. & Lancaster, R. A. (2006). An integrated approach to the control of clubroot in vegetable brassica crops. Acta Horticulturae 706, 283–300.Google Scholar
Donaldson, S. P. & Deacon, J. W. (1993). Changes in motility of Pythium zoospores induced by calcium and calcium-modulating drugs. Mycological Research 97, 877–883.Google Scholar
Doran, J. W. & Zeiss, M. R. (2000). Soil health and sustainability: managing the biotic component of soil quality. Applied Soil Ecology 15, 3–11.CrossRefGoogle Scholar
Doran, J. W., Sarrantonio, M. & Liebig, M. A. (1996). Soil health and sustainability. Advances in. Agronomy 56, 2–54.Google Scholar
Einhorn, G. H., Bochow, H., Huber, J. & Krebs, B. (1991). Methodological studies to detect antagonists of the clubroot pathogen Plasmodiophora brassicae Wor. Archive für Phytopathologie und Pflanzenschutz 27, 205–208.Google Scholar
Ernst, F. A. (1928). Fixation of Atmospheric Nitrogen. London: Chapman & Hall.Google Scholar
European Union (2008). Commission Regulation (EC) No 1107/2008 of 7 November 2008 amending Regulation (EC) No 2003/2003 of the European Parliament and of the Council relating to fertilisers for the purposes of adapting Annexes I and IV thereto to technical progress. Official Journal of the European Union L299 51, 13–16.Google Scholar
Eveillard, E. (2005). Improve Mineral N Efficiency to Protect the Environment: the French Experience. Paris, France: UNIFA union des Industries de la Fertilisation.Google Scholar
Fletcher, J. T., Hims, M. J., Archer, F. C. & Brown, A. (1982). Effects of adding calcium and sodium salts to field soils on the incidence of clubroot. Annals of Applied Biology 100, 245–251.CrossRefGoogle Scholar
Frank, A. (1908). Chemical industry in relation to agriculture. Journal of the Society of Chemical Industry 27, 1093–1100.Google Scholar
Frank, D. A. & Groffman, P. M. (2009). Plant rhizospheric N processes: what we don't know and why we should care. Ecology 90, 1512–1519.Google Scholar
Garbeva, P., van Veen, J. A. & van Elsas, J. D. (2004). Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppression. Annual Review of Phytopathology 42, 243–270.Google Scholar
Garrett, D. (1958). The Biology of Root Invading Fungi. Cambridge, UK: Cambridge University Press.Google Scholar
Gianquinto, G., Sambo, P. & Bona, S. (2003). The use of SPAD-502 chlorophyll meter for dynamically optimising the nitrogen supply in potato crop: a methodological approach. Acta Horticulturae 627, 217–224.Google Scholar
Greenwood, D. J. (1982). Nitrogen supply and crop yield: the global scene. Plant and Soil 67, 45–59.Google Scholar
Güthner, T. & Mertschenk, B. (2006). Cyanamides. In Ullmann's Enclyclopedia of Industrial Chemistry (Ed. Elvers, B.), pp. 645–664. Berlin, Germany: Wiley-VCH Verllag GmbH & Co. KgaA.Google Scholar
Haenseler, C. M. & Moyer, T. R. (1937). Effect of calcium cyanamide on the soil microflora with special reference to certain plant parasites. Soil Science 43, 133–152.Google Scholar
Hall, A. D. (1905). Calcium cyanamide. Journal of Agricultural Science, Cambridge 1, 146–148.Google Scholar
Harling, R. & Oxley, S. (2007). Clubroot Disease of Oilseed Rape and Other Brassica Crops. Technical Note TN602. Edinburgh, UK: Scottish Agricultural College.Google Scholar
Harling, R., Stewart, K. & Gladders, P. (2007). Clubroot Control Using Novel and Sustainable Methods. Project report (HH322TFV), London: Department for the Environment, Food and Rural Affairs (Defra).Google Scholar
Hartwig, N. L. & Ammon, H. U. (2002). Cover crops and living mulches. Weed Science 50, 688–699.Google Scholar
Hinsinger, P., Gobran, G. R., Gregory, P. J. & Wenzel, W. W. (2005). Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist 168, 293–303.Google Scholar
Horiuchi, S., Hori, M., Takashi, S. & Shimizu, K. (1983). Factors responsible for the development of clubroot-suppressing effect in soil solarization. Bulletin of the Chugoku National Agricultural Experiment Station E20, 25–48.Google Scholar
Hsieh, W-H. & Wang, J.-F. (1986). Investigation on suppressive soils of clubroot of crucifers in Taiwan. Plant Protection Bulletin (Taiwan R.O.C.) 28, 353–362.Google Scholar
Huang, H. C. & Sun, S. K. (1991). Effects of S-H mixture or Perlka™ on carpogenic germination and survival of sclerotia of Sclerotinia sclerotiorum . Soil Biology and Biochemistry 23, 809–813.Google Scholar
Humpherson-Jones, F. M., Dixon, G. R., Craig, M. A. & Ann, D. M. (1992). Control of clubroot using calcium cyanamide – a review. In Brighton Crop Protection Conference, Pests and Diseases 1992, Vol. 3 (Session editor Ed. Russell, P. E.), pp. 1147–1154. Farnham, Surrey, UK: British Crop Protection Council.Google Scholar
Jacob, K. D., Allison, F. E. & Braham, J. M. (1924). Chemical and biological studies with Cyanamid and some of its transformation products. Journal of Agricultural Research 28, 37–69.Google Scholar
Jones, D. & Gray, E. G. (1973). Factors affecting germination of sclerotia of Sclerotinia sclerotiorum from peas. Transactions of the British Mycological Society (now Mycological Research) 60, 495–500.Google Scholar
Kamo, T., Hiradate, S. & Fujii, Y. (2003). First isolation of natural cyanamide as a possible allelochemical from hairy vetch (Vicia villosa). Journal of Chemical Ecology 29, 275–283.Google Scholar
Kamo, T., Sato, M., Kato, K., Hiradate, S., Nakajima, E., Fujii, Y. & Hirota, M. (2006). Quantification of cyanamide contents in herbaceous plants. Bioscience, Biotechnology and Biochemistry 70, 2310–2312.CrossRefGoogle ScholarPubMed
Kamo, T., Takemura, T., Wasano, N., Fujii, Y. & Hiradate, S. (2012). Quantification of cyanamide in young seedlings of Vicia species, Lens culinaris and Robinia pseudo-acacia by gas chromatography-mass spectrometry. Bioscience Biotechnology and Biochemistry 76, 1416–1418.Google Scholar
Karling, J. S. (1968). The Plasmodiophorales – Including a Complete Host Index, Bibliography and a Description of Diseases Caused by Species of this Order. New York: Hafner Publishing Company.Google Scholar
Kirkby, E. A. (1968). Influence of ammonium and nitrate nutrition on the cation-anion balance and nitrogen and carbohydrate metabolism of white mustard plants grown in dilute nutrient solutions. Soil Science 105, 133–141.Google Scholar
Klasse, H. J. (1996). Calcium cyanamide–an effective tool to control clubroot – a review. Acta Horticulturae 407, 403–409.Google Scholar
Klasse, H. J. (1999). Calcium cyanamide-a unique source of nitrogen promoting healthy growth and improving crop quality of vegetables. In Improved Crop Quality by Nutrient Management (Eds Anac, D. & Martin-Prével, P.), pp. 233–235.CrossRefGoogle Scholar
Klasse, H. J. (2002). Calcium cyanamide-an important tool in methyl bromide replacement strategies. Paper presented at 3rd International Conference for the Alternatives to Methyl Bromide, Heraklion, Crete 6th to 9th December 1999 and published online by the Ministry of Agriculture, Athens, Greece Available from wdelword_www.minagric.gr/greek/data/files2251/PERLKLA1.DOC (verified 13 September 2016).Google Scholar
Kuhn, J. & Drechsel, O. (1928). Der Einfluß der Kalkstickstoffs auf das Bakterienleben im Boden. Zietschrift für Pflansenernähr Düngung und Bodenkde 7, 105–118.Google Scholar
Lahlali, R. & Peng, G. (2014). Suppression of clubroot by Clondrostachys rosea via antibiosis and induced host resistance. Plant Pathology 63, 447–455.Google Scholar
Lahlali, R. L., McGregor, L., Song, T., Gossen, B. D., 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, e94144. doi: 10.1371/journal.pone.0094144 Google Scholar
Lehmann, J. & Kleber, M. (2015). The contentious nature of soil organic matter. Nature 528, 60–68.Google Scholar
Lehtovirta-Morley, L. E., Stoecker, K., Vilcinskas, A., Prosser, J. I. & Nicol, G. W. (2011). Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proceedings of the National Academy of Science USA 108, 15892–15897.Google Scholar
Leigh, G. J. (2004). The triumph of industrial chemistry. In The World's Greatest Fix – a History of Nitrogen and Agriculture (Ed. Leigh, G. J.), pp. 121–163. Oxford, UK: Oxford University Press.Google Scholar
Liesack, W., Janssen, P. H., Rainey, F. A., Ward-Rainey, N. L. & Stackebrandt, E. (1997). Microbial diversity in soil: the need for a combined approach using molecular and cultivation techniques. In Modern Soil Microbiology (Eds van Elsas, J. D., Trevors, J. T. & Wellington, E. M. H.), pp. 375–439. New York, USA: Marcel Dekker.Google Scholar
Linde, C. P. (1916). Aus meinem Leben und von meiner Arbeit. Munich, Germany: R. Oldenbourg.Google Scholar
Ma, J., Sun, W., Hu, Q., Yu, Q., Wang, Q. & Fu, J. (2013). Effects of cyanamide fertiliser on microbial community structure of continuous cropping soil. Journal of Zhejiang University (Agriculture & Life Sciences) 39, 281–290.Google Scholar
Macfarlane, I. (1958). A solution-culture technique for obtaining root-hair or primary, infection by Plasmodiophora brassicae . Journal of General Microbiology 18, 720–732.Google Scholar
Maier-Greiner, U. H., Obermaier-Skrobranek, M. M., Estermaier, L. M., Kammerloher, W., Freund, C., Wülfing, C., Burkert, U. I., Matern, D. H., Breuer, M. & Eulitz, M. (1991). Isolation and properties of a nitrile hydratase from the soil fungus Myrothecium verrucaria that is highly specific for the fertilizer cyanamide and cloning of its gene. Proceedings of the National Academy of Sciences USA 88, 4260–4264.Google Scholar
Marschner, H., Römheld, V., Horst, W. J. & Martin, P. (1986). Root-induced changes in the rhizosphere: importance for mineral nutrition of plants. Zeitschrift für Pflanzenernährung und Bodenkunde (Journal of Plant Nutrition and Soil Science) 149, 441–456.Google Scholar
Martin, W. H. (1933). Plant Pathology. Report of New Jersey Agricultural Experiment Station for the 2-year period ending June 30 1933, 57–66. New Brunswick, NJ, USA: New Jersey Agricultural Experiment Station.Google Scholar
Mattey, M. & Dixon, G. R. (2015). Premature germination of resting spores as a means of protecting brassica crops from Plasmodiophora brassicae Wor., (Clubroot). Crop Protection 77, 27–30.Google Scholar
Mazzola, M. (2004). Assessment and management of soil microbial community structure for disease suppression. Annual Review of Phytopathology 42, 35–59.CrossRefGoogle ScholarPubMed
McDonald, M. R. (2002). Improved Management of Clubroot in Crucifer Crops – Report 2002. King, Ontario, Canada: University of Guelph, Muck Crops Research Station.Google Scholar
McDonald, M. R., Kornatowska, B. & McKeown, A. W. (2004). Management of clubroot of Asian Brassica crops grown on organic soils. Acta Horticulturae 635, 25–30.Google Scholar
Mellor, J. W. (1925). A Comprehensive Treatise on Inorganic and Theoretical Chemistry, Vol. 5. London, UK: Longmans.Google Scholar
Müller, H. (1955). Untersuchungen über die Wirkung des Cyanamids im Kalkstickstoff auf pathogene und nichtpathogene Mikroorganismen im Boden. Archiv für Mikrobiologie 22, 285–306.Google Scholar
Mukerji, B. K. (1932). Studies on calcium cyanamide. II. Microbiological aspects of nitrification in soils under varied environmental conditions. Journal of Agricultural Science, Cambridge 22, 335–347.Google Scholar
Murakami, H., Tsushima, S., Kuroyanagi, Y. & Shishido, Y. (2002). Reduction of resting spore density of Plasmodiophora brassicae and clubroot disease severity by liming. Soil Science and Plant Nutrition 48, 685–691.Google Scholar
Myers, D. C. & Campbell, R. N. (1985). Lime and the control of clubroot of crucifers: effects of pH, calcium, magnesium, and their interactions. Phytopathology 75, 670–673.Google Scholar
Naiki, T. & Dixon, G. R. (1987). The effects of chemicals on developmental stages of Plasmodiophora brassicae (clubroot). Plant Pathology 36, 316–327.Google Scholar
Naiki, T., Kageyama, K. & Ikegami, H. (1978). The relation of spore density of Plasmodiophora brassicae Wor. to the root hair infection and club formation in Chinese cabbage (Studies on the clubroot of cruciferous plant II). Annals of the Phytopathology Society of Japan 44, 432–439.Google Scholar
Neuhauser, S., Kirchmair, M. & Gleason, F. H. (2011). The ecological potentials of Phytomyxea (“plasmodiophorids”) in aquatic food webs. Hydrobiologia 659, 23–35.Google Scholar
Newton, A. C., Fitt, B. D. L., Atkins, S. D., Walters, D. R. & Daniell, T. J. (2010). Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends in Microbiology 18, 365–373.Google Scholar
Niwa, R., Kumei, T., Nomura, Y., Yoshida, S., Osaki, M. & Ezawa, T. (2007). Increase in soil pH due to Ca-rich organic matter application causes suppression of the clubroot disease of crucifers. Soil Biology & Biochemistry 39, 778–785.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 Pathology 57, 443–452.Google Scholar
Nõmmik, H. (1958). On decomposition of calcium cyanamide and dicyanamide in the soil. Acta Agriculturae Scandinavica 8, 404–440.Google Scholar
Page, L. V. (2001). Studies of components for a potential integrated control system for Plasmodiophora brassicae. Ph. D, thesis, University of Strathclyde, Glasgow, UK.Google Scholar
Pankhurst, C. E., Doube, B. M. & Gupta, V. V. S. R. (1997). Biological indicators of soil health: synthesis. In Biological Indicators of Soil Health (Eds Pankhurst, C., Doube, B. M. & Gupta, V. V. S. R.), pp. 419–435. Oxford, UK: CAB International.Google Scholar
Paustian, K., Lehmann, J., Ogle, S., Reay, D., Robertson, G. P. & Smith, P. (2016). Climate-smart soils. Nature 532, 49–57.Google Scholar
Pimpini, F., Venter, F. & Wünsch, A. (1970). The influence of different nitrogen forms and increasing nitrogen doses on the content of total nitrogen and of nitrate in cauliflower plants. Landwirtschaftliche Forschung 23, 363–370.Google Scholar
Pleysier, J. L., Arora, Y. & Juo, A. S. R. (1987). Nitrogen leaching and uptake from calcium cyanamide in comparison to urea and calcium ammonium nitrate in an ultisol from the humid tropics. Nutrient Cycling in Agroecosystems 12, 193–199.Google Scholar
Raaijmakers, J. M. & Mazzola, M. (2016). Soil immune responses. Science 352, 1392–1393.Google Scholar
Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C. & Moëmme-Loccoz, Y. (2009). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. In Rhizosphere: Achievements and Challenges (Eds Dessaux, Y., Hinsinger, P. & Lemanceau, P.), pp. 341–361. Developments in Plant and Soil Sciences no. 104. Dordrecht, the Netherlands: Springer.Google Scholar
Rathsack, K. (1978). Die nitrificide Wirkung des Dicyanamides. Landwirtschaftliche Forschung 31, 347–358.Google Scholar
Rieder, G. (1981). Calcium cyanamide–fertiliser or pesticide? World Crops 33, 17–20.Google Scholar
Rosenzweig, C., Elliott, J., Deryng, D., Ruane, A. C., Müller, C., Arneth, A., Boote, K. J., Folberth, C., Glotter, M., Khabarov, N., Neumann, K., Piontek, F., Pugh, T. A. M., Schmid, E., Stehfest, E., Yang, H. & Jones, J. W. (2014). Assessing agricultural risks of climate change in the 21st century in a global gridded crop model intercomparison. Proceedings of the National Academy of Sciences USA 111, 3268–3273.Google Scholar
Rouxel, F., Briard, M. & Lejeune, B. (1988). Studies of soil receptiveness to clubroot caused by Plasmodiophora brassicae: experiments on responses of a series of vegetable soils in Brittany. In Progress on Pest Management of Field Vegetables. Proceedings of the CEC/IOBC Experts’ Group, Rennes, France 20–22 November 1985 (Eds Cavalloro, R. & Pelerents, C. J.), pp. 145–152. Rotterdam, The Netherlands: A A Balkema.Google Scholar
Roy, A. H. (2015). Global Fertiliser Industry: Transitioning from Volume to Value. Proceedings of the International Fertiliser Society no 769. Colchester, UK: International Fertiliser Society.Google Scholar
Schutter, M., Sandeno, J. & Dick, R. (2001). Seasonal, soil type, and alternative management influences on microbial communities of vegetable cropping systems. Biology and Fertility of Soils 34, 397–410.Google Scholar
Schwelm, A., Fogelqvist, J., Knaust, A., Jülke, S., Lilja, T., Bonilla-Rosso, G., Karlsson, M., Shevchenko, A., Dhandapani, V., Choi, S. R., Kim, H. G., Park, J. Y., Lim, Y. P., Ludwig-Müller, J. & Dixelius, C. (2015). The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Nature Scientific Reports 5, 11153. doi: 10.1038/srep11153.Google Scholar
Shi, K., Wang, L., Zhou, Y-H., Yu, Y-L. & Yu, J-Q. (2009). Effects of calcium cyanamide on soil microbial communities and Fusarium oxysporum f. sp. cucumberinum . Chemosphere 75, 872–877.Google Scholar
Sieling, K. & Kage, H. (2010). Efficient N management using winter oilseed rape: a review. Agronomy for Sustainable Development 30, 271–279.Google Scholar
Smith, A. M. (1961). Calcium cyanamide. In Manures and Fertilisers (Ed. Smith, A. M.), pp. 115–117. London: Thomas Nelson & Sons Ltd.Google Scholar
Smil, V. (2004). Enriching the Earth: Fritz Harber, Carl Bosch, and the Transformation of World Food Production. Cambridge, Massachusetts, USA: Massachusetts Institute of Technology (MIT) Press.Google Scholar
Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Avery, T. K., Tignor, M. M. B. & Miller, H. L. Jr (2007). Climate Change 2007: The Physical Science Basis. Contributions of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press.Google Scholar
Stewart, K. L. (2008). Conventional and novel treatments for control of clubroot disease of brassicas. PhD Thesis, University of Edinburgh, UK.Google Scholar
Stransky, H. & Amberger, A. (1973). Isolation and properties of a cyanamide hydratase (EC 4·2·1) from Myrothecium verrucaria . Zeitschrift fur Pflanzenphysiologie 70, 174–187.Google Scholar
Strelkov, S. E. & Dixon, G. R. (2014). Clubroot (Plasmodiophora brassicae) on canola and other brassica species – disease development, epidemiology and management. Canadian Journal of Plant Pathology 36, (Suppl. 1), 1–4.Google Scholar
Sturkie, D. G. (1937). Control of weeds in lawns with calcium cyanamide. Journal of the American Society of Agronomy 29, 803–808.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 . Journal of Phytopathology 150, 529–535.Google Scholar
Takahashi, H., Ishikawa, T., Kaido, M., Takita, K., Hayakawa, T., Okazaki, K., Itoh, K., Mitsui, T. & Hori, H. (2006). Plasmodiophora brassicae-induced cell death and medium alkalization in clubroot-resistant cultured roots of Brassica rapa . Journal of Phytopathology 154, 156–162.Google Scholar
Tewari, K., Suganuma, T., Fuijikake, H., Ohtake, N., Sueyoshi, K., Takahashi, Y. & Ohyama, T. (2004). Effect of deep placement of N fertilizers and different inoculation methods of bradyrhizobia on growth, N2-fixation activity and N absorption rate of field-grown soybean plants. Journal of Agronomy and Crop Science 190, 46–58.Google Scholar
Thorman, R. E., Williams, J. R., Musselbrook, T. H., Rollett, A. J., Bowden, A., Shrosbree, A. & Chambers, B. J. (2014). Nitrification inhibitor and nitrogen fertiliser application timing strategies to reduce nitrous oxide emissions from winter wheat land. In The Nitrogen Challenge: Building a Blueprint for Nitrogen Use Efficiency and Food Security. Proceedings of the 18th Nitrogen Workshop, Lisbon, Portugal 30th June to 3rd July 2014 (Ed. Cordovil, C. M. d. S.), pp. 521–523. Lisbon, Portugal: ISA Press.Google Scholar
Tian, Y., Zhang, X., Liu, J., Chen, Q. & Gao, L. (2009). Microbial properties of rhizosphere soils as affected by rotation, grafting and soil sterilisation in intensive vegetable production. Scientia Horticulturae 123, 139–147.Google Scholar
Tollefson, J. (2010). Intensive farming may ease climate change. Nature 465, 853.Google Scholar
Torsvik, V. & Ovreas, I. (2002). Microbial diversity and function in soil: from genes to ecosystems. Current Opinion in Microbiology 5, 240–245.Google Scholar
Torsvik, V., Goksoyr, J. & Daae, F. D. (1990). High diversity in DNA of soil bacteria. Applied & Environmental Microbiology 56, 782–787.Google Scholar
Tourna, M., Steiglmeier, M., Spang, A., Könneke, M., Schintlmeister, A., Urich, T., Engel, M., Schloter, M., Wagner, M., Richter, A. & Schleper, C. (2011). Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences USA 108, 8420–8425.Google Scholar
Tremblay, N., Belec, C., Coulombe, J. & Godin, C. (2005). Evaluation of calcium cyanamide and liming for control of clubroot disease in cauliflower. Crop Protection 24, 798–803.Google Scholar
van Bruggen, A. H. C., Semenov, A. M., van Diepeningen, A. D., de Vos, O. J. & Blok, W. J. (2006). Relation between soil health, wave-like fluctuations in microbial populations and soil-borne plant disease management. European Journal of Plant Pathology 115, 105–122.Google Scholar
Verona, O. (1970). The effect of calcium cyanamide on some groups of lower fungi [Der Einfluß des Kalkstickstoffs auf einige Gruppen von niederen Pilzen]. Landwirtschaftliche Forschung 23, 36–50.Google Scholar
Vilsmeier, K. & Amberger, A. (1978). Model experiments concerning the breakdown of powdered and granulated calcium cyanamide fertilisers. Journal of Agronomy and Crop Science 147, 68–77.Google Scholar
von Braun, J. (2010). Strategic body needed to beat food crisis. Nature 465, 548–549.Google Scholar
Walker, J. C. & Larson, R. H. (1935). Calcium cyanamide in relation to control of clubroot of cabbage. Journal of Agricultural Research 51, 183–189.Google Scholar
Wall, D. H., Nielsen, U. N. & Six, J. (2015). Soil biodiversity and human health. Nature 528, 69–76.Google Scholar
Walters, D. R., Ratsep, J. & Havis, N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. Journal of Experimental Botany 64, 1263–1280.Google Scholar
Wang, J-F. & Hsieh, W-H. (1986). Studies on the suppressive factors and characteristics of suppressive soils of clubroot in crucifers. Plant Protection Bulletin (Taiwan ROC) 28, 363–370.Google Scholar
Webster, M. A. (1986). pH and nutritional effects on infection by Plasmodiophora brassicae Wor. and clubroot symptoms. Ph. D. thesis, University of Aberdeen, UK.Google Scholar
Webster, M. A. & Dixon, G. R. (1991 a). Calcium, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae . Mycological Research 95, 64–73.Google Scholar
Webster, M. A. & Dixon, G. R. (1991 b). Boron, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae . Mycological Research 95, 74–79.Google Scholar
Williamson, C. J. & Dyce, P. E. (1989). The effect of calcium cyanamide on the reaction of swede cultivars to populations of Plasmodiophora brassicae . Plant Pathology 38, 230–238.Google Scholar
Wissuwa, M., Mazzola, M. & Picard, C. (2009). Novel approaches in plant breeding for rhizosphere-related traits. Plant and Soil 321, 409–430.Google Scholar
Wolfe, A. & Wolfe, G. (1930). Ueber den Einfluss des Kalkstickstoffs auf die Mikroflora des Bödens. Centblatt Bakteriologie. (II). 81, 221–230.Google Scholar
Wood, M. (1998). Cah marker gene aids plant transformations. Agricultural Research 46, 12–13. Available from: http://ufdc.ufl.edu/UF00074949/00018/12j (verified 9 August 2016).Google Scholar
Woronin, M. S. (1878). Plasmodiophora brassicae – the cause of cabbage hernia. Jarbücher für Wissenschaftliche Botanik 11, 548–574 (in German).Google Scholar
Yamamoto, A., Akiyama, H., Naokawa, T. & Yagi, K. (2012). Effect of lime-nitrogen application on N2O emmission from an andosol vegetable field. Soil Science and Plant Nutrition 58, 245–254.Google Scholar
Yamamoto, A., Akiyama, H., Naokawa, T. & Yagi, K. (2013). Lime-nitrogen application reduces N2O emission from a vegetable field with imperfectly-drained sandy clay-loam soil. Soil Science and Plant Nutrition 59, 442–449.Google Scholar
Yano, S., Tanaka, S., Kameya-Iwaki, M. & Katumoto, K. (1991). Relation of Ca2+ efflux to germination of resting spores of clubroot fungus. Bulletin of the Faculty of Agriculture, Yamaguchi University 39, 105–112.Google Scholar
Yao, H., He, Z., Wilson, M. J. & Campbell, C. D. (2000). Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microbial Ecology 40, 223–237.Google Scholar
Yu, X-X., Zhao, Y. T., Cheng, J. & Wang, W. (2015). Biocontrol effect of Trichoderma harzianum T4 on brassica clubroot and analysis of rhizosphere microbial communities based on T-RFLP. Biocontrol Science and Technology 25, 1493–1505.Google Scholar
Zhu, B. L., Ma, J. W., Ye, X. Z. & Xia, Z. M. (2001). Effects of lime-nitrogen on soil amelioration and vegetable production (Chinese with English summary). Journal of Zheijang University 27, 339–342.Google Scholar