Abstract
The bioactive hydrolysis products of glucosinolates, particularly the isothiocyanates, can be used to control soil pests and weeds by incorporating glucosinolate-containing plant material in soil—a practice known as biofumigation. The fate of glucosinolates and their hydrolysis products in soil determines both the efficacy and environmental impact of biofumigation. Knowledge of the processes by which these compounds are sorbed, degraded or otherwise lost from the soil is fundamental to developing effective, but environmentally benign biofumigation strategies. Effective biofumigation relies on maximum hydrolysis of the glucosinolate in the plant tissue to generate high isothiocyanate concentrations in the soil after incorporation. This is favoured by maximum cell disruption, by addition of water, and a high soil temperature. Residual glucosinolates are very weakly sorbed, readily leached and are microbially degraded and mineralised in soil. In contrast, isothiocyanates are strongly sorbed by the organic matter in soil, react strongly with nucleophilic groups present in soil, and are prone to volatilization losses in addition to microbial degradation and mineralisation. These loss processes are influenced by soil type, water content and temperature. Using appropriate incorporation strategies, sufficiently high isothiocyanate concentrations (>100 nmol g−1) can be achieved in soil using biofumigation for effective suppression of susceptible pests. The relatively rapid sorption and degradation of the isothiocyanates in the period of days after incorporation minimizes the risks of persistence in the environment or leaching. Biofumigation is therefore a promising technique which can be further developed to form part of IPM (Integrated Pest Management) strategies to reduce reliance on synthetic pesticides with minimal unintended impacts on the environment.
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References
Al-Turki AI, Dick WA (2003) Myrosinase activity in soil. Soil Sci Soc Am J 67:139–145
Angus JF, Gardner PA, Kirkegaard JA, Desmarchelier JM (1994) Biofumigation—Isothiocyanates released from Brassica roots inhibit growth of the take-all fungus. Plant Soil 162:107–112. doi:10.1007/BF01416095
Bailey KL, Lazarovits G (2003) Suppressing soil-borne diseases with residue management and organic amendments. Soil Tillage Res 72:169–180. doi:10.1016/S0167-1987(03)00086-2
Bending GD, Lincoln SD (1999) Characterisation of volatile sulphur-containing compounds produced during decomposition of Brassica juncea tissues in soil. Soil Biol Biochem 31:695–703. doi:10.1016/S0038-0717(98)00163-1
Bones AM, Rossiter JT (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 97:194–208. doi:10.1111/j.1399-3054.1996.tb00497.x
Borek V, Morra MJ (2005) Ionic thiocyanate (SCN−) production from 4-hydroxybenzyl glucosinolate contained in Sinapis alba seed meal. J Agric Food Chem 53:8650–8654. doi:10.1021/jf051570r
Borek V, Morra MJ, Brown PD, McCaffrey JP (1994) Allelochemicals produced during sinigrin decomposition in soil. J Agric Food Chem 42:1030–1034. doi:10.1021/jf00040a037
Borek V, Morra MJ, Brown PD, McCaffrey JP (1995) Transformation of the glucosinolate-derived allelochemicals allyl isothiocyanate and allylnitrile in soil. J Agric Food Chem 43:1935–1940. doi:10.1021/jf00055a033
Borek V, Morra MJ, McCaffrey JP (1996) Myrosinase activity in soil extracts. Soil Sci Soc Am J 60:1792–1797
Boydston RA, Hang A (1995) Rapeseed (Brassica napus) green manure crop suppresses weeds in poatato (Solanum tuberosum). Weed Technol 9:669–675
Brinch UC, Ekelund F, Jacobsen CS (2002) Method for spiking soil samples with organic compounds. Appl Environ Microbiol 68:1808–1816. doi:10.1128/AEM.68.4.1808-1816.2002
Brown PD, Morra MJ (1993) Fate of ionic thiocyanate (Scn-) in soil. J Agric Food Chem 41:978–982. doi:10.1021/jf00030a029
Brown PD, Morra MJ (1997) Control of soil-borne plant pests using glucosinolate-containing plants. Adv Agron 61:167–231
Brown PD, Morra MJ, McCaffrey JP, Auld DL, Williams L (1991) Allelochemicals produced during glucosinolate degradation in soil. J Chem Ecol 17:2021–2034. doi:10.1007/BF00992585
Brown PD, Morra MJ, Borek V (1994) Gas chromatography of allelochemicals produced during glucosinolate degradation in soil. J Agric Food Chem 42:2029–2034. doi:10.1021/jf00045a037
Cohen MF, Mazzola M (2005) Suppression of rhizoctonia root rot by streptomyces in Brassica napus seed meal amended soil. Phytopathology 95:S20
Galletti S, Bernardi R, Leoni O, Rollin P, Palmieri S (2001) Preparation and biological activity of four epiprogoitrin myrosinase-derived products. J Agric Food Chem 49:471–476. doi:10.1021/jf000736f
Gil V, MacLeod AJ (1980) The effects of pH on glucosinolate degradation by a thioglucoside glucohydrolase preparation. Phytochemistry 19:2547–2551. doi:10.1016/S0031-9422(00)83916-3
Gimsing AL, Kirkegaard JA (2006) Glucosinolate and isothiocyanate concentration in soil following incorporation of Brassica biofumigants. Soil Biol Biochem 38:2255–2264. doi:10.1016/j.soilbio.2006.01.024
Gimsing AL, Kirkegaard JA, Hansen HCB (2005) Extraction and determination of glucosinolates from soil. J Agric Food Chem 53:9663–9667. doi:10.1021/jf051812n
Gimsing AL, Sorensen JC, Tovgaard L, Jorgensen AMF, Hansen HCB (2006) Degradation kinetics of glucosinolates in soil. Environ Toxicol Chem 25:2038–2044. doi:10.1897/05-610R.1
Gimsing AL, Poulsen JL, Pedersen HL, Hansen HCB (2007a) Formation and degradation kinetics of the biofumigant benzyl isothiocyanate in soil. Environ Sci Technol 41:4271–4276. doi:10.1021/es061987t
Gimsing AL, Sorensen JC, Strobel BW, Hansen HCB (2007b) Adsorption of glucosinolates to metal oxides, clay minerals and humic acid. Appl Clay Sci 35:212–217. doi:10.1016/j.clay.2006.08.008
Gimsing AL, Strobel BW, Hansen HCB (2008) Benzyl and 2-propenyl isothiocyanate sorption and degradation in soil. Environ Toxicol Chem (submitted)
Kirkegaard JA, Matthiessen JN (2004) Developing and refining the biofumigation concept. Agroindustria 3:233–239
Kirkegaard JA, Sarwar M (1998) Biofumigation potential of Brassicas—I. Variation in glucosinolate profiles of diverse field-grown Brassicas. Plant Soil 201:71–89. doi:10.1023/A:1004364713152
Kirkegaard JA, Gardner PA, Desmarchelier JM, Angus JF (1993) Biofumigation—using Brassica species to control pests and diseases in horticulture and agriculture. In: Wratten N, Mailer RJ (eds) Proceedings 9th Australian research assembly on Brassicas, Agricultural Research Institiute, Wagga Wagga, pp 77–82
Kirkegaard JA, Sarwar M, Wong PTW, Mead A, Howe G, Newell M (2000) Field studies on the fumigation of take all by Brassica break crops. Aust J Agric Res 51:445–456. doi:10.1071/AR99106
Larkin RP, Griffin TS (2007) Control of soilborne potato diseases using Brassica green manures. Crop Prot 26:1067–1077. doi:10.1016/j.cropro.2006.10.004
Larkin RP, Honeycut CW (2006) Effects of different 3-yr cropping systems on soil microbial communities and soilborne disease in potato. Phytopathology 96:68–79. doi:10.1094/PHYTO-96-0068
Lazzeri L, Leoni O, Manici LM (2004) Biocidal plant dried pellets for biofumigation. Ind Crops Prod 20:59–65. doi:10.1016/j.indcrop. 2003.12.018
Mari M, Iori R, Leoni O, Marchi A (1993) In vitro activity of glucosinolate-derived ITCs against postharvest fruit pathogens. Ann Appl Biol 123:155–164. doi:10.1111/j.1744-7348.1993.tb04082.x
Martin FN (2003) Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Annu Rev Phytopathol 41:325–350. doi:10.1146/annurev.phyto.41.052002.095514
Matthiessen JN, Kirkegaard JA (2006) Biofumigation and enhanced biodegradation: opportunity and challenge in soilborne pest and disease management. Crit Rev Plant Sci 25:235–265. doi:10.1080/07352680600611543
Matthiessen JN, Shackleton MA (2005) Biofumigation: environmental impacts on the biological activity of diverse pure and plant-derived isothiocyanates. Pest Manag Sci 61:1043–1051. doi:10.1002/ps.1086
Matthiessen JN, Desmarchelier JM, Vu LT, Shackleton MA (1996) Comparative efficacy of fumigants against hatchling whitefringed beetle (Coleoptera: Curculionidae) larvae and their sorption in soil. Ecotoxicology 89:1372–1378
Matthiessen JN, Warton B, Shackleton MA (2004a) Enhanced biodegradation reduces the capacity of metham sodium to control soil pests. Aust J Entomol 43:72–76. doi:10.1111/j.1440-6055.2003.00387.x
Matthiessen JN, Warton B, Shackleton MA (2004b) The importance of plant maceration and water addition in achieving high Brassica-derived isothiocyanate levels in soil. Agroindustria 3:277–280
Mithen R (2001a) Glucosinolates—biochemistry, genetics and biological activity. Plant Growth Regul 34:91–103. doi:10.1023/A:1013330819778
Mithen RF (2001b) Glucosinolates and their degradation products. Adv Bot Res 35:213–262
Mojtehedi H, Santo GS, Wilson JH, Hang AN (1993) Managing Meloidogyne chitwoodi on potato with rapeseed as green manure. Plant Dis 77:42–46
Morra MJ, Kirkegaard JA (2002) Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biol Biochem 34:1683–1690. doi:10.1016/S0038-0717(02)00153-0
Papadopoulos A, Alderson P (2007) A new method for collecting isothiocyanates released from plants residues incorporated into soil. Ann Appl Biol 151:61–65. doi:10.1111/j.1744-7348.2007.00149.x
Petersen J, Belz R, Walker F, Hurle K (2001) Weed suppression by release of isothiocyanates from turnip-rape mulch. Agron J 93:37–43
Poulsen JL, Gimsing AL, Halkier BA, Bjarnholt NB, Hansen HCB (2008) Mineralization of benzyl glucosinolate and its hydrolysis product the biofumigant benzyl isothiocyanate in soil. Soil Biol Biochem 40:135–141. doi:10.1016/j.soilbio.2007.07.015
Price AJ, Charron CS, Saxton AM, Sams CE (2005) Allyl isothiocyanate and carbon dioxide produced during degradation of Brassica juncea tissue in different soil conditions. Hortscience 40:1734–1739
Rakariyatham N, Butrindr B, Niamsup H, Shank L (2005) Screening of filamentous fungi for production of myrosinase. Braz J Microbiol 36:242–245. doi:10.1590/S1517-83822005000300007
Rice AR, Johnson-Maynard JL, Thill DC, Morra MJ (2007) Vegetable crop emergence and weed control following amendment with different Brassicaceae seed meals. Renew Agric Food Syst 22:204–212. doi:10.1017/S1742170507001743
Rumberger A, Marschner P (2003) 2-Phenylethylisothiocyanate concentration and microbial community composition in the rhizosphere of canola. Soil Biol Biochem 35:445–452. doi:10.1016/S0038-0717(02)00296-1
Sakorn P, Rakariyatham N, Niamsup H, Nongkunsarn P (2002) Rapid detection of myrosinase-producing fungi: a plate method based on opaque barium sulphate formation. World J Microbiol Biotechnol 18:73–74. doi:10.1023/A:1013914423820
Schultz TW, Comeaux JL (1996) Structure-toxicity relationships for aliphatic isothiocyanates to Tetrahymena pyriformis. Bull Environ Contam Toxicol 56:638–642. doi:10.1007/s001289900093
Schultz TW, Yarbrough JW, Woldemeskel M (2005) Toxicity to Tetrahymena and abiotic thiol reactivity of aromatic isothiocyanates. Cell Biol Toxicol 21:181–189. doi:10.1007/s10565-005-0169-3
Smith BJ, Kirkegaard JA (2002) In-vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathol 51:585–593. doi:10.1046/j.1365-3059.2002.00744.x
Vaughn SF, Isbell TA, Weisleder D, Berhow MA (2005) Biofumigant compounds released by field pennycress (Thlaspi arvense) seedmeal. J Chem Ecol 31:167–177. doi:10.1007/s10886-005-0982-4
Vaughn SF, Palmquist DE, Duval SM, Berhow MA (2006) Herbicidal activity of glucosinolate-containing seedmeals. Weed Sci 54:743–748. doi:10.1614/WS-06-007R.1
Walker JC, Morell S, Foster H (1937) Toxicity of mustard oils and related sulphur compounds to certain fungi. Am J Bot 24:536–541. doi:10.2307/2437076
Warton B, Matthiessen JN, Shackleton MA (2003) Cross-enhancement: enhanced biodegradation of isothiocyanates in soils previously treated with metham sodium. Soil Biol Biochem 35:1123–1127. doi:10.1016/S0038-0717(03)00164-0
Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270. doi:10.1016/S1360-1385(02)02273-2
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Gimsing, A.L., Kirkegaard, J.A. Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil. Phytochem Rev 8, 299–310 (2009). https://doi.org/10.1007/s11101-008-9105-5
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DOI: https://doi.org/10.1007/s11101-008-9105-5