Allyl isothiocyanate shows promise as a naturally produced suppressant of the potato cyst nematode, Globodera pallida, in biofumigation systems

in Nematology
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The ability of isothiocyanates to suppress Globodera pallida was evaluated through in vitro assays. Several isothiocyanates increased juvenile mortality, the most effective being allyl isothiocyanate, which caused 100% mortality at both 25 and 50 ppm after 72 and 24 h exposure, respectively. In a hatching assay, allyl isothiocyanate was able to suppress hatch; in addition, replenishing allyl isothiocyanate every 3 days increased hatch suppression, and viability staining indicated that egg mortality was increased. Allyl isothiocyanate above concentrations of 50 ppm significantly affected both hatch suppression and mortality. Differing effects of isothiocyanates on G. pallida suggest that their toxicity depends on the pest of interest and this study shows that allyl isothiocyanate is a good candidate for the control of potato cyst nematodes using biofumigation.

Allyl isothiocyanate shows promise as a naturally produced suppressant of the potato cyst nematode, Globodera pallida, in biofumigation systems

in Nematology

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References

AngusJ.F.GardnerP.A.KirkegaardJ.A.DesmarchelierJ.M. (1994). Biofumigation: isothiocyanates released from Brassica roots inhibit growth of the take-all fungus. Plant and Soil 162107-112. DOI: 10.1007/BF01416095

AntoniousG.F.BomfordM.VincelliP. (2009). Screening Brassica species for glucosinolate content. Journal of Environmental Science and Health Part B: Pesticides Food Contaminants and Agricultural Wastes 44311-316. DOI: 10.1080/03601230902728476

BellL.Oruna-ConchaM.J.WagstaffC. (2015). Identification and quantification of glucosinolate and flavonol compounds in rocket salad (Eruca sativa, Eruca vesicaria and Diplotaxis tenuifolia) by LC-MS: highlighting the potential for improving nutritional value of rocket crops. Food Chemistry 172852-861. DOI: 10.1016/j.foodchem.2014.09.116

BellostasN.SorensenJ.C.SorensenH. (2007). Profiling glucosinolates in vegetative and reproductive tissues of four Brassica species of the U-triangle for their biofumigation potential. Journal of the Science of Food and Agriculture 871586-1594. DOI: 10.1002/jsfa.2896

BendingG.LincolnS.D. (1999). Characterisation of volatile sulphur containing compounds produced during decomposition of Brassica juncea tissues in soil. Soil Biology and Biochemistry 31695-703. DOI: 10.1016/S0038-0717(98)00163-1

BorekV.MorraM.J.BrownP.D.McCaffreyJ.P. (1994). Allelochemicals produced during sinigrin decomposition in soil. Journal of Agricultural and Food Chemistry 421030-1034. DOI: 10.1021/jf00040a037

BorekV.MorraM.J.BrownP.D.McCaffreyJ.P. (1995). Transformation of the glucosinolate-derived allelochemicals allyl isothiocyanate and allylnitrile in soil. Journal of Agricultural and Food Chemistry 431935-1940. DOI: 10.1021/jf00055a033

BrolsmaK.M.SalmJ.N.HofflandE.de GoedeR.G.M. (2014). Hatching of Globodera pallida is inhibited by 2-propenyl isothiocyanate in vitro but not by incorporation of Brassica juncea tissue in soil. Applied Soil Ecology 846-11. DOI: 10.1016/j.apsoil.2014.05.011

BrownK.K.HamptonM.B. (2011). Biological targets of isothiocyanates. Biochimica et Biophysica Acta 1810888-894. DOI: 10.1016/j.bbagen.2011.06.004

BrownP.D.MorraM.J. (1995). Glucosinolate-containing plant tissues as bioherbicides. Journal of Agricultural and Food Chemistry 433070-3074. DOI: 10.1021/jf00060a015

BrownP.D.MorraM.J. (1996). Hydrolysis products of glucosinolates in Brassica napus tissues as inhibitors of seed germination. Plant and Soil 181307-316. DOI: 10.1007/BF00012065

BrownP.D.MorraM.J.McCaffreyJ.P.AuldD.L.WilliamsL. (1991). Allelochemicals produced during glucosinolate degradation in soil. Journal of Chemical Ecology 172021-2034. DOI: 10.1007/BF00992585

BuskovS.SerraB.RosaE.SorensenH.SorensenJ.C. (2002). Effects of intact glucosinolates and products produced from glucosinolates in myrosinase-catalyzed hydrolysis on the potato cyst nematode (Globodera rostochiensis cv. Woll). Journal of Agricultural and Food Chemistry 50690-695. DOI: 10.1021/jf010470s

CharronC.S.SaxtonA.M.SamsC.E. (2005). Relationship of climate and genotype to seasonal variation in the glucosinolate-myrosinase system. I. Glucosinolate content in ten cultivars of Brassica oleracea grown in fall and spring seasons. Journal of the Science of Food and Agriculture 85671-681. DOI: 10.1002/jsfa.1880

ColeR.A. (1976). Isothiocyanates, nitriles and thiocyanates as products of autolysis of glucosinolates in Cruciferae. Phytochemistry 15759-762. DOI: 10.1016/S0031-9422(00)94437-6

D’AntuonoL.F.ElementiS.NeriR. (2008). Glucosinolates in Diplotaxis and Eruca leaves: diversity, taxonomic relations and applied aspects. Phytochemistry 69187-199. DOI: 10.1016/j.phytochem.2007.06.019

DaxenbichlerM.E.SpencerG.F.CarlsonD.G.RoseG.B.BrinkerA.M.PowellR.G. (1991). Glucosinolate composition of seeds from 297 species of wild plants. Phytochemistry 302623-2638. DOI: 10.1016/0031-9422(91)85112-D

DonkinS.G.EitemanM.A.WilliamsP.L. (1995). Toxicity of glucosinolates and their enzymatic decomposition products to Caenorhabditis elegans. Journal of Nematology 27258-262.

EllenbyC. (1946). Nature of the cyst wall of the potato-root eelworm Heterodera rostochiensis Wollenweber, and its permeability to water. Nature 157302.

FaheyJ.W.ZalcmaanA.T.TalalayP. (2001). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 565-51. DOI: 10.1016/S0031-9422(00)00316-2

FenwickG.R.HeaneyR.K. (1983). Glucosinolates and their breakdown products in cruciferous crops, foods and feedingstuffs. Food Chemistry 11249-271. DOI: 10.1016/0308-8146(83)90074-2

GardinerJ.B.MorraM.J.EberleinC.V.BrownP.D.BorekV. (1999). Allelochemicals released in soil following incorporation of rapeseed (Brassica napus) green manures. Journal of Agricultural and Food Chemistry 473837-3842. DOI: 10.1021/jf9812679

GimsingA.L.KirkegaardJ.A. (2006). Glucosinolate and isothiocyanate concentration in soil following incorporation of Brassica biofumigants. Soil Biology and Biochemistry 382255-2264. DOI: 10.1016/j.soilbio.2006.01.024

KirkegaardJ.A.SarwarM. (1998). Biofumigation potential of brassicas. Plant and Soil 20171-89. DOI: 10.1023/A:1004364713152

LazzeriL.TacconiR.PalmieriS. (1993). In vitro activity of some glucosinolates and their reaction products toward a population of the nematode Heterodera schachtii. Journal of Agricultural and Food Chemistry 41825-829. DOI: 10.1021/jf00029a028

LordJ.S.LazzeriL.AtkinsonH.J.UrwinP.E. (2011). Biofumigation for control of pale potato cyst nematodes: activity of brassica leaf extracts and green manures on Globodera pallida in vitro and in soil. Journal of Agricultural and Food Chemistry 597882-7890. DOI: 10.1021/jf200925k

MatthiessenJ.KirkegaardJ.A. (2006). Biofumigation and enhanced biodegradation: opportunity and challenge in soilborne pest and disease management. Critical Reviews in Plant Sciences 25235-265. DOI: 10.1080/07352680600611543

MatthiessenJ.N.WartonB.ShackletonM.A. (2004). The importance of plant maceration and water addition in achieving high Brassica-derived isothiocyanate levels in soil. Agroindustria 3277-280.

MinnisS.T.HaydockP.P.J.IbrahimS.K.GroveI.G.EvansK.RussellM.D. (2002). Potato cyst nematodes in England and Wales – occurrence and distribution. Annals of Applied Biology 140187-195. DOI: 10.1111/j.1744-7348.2002.tb00172.x

MorraM.J.KirkegaardJ.A. (2002). Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biology and Biochemistry 341683-1690. DOI: 10.1016/S0038-0717(02)00153-0

NeubauerC.HeitmannB.MüllerC. (2014). Biofumigation potential of Brassicaceae cultivars to Verticillium dahliae. European Journal of Plant Pathology 140341-352. DOI: 10.1007/s10658-014-0467-9

NgalaB.M.HaydockP.P.J.WoodsS.BackM.A. (2014). Biofumigation with Brassica juncea, Raphanus sativus and Eruca sativa for the management of field populations of the potato cyst nematode Globodera pallida. Pest Management Science 71759-769. DOI: 10.1002/ps.3849

NgalaB.M.WoodsS.R.BackM.A. (2015). In vitro assessment of the effects of Brassica juncea and Raphanus sativus leaf and root extracts on the viability of Globodera pallida encysted eggs. Nematology 17543-556. DOI: 10.1163/15685411-00002888

OjaghianM.R.JiangH.XieG.CuiZ.ZhangJ.LiB. (2012). In vitro biofumigation of Brassica tissues against potato stem rot caused by Sclerotinia sclerotiorum. Plant Pathology Journal 28185-190. DOI: 10.5423/PPJ.2012.28.2.185

PapadopoulosA.AldersonP. (2007). A new method for collecting isothiocyanates released from plant residues incorporated in soil. Annals of Applied Biology 15161-65. DOI: 10.1111/j.1744-7348.2007.00149.x

PasiniF.VerardoV.CaboniM.F.D’AntuonoL.F. (2012). Determination of glucosinolates and phenolic compounds in rocket salad by HPLC-DAD-MS: evaluation of Eruca sativa Mill. and Diplotaxis tenuifolia L. genetic resources. Food Chemistry 1331025-1033. DOI: 10.1016/j.foodchem.2012.01.021

PerryR.N. (1989). Dormancy and hatching of nematode eggs. Parasitology Today 5377-383. DOI: 10.1016/0169-4758(89)90299-8

PerryR.N.MoensM. (2011). Survival of parasitic nematodes outside the host. In: PerryR.N.WhartonD.A. (Eds). Molecular and physiological basis of nematode survival. Wallingford, UKCAB International pp.  1-27. DOI: 10.1079/9781845936877.0001

PetersenJ.BelzR.WalkerF.HurleK. (2001). Weed suppression by release of isothiocyanates from turnip-rape mulch. Agronomy Journal 9337-43. DOI: 10.2134/agronj2001.93137x

PriceA.J.CharronC.S.SaxtonA.M.SamsC.E. (2005). Allyl isothiocyanate and carbon dioxide produced during degradation of Brassica juncea tissue in different soil conditions. HortScience 401734-1739.

PubChem. Allyl isothiocyanate. Available online at https://pubchem.ncbi.nlm.nih.gov/compound/5971 (accessed 25 May 2016).

PubChem. Benzyl isothiocyanate. Available online at https://pubchem.ncbi.nlm.nih.gov/compound/2346 (accessed 25 May 2016).

SerraB.RosaE.IoriR.BarillariJ.CardosoA.AbreuC.RollinP. (2002). In vitro activity of 2-phenylethyl glucosinolate and its hydrolysis derivatives on the root-knot nematode Globodera rostochiensis (Woll.). Scientia Horticulturae 9275-81. DOI: 10.1016/S0304-4238(01)00277-1

ShepherdA.M. (1962). New Blue R, a stain that differentiates between living and dead nematodes. Nematologica 8201-208. DOI: 10.1163/187529262X00431

SmithB.J.KirkegaardJ.A. (2002). In vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathology 51585-593. DOI: 10.1046/j.1365-3059.2002.00744.x

SmolinskaU.MorraM.J.KnudsenG.R.JamesR.L. (2003). Isothiocyanates produced by Brassicaceae species as inhibitors of Fusarium oxysporum. Plant Disease 87407-412. DOI: 10.1094/PDIS.2003.87.4.407

TaylorF.I.KenyonD.RosserS. (2014). Isothiocyanates inhibit fungal pathogens of potato in in vitro assays. Plant and Soil 382281-289. DOI: 10.1007/s11104-014-2157-y

ValdesY.ViaeneN.PerryR.N.MoensM. (2011). Effect of the green manures Sinapis alba, Brassica napus and Raphanus sativus on hatching of Globodera rostochiensis. Nematology 13965-975. DOI: 10.1163/15685411-00002888

ValdesY.ViaeneN.BlokV.Palomares-RiusJ.E.MoensM. (2012). Changes in the pre-parasitic developmental stage of Globodera rostochiensis in response to green manures. Nematology 14925-932. DOI: 10.1163/156854112X635869

WartonB.MatthiessenJ.N.ShackletonM.A. (2001). Glucosinolate content and isothiocyanate evolution – two measures of the biofumigation potential of plants. Journal of Agricultural and Food Chemistry 495244-5250. DOI: 10.1007/s10658-014-0467-9

WiddowsonE. (1985). Potato root diffusate production. Nematologica 36-14. DOI: 10.1163/187529258X00283

Figures

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    Percentage mortality of Globodera pallida second-stage juveniles (J2) when exposed to different concentrations (12.5-50 ppm) of ten isothiocyanates (ITC) over an exposure period of 72 h. Error bars represent the SEM of four replicates for each 24 h period. Treatments labelled with ∗ indicate a significant difference in total mortality compared to the H2O control at the P<0.05 level based on Dunnett’s test following ANOVA. ITCs used were: allyl (AITC), benzyl (BITC), 2-phenylethyl (PEITC), methyl (MITC), propyl (PITC), isopropyl (IITC), ethyl (EITC), phenyl (PHITC), butyl (BUITC) isothiocyanate and sulforaphane (SUL).

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    Percentage of Globodera pallida second-stage juveniles (J2) that were dead, hatched and unhatched viable after exposure to allyl isothiocyanate (AITC) (3.125-50 ppm) refreshed every 3 days for A: 1 day’s exposure; B: 4 days exposure; and C: 7 days exposure. Error bars represent the SEM over four replicates for each category. Means labelled with ∗ are significantly different from the H2O control at the P<0.05 level based on Dunnett’s test following ANOVA. Means labelled with ∗∗ indicate significant differences in both dead and hatched J2 compared to the control.

  • View in gallery

    Percentage of Globodera pallida second-stage juveniles (J2) that were dead, hatched and unhatched viable after exposure to high concentrations (50-1500 ppm) of allyl isothiocyanate (AITC) for 1 day’s exposure followed by 4 week delay before hatch stimulation. Error bars represent the SEM over four replicates for each category. Means labelled with ∗ are significantly different from the H2O control at the P<0.05 level based on Dunnett’s test following ANOVA. Means labelled with ∗∗ indicate significant differences in both dead and hatched J2 compared to the control.

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