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Adverse effects of brassica green manures on encysted eggs, infective second-stage juveniles and the reproduction of Globodera rostochiensis

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Abstract

Potato cyst nematodes (PCN), Globodera spp., are major pests of potato worldwide. In this study, the toxicity of an aqueous extract (1 g/ml) of fresh leaves of brassica species (savoy cabbage, cauliflower, broccoli, red cabbage, turnip, white mustard and edible radish) was tested on G. rostochiensis encysted eggs and infective, second-stage juveniles (J2) in vitro. Soil infested with cysts (Pi 20 eggs/g soil) was either fumigated with metham sodium and/or biofumigated with 2 % green manure of brassica and wheat under glasshouse conditions. More than 99 % of the J2 were paralysed after 24 h and <1 % of J2 hatched from encysted eggs during a 6-week exposure to brassica extracts. Nematode reproduction on the susceptible potato cv. Marfona was reduced by green manure amendments, the numbers of new cysts was reduced by between 60 % in radish- and 33 % in cauliflower-treated soil. The reproduction rate of G. rostochiensis was reduced to less than 1, and final populations of eggs and J2/g soil were reduced by between 73 % (white mustard) and 92 % (edible radish). Likewise, green manure of wheat and metham sodium fumigation decreased potato cyst nematode reproduction rates to below one, new cysts by 50 and 42 %, and final eggs/g soil by 81 and 88 %, respectively. In infested soil, total fresh weight of aerial parts and roots of potato was decreased by 64 %, while total weight of plants was increased between 21 and 74 % in brassica amended soil, and 56 and 76 % in wheat and metham sodium-treated soil, respectively.

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References

  1. Aires A, Carvalho R, Barbosa M, Da C, Rosa E (2009) Suppressing potato cyst nematode, Globodera rostochiensis, with extracts of Brassicacea plants. Am J Potato Res 86:327–333

    Article  Google Scholar 

  2. Akhtar M, Malik A (2000) Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour Technol 74:35–47

    Article  CAS  Google Scholar 

  3. Bailey KL, Lazarovits G (2003) Suppressing soil-borne diseases with residue management and organic amendments. Soil Tillage Res 72:169–180

    Article  Google Scholar 

  4. Been TH, Schomaker CH (1999) Fumigation of marine clays soils infested with Globodera pallida and G. rostochiensis using 1, 3 dichloropropene and additional top soil treatments. Nematology 1:3–14

    Article  CAS  Google Scholar 

  5. Belair G, Tremblay N (1995) The influence of chitin-urea amendments applied to an organic soil on a Meloidogyne hapla population and on the growth of greenhouse tomato. Phytoprotection 76:75–80

    Article  Google Scholar 

  6. Bending GD, Lincoln SD (2000) Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products. Soil Biol Biochem 32:1261–1269

    Article  CAS  Google Scholar 

  7. Bones AM, Rossiter JT (2006) The enzymatically and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067

    Article  CAS  PubMed  Google Scholar 

  8. Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Soil Tillage Res 14:224–228

    Google Scholar 

  9. Buskov S, Serra B, Rosa E, Sorensen H, Sorensen JC (2002) Effects of intact glucosinolates and products produced from glucosinolates in myrosinase-catalyzed hydrolysis on the potato cyst nematode (Globodera rostochiensis Woll). J Agric Food Chem 50:690–695

    Article  CAS  PubMed  Google Scholar 

  10. Chitwood DJ (2002) Phytochemical based strategies for nematode control. Annu Rev Phytopathol 40:221–249

    Article  CAS  PubMed  Google Scholar 

  11. Collins H, Alva A, Boydston R, Cochran R, Hamm P, McGuire A, Riga E (2006) Soil microbial, fungal, and nematode responses to soil fumigation and cover crops under potato production. Biol Fertil Soils 42:247–257

    Article  CAS  Google Scholar 

  12. Craig SC, Saxton AM, Sams CE (2005) Relationship of climate and genotype to seasonal variation in the glucosinolate myrosinase system. 1. Glucosinolate content in ten cultivars of Brassica oleracea grown in fall and spring seasons. J Sci Food Agric 85:671–681

    Article  Google Scholar 

  13. Crow WT, Guertal EA, Rodriguez-Kabana R (1996) Responses of Meloidogyne arenaria and Meloidogyne incognita to green manures and supplemental urea in glasshouse culture. J Nematol 28:648–654

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Cunha MJM, Conceição ILPM, Abrantes IMO, Santos MSNA (2004) Characterization of potato cyst nematode populations from Portugal. Nematology 6:55–58

    Article  Google Scholar 

  15. Ebadi M, Fatemy S, Riahi H (2009) Evaluation of the efficacy of Pochonia chlamydosporia var. chlamydosporia as a biological control agent of Meloidogyne javanica on pistachio. Biocontrol Sci Tech 19(7):689–700

    Article  Google Scholar 

  16. Evans K, Brodie BB (1980) The origin and distribution of the golden nematode and its potential in the USA. Am Potato J 57:79–89

    Article  Google Scholar 

  17. Fahey JW, Zakmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Photochemistry 56:50–51

    Article  Google Scholar 

  18. Fenwick DW (1940) Methods for the recovery and counting of cysts of Heterodera schachtii from soil. J Helminthol 18:155–172

    Article  Google Scholar 

  19. Fourie H, Ahuja P, Lammers J, Daneel M (2016) Brassicacea-based management strategies as an alternative to combat nematode pests: a synopsis. Crop Prot 80:21–41. doi:10.1016/j.cropro.2015.10.026

    Article  Google Scholar 

  20. Gamliel A, Stapleton JJ (1993) Characterization of antifungal volatile compounds evolved from solarized soil amended with cabbage residues. Phytopathology 83:899–905

    Article  CAS  Google Scholar 

  21. Gardiner JB, Morra MJ, Eberlein CV, Brown PD, Borek V (1999) Allelochemicals released in soil following incorporation of rapeseed (Brassica napus) green manures. J Agric Food Chem 47:3837–3842

    Article  CAS  PubMed  Google Scholar 

  22. Ghasemi H, Fatemy S (2014) In vitro examination of mustard and tarragon extracts on the activity of Globodera rostochiensis. Asp Appl Biol 126:139–143

    Google Scholar 

  23. Gitty M, Tanha Maafi Z (2010) First report of a potato cyst nematode, Globodera rostochiensis, on potato, in Iran. Plant Pathol 59(2):412. doi:10.1111/j.1365-3059.2009.02135.x

    Article  Google Scholar 

  24. Gitti M, Tanha Maafi Z, Arjmandian A, Pishevar S (2011) Occurrence of potato golden cyst nematode in Iran and its distribution in Hamadan Province. Agric Biotechnol 2(1):53–61

    Google Scholar 

  25. Hafez SL, Sundararai P, Handoo ZA, Skarrtar AM, Carta LK, Chitwood DJ (2007) First report of the pale cyst nematode, Globodera pallida in the United States. Plant Dis 91:325

    Article  Google Scholar 

  26. Hooks CRR, Wang KH, Ploeg A, McSorley R (2010) Using marigold (Tagetes spp.) as a cover crop to protect crops from plant-parasitic nematodes. Appl Soil Ecol 46:307–320

    Article  Google Scholar 

  27. Ibekwe AM, Papiernik SK, Gan J, Yates SR, Yang CH, Crowley DE (2001) Impact of soil fumigants on soil microbial communities. Appl Environ Microbiol 67:3245–3257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Jaffee BA, Ferris H, Stapleton JJ, Norton MVK, Muldoon AE (1994) Parasitism of nematodes by the fungus Hirsutella rhossiliensis as affected by certain organic amendments. J Nematol 26:152–161

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Johnson AW, Golden AM, Auld DL, Sumner DR (1992) Effects of rapeseed and vetch as green manure crops and fallow on nematodes and soil borne pathogens. J Nematol 24:117–126

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Jones JM (1973) Trials on the chemical control of the potato cyst eelworm in the Yorks. and Lancs. Region. In: Proceedings of the 7th British Insecticide and Fungicide Conference, Brighton, UK, pp 425–429

  31. Kimpinski J, Gallant CF, Henry R, Macleod JA, Sanderson JB, Sturz AV (2003) Effect of compost and manure soil amendments on nematodes and yields of potato and barley: a 7-year study. J Nematol 35:289–293

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Kirkegaard J, Matthiessen J (2004) Developing and refining the biofumigation concept. Agroindustria 3:233–239

    Google Scholar 

  33. 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) 9th Australian research assembly on Brassicas. British Society for Plant Pathology, Agricultural Research Institute, Wagga Wagga, pp 77–82

    Google Scholar 

  34. Kokalis-Burelle N, Rodriguez-Kabana R, Weaver CF, King PS (1994) Evaluation of powdered pine bark for control of Meloidogyne arenaria and Heterodera glycines on soybean. Plant Soil 162:163–168

    Article  Google Scholar 

  35. Kruger DHM, Fourie JC, Malan AP (2013) Cover crops with biofumigation properties for the suppression of plant-parasitic nematodes: a review. S Afr J Enol Vitic 34(2):287–295

    Google Scholar 

  36. Kwerepe BC, Labuschagne N (2003) Biofumigation and soil solarization as integrated pest management (IPM) components for the control of root-knot nematode, Meloidogyne incognita (Kofoid and White Chitwood) on Bambara groundnut (Vigna subterranean (L.) Verdc.). UNISWA J Agric 11:56–63

    Google Scholar 

  37. Lazzeri L, Tacconi R, Palmieri S (1993) In vitro activity of some glucosinolates and their reaction products towards a population of the nematode Heterodera schachtii. J Agric Food Chem 41:825–829

    Article  CAS  Google Scholar 

  38. Lewis JA, Papavizas GC (1970) Evolution of volatile sulfur containing compounds from decomposition of crucifers in soil. Soil Biol Biochem 2:239–246

    Article  CAS  Google Scholar 

  39. Lopez-Perez JA, Roubtsova T, Ploeg A (2005) Effect of three plant residues and poultry litter used as biofumigants at three temperatures on Meloidogyne incognita infestation of tomato in greenhouse experiments. J Nematol 37:489–494

    PubMed  PubMed Central  Google Scholar 

  40. Lord J, Lazzeri L, Atkinson H, Urwin P (2011) Biofumigation for control of potato cyst nematodes: activity of brassica leaf extracts and green manures on Globodera pallida in vitro and in soil. J Agric Food Chem 59:7882–7890

    Article  CAS  PubMed  Google Scholar 

  41. Mai WF (1977) Worldwide distribution of potato cyst nematodes and their importance in crop production. J Nematol 9:30–34

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Malik MS, Riley MB, Norsworthy JK, Bridges W Jr (2010) Glucosinolate profile variation of growth stages of wild radish, (Raphanus raphanistrum). J Agric Food Chem 58:3309–3315

    Article  CAS  PubMed  Google Scholar 

  43. Marks RJ, Brodie BB (1998) Potato cyst nematodes biology, distribution and control. CAB International, Wallingford, p 424

    Google Scholar 

  44. Matthiessen JN, Kirkegaard JA (2006) Biofumigation and enhanced biodegradation: opportunity and challenge in soil-borne pest and disease management. Crit Rev Plant Sci 2:235–265

    Article  Google Scholar 

  45. Matthiessen JN, Warton B, Shackleton MA (2004) The importance of plant maceration and water addition in achieving high Brassica-derived isothiocyanate levels in soil. Agroindustria 3:277–280

    Google Scholar 

  46. McCulley EM, Miller C, Sprague JS, Huang XC, Kirkegaard AJ (2008) Distribution of glucosinolates and sulphur-rich cells in roots of field-grown canola (Brassica napus). New Phytol 180:193–205

    Article  Google Scholar 

  47. Mcleod R, Da Silva E (1994) Cover crops and inter row nematode infestation in vineyards. 2. Effects of green material and of roots of cereals, legume and crucifer crops on root knot (Meloidogyne incognita and Meloidogyne javanica) and citrus (Tylenchulus semipenetrans) nematodes. Aust Grape Grow Winemak 366:119–124

    Google Scholar 

  48. Mcleod RW, Steel CC (1999) Effects of brassica-leaf green manures and crops on activity and reproduction of Meloidogyne javanica. Nematology 1(6):613–624

    Article  Google Scholar 

  49. McSorley R (2011) Overview of organic amendments for management of plant-parasitic nematodes, with case studies from Florida. J Nematol 43(2):69–81

    PubMed  PubMed Central  Google Scholar 

  50. McSorley R, Gallaher RN (1995) Cultural practices improve crop tolerance to nematodes. Nematropica 25:53–60

    Google Scholar 

  51. Mian IH, Rodriguez-Kabana R (1982) Soil amendments with oil cakes and chicken litter for control of Meloidogyne arenaria. Nematropica 12:205–220

    Google Scholar 

  52. Mojtahedi H, Santo GS, Hang AN, Wilson JH (1991) Suppression of root-knot nematode populations with selected rapeseed cultivars as green manure. J Nematol 23:170–174

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Mojtahedi H, Santo GS, Wilson JH, Hang AN (1993) Managing Meloidogyne chitwoodi on potato with rapeseed as green manure. Plant Dis 77:42–46

    Article  Google Scholar 

  54. Morra MJ, Kirkegaard JA (2002) Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biol Biochem 34:1683–1690

    Article  CAS  Google Scholar 

  55. Neves WS, Freitas LG, Coutinho MM, Parreira DF, Ferraz S, Costa MD (2007) Biofiumigation of soil with species of Brassicaceae for the control of Meloidogyne javanica. J Nematol 31:195–201

    Google Scholar 

  56. Ngala BM, Haydock PPJ, Woods S, Back MA (2015) Biofumigation with Brassica juncea, Raphanus sativus and Eruca sativa for the management of field populations of the potato cyst nematode Globodera pallida. Pest Manag Sci 71:759–769

    Article  CAS  PubMed  Google Scholar 

  57. Oka Y (2010) Mechanisms of nematode suppression by organic soil amendments: a review. Appl Soil Ecol 44:101–115

    Article  Google Scholar 

  58. Pinto S, Rosa E, Santos S (1998) Effect of 2-propenyl glucosinolate and derived isothiocyanate on the activity of the nematodes Globodera rostochiensis (Woll.). Acta Hortic 459:323–327

    Article  CAS  Google Scholar 

  59. Ploeg AT (2000) Effects of amending soil with Tagetes patula cv. Single Gold on Meloidogyne incognita infestation of tomato. Nematology 2:489–493

    Article  Google Scholar 

  60. Ploeg AT (2008) Biofumigation to manage plant-parasitic nematodes. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, The Netherlands, pp 239–248

    Google Scholar 

  61. Potter MJ, Davies K, Rathjen AJ (1998) Suppressive impact of glucosinolates in Brassica vegetative tissues on root lesion nematode Pratylenchus neglectus. J Chem Ecol 24:67–80

    Article  CAS  Google Scholar 

  62. Pourmehdi Zanbouri B, Fatemy S (2014) Two methods of evaluating bionematicide effects of Mentha pulegium and Lepidium sativum on hatching of Globodera rostochiensis. Asp Appl Biol 126:133–137

    Google Scholar 

  63. Ritzinger CHSP, McSorley R (1998) Effect of castor and velvet bean organic amendments on Meloidogyne arenaria in greenhouse experiments. J Nematol 30:624–631

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Roubtsova T, Lopez-Perez JA, Edwards S, Ploeg A (2007) Effect of Broccoli (Brassica oleraceae) tissue, incorporated at different depths in a soil column, on Meloidogyne incognita. J Nematol 39(2):111–117

    PubMed  PubMed Central  Google Scholar 

  65. Sahasrabudhe MR (1977) Crismer values and erucic acid contents of rapeseed oils. J Am Oil Chem Soc 54(8):323. doi:10.1007/BF02672436

    Article  CAS  Google Scholar 

  66. Serra B, Rosa E, Iori R, Barillari J, Cardoso A, Abreu C et al (2002) In vitro activity of 2-phenyl ethyl glucosinolate and its hydrolysis derivatives on the root-knot nematode Globodera rostochiensis (Woll.). Sci Hortic 92:75–81

    Article  CAS  Google Scholar 

  67. Southey JF (1986) Laboratory methods for work with plant and soil nematodes, 6th edn. Ministry of Agriculture, Fisheries and Food Reference Book, vol 402. Her Majesty’s Stationary Office, London

    Google Scholar 

  68. Stirling GR (1991) Biological control of plant parasitic nematodes. CAB International, Wallingford, p 281

    Google Scholar 

  69. Storey RMJ (1982) The ATP method for rapid assessment of the efficacy of a single application of a fumigant against Globodera spp. in field soils. Ann Appl Biol 101:93–98

    Article  CAS  Google Scholar 

  70. Thoden TC, Korthals GW, Termorshuizen AJ (2011) Organic amendments and their influences on plant-parasitic and free-living nematodes: A promising method for nematode management. Nematology 13:133–153

    Article  Google Scholar 

  71. Toyota K, Ritz K, Kuninaga S, Kimura M (1999) Impact of fumigation with metham sodium upon soil microbial community structure in two Japanese soils. Soil Sci Plant Nutr 45:203–207

    Article  Google Scholar 

  72. Turner SJ, Evans K (1998) The origins, global distribution and biology of potato cyst nematodes Globodera rostochiensis (Woll.) and Globodera pallida (Stone.). In: Marks RJ, Brodie BB (eds) Potato cyst nematodes. Biology, distribution and control. CAB International, Wallingford, Oxon, pp 7–26

    Google Scholar 

  73. Turner SJ, Fleming CC, Moreland BP, Martin TJG (2009) Variation in hatch among pathotypes of the potato cyst nematodes, Globodera rostochiensis and G. pallida, in response to potato root diffusate from Solanum spp. I. Preliminary assessments to establish optimal testing conditions. Nematology 11:749–756

    Article  Google Scholar 

  74. Wang KH, Sipes BS, Schmitt DP (2001) Suppression of Rotylenchulus reniformis by Crotalaria juncea, Brassica napus, and Tagetes erecta. Nematropica 31:237–251

    Google Scholar 

  75. Wang KH, Sipes BS, Schmitt DP (2002) Crotalaria as a cover crop for nematode management: a review. Nematropica 32:35–57

    CAS  Google Scholar 

  76. Wang D, Rosen C, Kinke IL, Cao A, Tharayil N, Gerik J (2009) Production of methyl sulfide and dimethyl disulfide from soil-incorporated plant materials and implications for controlling soil borne pathogens. Plant Soil 324:185–197

    Article  CAS  Google Scholar 

  77. Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55:25–38

    Article  Google Scholar 

  78. Youssef MMA, Lashein AMS (2013) Effect of cabbage (Brassica oleracea) leaf residue as a biofumigant, on root-knot nematode, Meloidogyne incognita infecting tomato. J. Plant Prot Res 53:3. doi:10.2478/jprr-2013-0040

    Article  Google Scholar 

  79. Zasada IA, Ferris H (2004) Nematode suppression with brassicaceous amendments: application based upon glucosinolate profiles. Soil Biol Biochem 36:1017–1024

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by Iranian Research Institute of Plant Protection, Agricultural Research Education and Extension Organization, AREO, Tehran, Iran.

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Fatemy, S., Sepideh, A. Adverse effects of brassica green manures on encysted eggs, infective second-stage juveniles and the reproduction of Globodera rostochiensis . J Plant Dis Prot 123, 225–233 (2016). https://doi.org/10.1007/s41348-016-0031-2

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