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Effects of biofumigation using Brassica juncea and Raphanus sativus in comparison to disinfection using Basamid on apple plant growth and soil microbial communities at three field sites with replant disease

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Abstract

Aims

The effects of biofumigation with Brassica juncea ‘Terra Plus’ and Raphanus sativus ‘Defender’ in comparison to Basamid on apple plant growth and on soil microbial communities were studied at three sites affected by replant disease under field conditions.

Methods

Apple rootstocks were planted on differently treated plots to evaluate the effect of the treatments on plant growth under field and greenhouse conditions. The glucosinolates in biofumigant plant organs and their breakdown products in soils were determined. Denaturing gradient gel electrophoresis fingerprints were performed with 16S rRNA gene and ITS fragments amplified from total community DNA extracted from different soils.

Results

The highest glucosinolate concentrations were found in inflorescences of both biofumigant plant species with no differences between sites. The most abundant degradation product in soil biofumigated with B. juncea was 2-propenyl isothiocyanate, while in soil treated with R. sativus only 4-(methylthio)-3-butenyl isothiocyanate was detected. Effects of biofumigation were recorded to be stronger on fungi than on bacteria. Growth of apple rootstocks was positively affected by the treatments in a site-dependent manner.

Conclusions

The effects of biofumigation evaluated by the apple plant growth were site-dependent and might result from suppression of soil-borne pests and pathogens, changes in soil microbial community compositions, and additional nutrients from the incorporated biomass.

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References

  • Agerbirk N, Olsen CE (2012) Glucosinolate structures in evolution. Phytochemistry 77:16–45

    Article  CAS  PubMed  Google Scholar 

  • Al-Turki A, Dick WA (2003) Myrosinase activity in soil. Soil Sci Soc Am J 67:139–145

    Article  CAS  Google Scholar 

  • Antonious GF, Bomford M, Vincelli P (2009) Screening Brassica species for glucosinolate content. J Environ Sci Health Part B 44:311–316

    Article  CAS  Google Scholar 

  • Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13

    Article  CAS  Google Scholar 

  • Bangarwa SK, Norsworthy JK, Mattice JD, Gbur ED (2011) Glucosinolate and isothiocyanate production from Brassicaceae cover crops in a plasticulture production system. Weed Sci 59:247–254

    Article  CAS  Google Scholar 

  • Bellostas N, Sørensen JC, Sørensen H (2007) Profiling glucosinolates in vegetative and reproductive tissues of four Brassica species of the U-triangle for their biofumigation potential. J Sci Food Agric 87:1586–1594

    Article  CAS  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  CAS  PubMed  Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brown PD, Morra MJ (1993) Fate of ionic thiocyanate (SCN) in soil. J Agric Food Chem 41:978–982

    Article  CAS  Google Scholar 

  • Brown PD, Morra MJ, McCafferey JP, Auld DL, Williams L (1991) Allelochemicals produced during glucosinolate degradation in soil. J Chem Ecol 17:2021–2034

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Campbell BJ, Polson SW, Hanson TE, Mack MC, Schuur EAG (2010) The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ Microbiol 12:1842–1854

    Article  CAS  PubMed  Google Scholar 

  • Campbell B, Han DY, Triggs CM, Fraser AG, Ferguson LR (2012) Brassicaceae: nutrient analysis and investigation of tolerability in people with Crohn’s disease in a New Zealand study. Funct Foods Health Dis 2:460–486

    Google Scholar 

  • Carlson DG, Daxenbichler ME, VanEtten CH (1985) Glucosinolates in radish cultivars. J Am Soc Hortic Sci 110:634–638

    CAS  Google Scholar 

  • Cartea ME, Francisco M, Soengas P, Velasco P (2011) Phenolic compounds in Brassica vegetables. Molecules 16:251–280

    Article  CAS  Google Scholar 

  • Cohen M, Mazzola M (2006) Resident bacteria, nitric oxide emission and particle size modulate the effect of Brassica napus seed meal on disease incited by Rhizoctonia solani and Pythium spp. Plant Soil 286:75–86

    Article  CAS  Google Scholar 

  • Combs SM, Denning JL, Frank KD (2012) Sulfate-sulfur. In: Nathan M, Gelderman R (eds) Recommended chemical soil test procedures for the North Central Region. North Central Regional Research Publication No. 221 (revised). Missouri Agricultural Experiment Station SB 1001, Missouri, pp 35–40

    Google Scholar 

  • De Nicola GR, D’Avino L, Curto G, Malaguti UL, Cinti S, Patalano G, Lazzeri L (2013) A new biobased liquid formulation with biofumigant and fertilizing properties for drip irrigation distribution. Ind Crop Prod 42:113–118

    Article  Google Scholar 

  • Ding GC, Radl V, Schloter-Hai B, Jechalke S, Heuer H, Smalla K, Schloter M (2014) Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS ONE. doi:10.1371/journal.pone.0092958

    Google Scholar 

  • Dungan RS, Gan J, Yates S (2003) Accelerated degradation methyl isothiocyanate in soil. Water Air Soil Pollut 142:299–310

    Article  CAS  Google Scholar 

  • EC 128/2009: Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Off J Eur Union L309, http://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32009R1107&from=EN

  • Emmett B, Nelson EB, Kessler A, Bauerle TL (2014) Fine-root system development and susceptibility to pathogen colonization. Planta 239:325–340

    Article  CAS  PubMed  Google Scholar 

  • Fayzalla EA, El-Barougy E, El-Rayes MM (2009) Control of soil-borne pathogenic fungi of soybean by biofumigation with mustard seed meal. J Appl Sci 9:2272–2279

    Article  CAS  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 

  • Gimsing AL, Sørensen JC, Tovgaard L, Jørgensen AMF, Hansen HCB (2006) Degradation kinetics of glucosinolates in soil. Environ Toxicol Chem 25:2038–2044

    Article  CAS  PubMed  Google Scholar 

  • Gregory PJ (2006) Roots and the biological environments. In: Gregory PJ (ed) Plant roots: growth, activity and interaction with soils. Blackwell Publishing Ltd, UK, pp 174–215

    Chapter  Google Scholar 

  • Hanschen FS, Yim B, Winkelmann T, Smalla K, Schreiner M (2015) Degradation of biofumigant isothiocyanates and allyl glucosinolate in soil and their effects on the microbial community composition. PLoS ONE. doi:10.1371/journal.pone.0132931

    Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heuer H, Wieland G, Schönfeld J, Schönwälder A, Gomes NCM, Smalla K (2001) Bacterial community profiling using DGGE or TGGE analysis. In: Rochelle PA (ed) Environmental molecular microbiology: protocols and applications. Horizon Scientific Press, Wymondham, pp 177–190

    Google Scholar 

  • Hoestra H (1994) Ecology and pathology of replant problems. Acta Hortic 363:2–10

    Article  Google Scholar 

  • Hu P, Hollister EB, Somenahally AC, Hons FM, Gentry TJ (2015) Soil bacterial and fungal communities respond differently to various isothiocyanates added for biofumigation. Front Microbiol 5:1–9

    Article  Google Scholar 

  • Kelderer M, Manici LM, Caputo F, Thalheimer M (2012) Planting in the ‘inter-row’ to overcome replant disease in apple orchards: a study on the effectiveness of the practice based on microbial indicators. Plant Soil. doi:10.1007/s11104-012-1172-0

    Google Scholar 

  • Kirkegaard JA, Sarwar M (1998) Biofumigation potential of brassicas. Plant Soil 201:71–89

    Article  CAS  Google Scholar 

  • Klaus H (1939) Das Problem der Bodenmüdigkeit unter Berücksichtigung des Obstbaus. Landw Jahrb 89:413–459

    Google Scholar 

  • Kropf S, Heuer H, Grüning M, Smalla K (2004) Significant test for comparing complex microbial community fingerprints using pairwise similarity measures. J Microbiol Methods 57:187–195

    Article  CAS  PubMed  Google Scholar 

  • Kviklys D, Lanauskas J, Sakalauskaitė J, Kviklienė N, Uselis N (2008) Soil exhaustion and rootstock effect on the growth of apple planting material. Agron Res 6:511–516

    Google Scholar 

  • Larkin RP, Griffin TS (2007) Control of soilborne potato diseases using Brassica green manures. Crop Prot 26:1067–1077

    Article  Google Scholar 

  • Lazzeri L, Baruzzi G, Malaguti L, Antoniacci L (2003) Replacing methyl bromide in annual strawberry production with glucosinolate-containing green manure crops. Pest Manag Sci 59:983–990

    Article  CAS  PubMed  Google Scholar 

  • Lazzeri L, Leoni O, Manici LM (2004) Biocidal plant dried pellets for biofumigation. Ind Crop Prod 20:59–65

    Article  CAS  Google Scholar 

  • Lazzeri L, D’Avino L, Gies D (2010) Additional benefits of the efficacy in containing soilborne pest and pathogens with biofumigant plants and materials. Acta Hortic 888:323–329

    Article  Google Scholar 

  • Lazzeri L, Malaguti L, Cinti S, Ugolini L, De Nicola GR, Bagatta M, Casadei N, D’Avino L, Matteo R, Patalano G (2013) The Brassicaceae biofumigation system for plant cultivation and defence. An Italian twenty-year experience of study and application. Acta Hortic 1005:375–382

    Article  Google Scholar 

  • Mai WF, Merwin IA, Abawi GS (1994) Diagnosis, etiology and management of replant disorders in New York cherry and apple orchards. Acta Hortic 363:33–41

    Article  Google Scholar 

  • Matthiessen JN, Shackleton MA (2005) Biofumigation: environmental impact on the biological activity of adverse pure and plant-derived isothiocyanates. Pest Manag Sci 61:1043–1051

    Article  CAS  PubMed  Google Scholar 

  • Matthiessen JN, Warton B, Shackleton MA (2004) Enhanced biodegradation reduces the capacity of metham sodium to control soil pests. Aust J Entomol 43:72–76

    Article  Google Scholar 

  • Mattner SW, Porter IJ, Gounder RK, Shanks AL, Wren DJ, Allen D (2008) Factors that impact on the ability of biofumigants to suppress fungal pathogens and weeds of strawberry. Crop Prot 27:1165–1173

    Article  CAS  Google Scholar 

  • Mazzola M (1998) Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington. Phytopathology 88:930–938

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Granatstein DM, Elfving DC, Mullinix K (2001) Suppression of specific apple root pathogens by Brassica napus seed meal amendment regardless of glucosinolate content. Phytopathology 91:673–679

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Brown J, Izzo AD, Cohen MF (2007) Mechanism of action and efficacy of seed meal-induced pathogen suppression differ in a Brassicaceae species and time dependent manner. Phytopathology 97:454–460

    Article  PubMed  Google Scholar 

  • Mazzola M, Brown J, Zhao X, Izzo AD, Fazio G (2009) Interaction of Brassicaceous seed meal and apple rootstock on recovery of Pythium spp. and Pratylenchus penetrans from roots grown in replant soils. Plant Dis 93:51–57

    Article  Google Scholar 

  • Mazzola M, Hewavitharana SS, Strauss SL (2015) Brassica seed meal soil amendments transform the rhizosphere microbiome and improve apple production through resistance to pathogen reinfestation. Phytopathology 105:460–469

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Neumann G, Bott GS, Ohler MA, Mock HP, Lippmann R, Grosch R, Smalla K (2014) Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils. F Microbiol. doi:10.3389/fmicb.2014.00002

    Google Scholar 

  • Norsworthy JK, Malik MS, Jha P, Riley MB (2007) Suppression of Digitaria sanguinalis and Amaranthus palmeri using autumn-sown glucosinolate-producing cover crops in organically grown bell pepper. Weed Res 47:425–432

    Article  CAS  Google Scholar 

  • Olivier C, Vaughn SF, Mizubuti ESG, Loria R (1999) Variation in allyl isothiocyanate production within Brassica species and correlation with fungicidal activity. J Chem Ecol 25:2687–2701

    Article  CAS  Google Scholar 

  • Palop ML, Smiths JP, Brink BT (1995) Degradation of sinigrin by Lactobacillus agilis strain R16. Int J Food Microbiol 26:219–229

    Article  CAS  Google Scholar 

  • Peterson CJ, Tsao R, Coats JR (1998) Glucosinolate aglucones and analogues insecticidal properties and a QSAR. Pestic Sci 54:35–42

    Article  CAS  Google Scholar 

  • Porter I, Pizano M, Besri M, Mattner SW, Fraser P (2010) Progress in the global phase out of methyl bromide and the relative effectiveness of soil disinfestation strategies. Acta Hortic 883:59–66

    Article  Google Scholar 

  • Reese ET, Clapp RC, Mandels M (1958) A thioglucosidase in fungi. Arch Biochem Biophys 75:228–242

    Article  CAS  PubMed  Google Scholar 

  • Rongai D, Cerato C, Lazzeri L (2009) A natural fungicide for the control of Erysiphe betae and Erysiphe cichoracearum. Eur J Plant Pathol. doi:10.1007/s10658-009-9448-9

  • Schreiter S, Ding GC, Heuer H, Neumann G, Sandmann M, Grosch R, Kropf S, Smalla K (2014) Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol. doi:10.3389/fmicb.2014.00144

    Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spethmann W, Otto G (2003) Replant problems and soil sickness. In: Roberts AV, Debener T, Gudin S (eds) Encyclopedia of rose science. Elsevier Academic Press, Amsterdam, pp 169–180

  • St. Laurent A, Merwin IA, Fazio G, Thies JE, Brown MG (2010) Rootstock genotype succession influences apple replant disease and root-zone microbial community composition in an orchard soil. Plant Soil 337:259–272

    Article  CAS  Google Scholar 

  • Van Reeuwijk LP (2002) Procedures for soil analysis (6th edition). Technical Paper, ISRIC, Wageningen. Accessed 30 June 2015: http://www.isric.org/content/technical-papers16-1.

  • Vervoort MTW, Vonk JA, Brolsma KM, Schütze W, Quist CW, de Goede RGM, Hoffland E, Bakker J, Mulder C, Hallmann J, Helder J (2014) Release of isothiocyanates does not explain the effects of biofumigation with Indian mustard cultivars on nematode assemblages. Soil Biol Biochem 68:200–207

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NCM, Schloter M, Berg G, Smalla K (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75:3859–3865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297

    Article  CAS  PubMed  Google Scholar 

  • Yim B, Smalla K, Winkelmann T (2013) Evaluation of apple replant problems based on different soil disinfection treatments-links to soil microbial community structure? Plant Soil 366:617–631

    Article  CAS  Google Scholar 

  • Yim B, Winkelmann T, Ding G-C, Smalla K (2015) Different bacterial communities in heat and gamma irradiation treated replant disease soils revealed by 16S rRNA gene analysis—contribution to improved aboveground apple plant growth? Front Microbiol. doi:10.3389/fmicb.2015.01224

    PubMed  PubMed Central  Google Scholar 

  • Zasada IA, Masler EP, Rogers ST, Halbrendt JM (2009) Behavioural response of Meloidogyne incognita to benzyl isothiocyanate. Nematology 11:603–610

    Article  Google Scholar 

  • Zhang H, Schonhof I, Krumbein A, Gutezeit B, Li L, Stützel H, Schreiner M (2008) Water supply and growing season influence glucosinolate concentration and composition in turnip root (Brassica rapa spp. rapifera L.). J Plant Nutr Soil Sci 171:255–265

  • Zheng W, Yates SR, Papiernik SK, Nunez J (2006) Conversion of metam sodium and emission of fumigant from soil columns. Atmos Environ 40:7046–7056

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the German Federal Ministry of Food and Agriculture within the initiative “Bundesprogramm ökologischer Landbau und andere Formen nachhaltiger Landwirtschaft” (BÖLN). We thank the three nurseries K, A, and M, in Schleswig-Holstein for the project cooperation. We are also thankful to Stefan Weiß, Simon Richartz, Bärbel Ernst, Ewa Schneider, and Friederike Schröder for assistance in the biotest experiment, Andrea Jankowsky for help in GS determination, and Annett Platalla and Elke Büsch for determination of GS breakdown products. We also acknowledge Ilse-Marie Jungkurth, Philipp Braun, and Stefan Weiß for critically reading the manuscript.

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Yim, B., Hanschen, F.S., Wrede, A. et al. Effects of biofumigation using Brassica juncea and Raphanus sativus in comparison to disinfection using Basamid on apple plant growth and soil microbial communities at three field sites with replant disease. Plant Soil 406, 389–408 (2016). https://doi.org/10.1007/s11104-016-2876-3

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