Soil-borne pathogens (SBPs) significantly reduce the yield and quality of crops worldwide. In the past, their control was principally accomplished by using soil fumigants such as methyl bromide (MB). However, this fumigant which is a powerful ozone-depleting substance, has completely been phased out under the Montreal Protocol (MP). New chemicals and non-chemical alternatives to MB, including biofumigation, have been actively researched, developed, and commercially adopted worldwide. This review seeks to provide the status of biofumigation for the control of SBPs in some non-temperate climate zones referred to in this paper as Article 5 countries or developing countries according to the Montreal Protocol (MP) classification. The review will first define “the non-temperate climate zone,” list the countries belonging to this zone, focus on the role and importance of the MP in phasing-out MB, and in searching and commercially adopting alternatives including biofumigation to this fumigant. It also describes the biofumigation techniques reported and used, reports its efficacy/inefficacy to manage SBPs in some non-climate temperate countries, insists on the place it must have in an IPM program to increase its efficacy, and finally, lists the collaboration and the research needed to further develop and commercially adopt this technology in non-temperate climate countries.
Dutta TK, Khan MR, Phani V. Plant-parasitic nematode management via biofumigation using Brassica and non-Brassica plants: Current status and future prospects. Curr Plant Biol. 2019; 17: 17-32. https://doi.org/10.1016/j.cpb.2019.02.001
Porter I, Pizano M, Besri M, Mattner S, Frazer P. Progress in the global phase out of methyl bromide and the relative effectiveness of soil disinfestation products to replace fumigation for pre-plant soil uses. Proceedings of the 7th International Symposium on Chemical and non-Chemical Soil and Substrate Disinfestation. Leuven, Belgium.13-18 September 2009. Acta Horticult. 2010; 883(25): Pages 59-66. https://doi.org/10.17660/ActaHortic.2010.883.4
MBTOC. Methyl Bromide Technical Options Committee 2018.Assessment Report. UNEP, Nairobi.2019; 225 pp.
Michel V. Ten years of biofumigation research in Switzerland. Aspects of Applied Biology 126. 5th International Symposium of Biofumigation, 2014; 1-10.
Michel V, Urba K, Clarkson J. Green Manures and cover crops to reduce the pressure of soil-borne diseases in annual crops. In: Final report. Focus Group on Soil-borne diseases. October. Ed. EIP-AGRI, 2015; European Union. 1-5.
Brennan RJ, Glaze-Corcoran S, Wick R, Hashemi M. Biofumigation: An alternative strategy for the control of plant-parasitic nematodes. J Integrat Agricul. 2020; 19(7): 1680-1690. https://doi.org/10.1016/S2095-3119(19)62817-0
Batchelor TA. International and European Community control on methyl bromide and the status of methyl bromide use and alternatives in the European Community. In: Proc. International Conference on Alternatives to Methyl Bromide. 5-8 March 2002; Sevilla. Office for Official Publications of the European Communities: Luxembourg. 2002; pp. 35-39.
Koop F. 2020; What are the different climate zones? A simple explainer.https://www.zmescience.com/other/feature-post/climate-zones-explainer/
UNEP Ozone Secretariat. Montreal Protocol Handbook, 2020, 14 the edition. .https://ozone.unep.org/sites/default/files/Handbooks/MP-Handbook-2020-English.pdf
Luken R, Tamas GT. The Montreal Protocol's multilateral fund and sustainable development. Ecol Econom. 2006; 56: 241-255. https://doi.org/10.1016/j.ecolecon.2004.04.013
MBTOC. Report of the Methyl Bromide Technical Options Committee. 2014 Assessment. UNEP, Nairobi, Kenya, 2015; pp. 277.
Mitidieri MS, Peralta R, Barbieri M, Brambilla V, Piris E, Sasía F, Obregón V, Vasquez P A, Iriarte L, Reybet G, Barón C. Biofumigation experiences in Argentina 2017; https://cdn.harper-adams.ac.uk/document/page/2_Biofumigation-Experiences-in-Argentina.pdf
Cid del Prado Vera. Biofumigation experiment Greenhouse tomatoes Texcoco, Mexico, 2019. in: Nacobbus aberrans, 2019; http://nemaplex.ucdavis.edu/Taxadata/G085s1.aspx)
TEAP Report of the Technology and Economic Assessment Panel, Progress report, UNEP, Nairobi, Kenya. 2020; 1: 112 pp Available at https://ozone.unep.org/science/assessment/teap
Wang D, Yang Zi, Qiao, Kang, Yuan R, Yao X, Hu X, Li S. Effects of Bio Fumigation on Inhibition of cucumber Fusarium wilt, quality and yield of cucumber. Chinese Agricultural Science Bulletin. 2016; 32(28):125-130. https://doi.org/10.1360/N972015-00951
Li S, Zheng C, Zhang R, Yang Z, Qu H, Liu T, Yuan R, Yao X, Wang X, Xu N, Zhang C. Effect of biofumigation on yield and Verticillium wilt incidence of continuous eggplant in greenhouse. Journal of Northeast Agricultural University, 2017; 48(5): 35~41.
Fourie H, Ahuja P, Lammers J, Daneel M. Brassicacea-based management strategies as an alternative to combat nematode pests: a synopsis, Crop. Prot. 2016; 80: 21-41. https://doi.org/10.1016/j.cropro.2015.10.026
Ghoname AA, Riad GS, Abdel Mohsen M, El-Bassiony AM, Tantawy AS. Biofumigation with Fresh Manure or Brassicaceae Residuals could be a Promising Methyl Bromide Alternative in Head Lettuce Production. 2017; Cross ref DOI link: https://doi.org/10.1007/s10343-017-0384-x https://doi.org/10.1007/s10343-017-0384-x
Ikeda K, Banno S, Fujimura M. Suppressive effect of incorporation of on-site cultivated Indian mustard (Brassica juncea) on Verticillium wilt of eggplant. Soil Microorganisms, 2017; 71(2): pp 44-48.
Gilardi G, Cucu MA, Pugliese M, Lodovica Gullino M, Garibaldi A. Effect of different organic amendments on lettuce Fusarium wilt and on soil-borne microorganisms. Proceedings of the IXth international symposium on soil and substrate disinfestation. Heraklion, Greece, 9-13 September 2018; P 17.
Michel V, Lazzeri L. Green manures and organic amendments to control the corky root of tomato. Acta Hort. (ISHS) 2010; 883: 287-294. https://doi.org/10.17660/ActaHortic.2010.883.35
Bangarwa SK, Norsworthy JK, Mattice JD, Gbur EE. Yellow nutsedge interference in polyethylene-mulched bell pepper as influenced by turnip soil amendment. Weed Technol. 2011; 25: 3. https://doi.org/10.1614/WT-D-10-00120.1
Mashela P, Pofu K, Nzanza B. Suitability of Brassica oleracea leaves in managing Meloidogyne incognita through the ground leaching technology system under micro plot conditions. Acta Agriculturae Scandinavica, Section B. Soil & Plant Science 2013; 63(1): 19-24. https://doi.org/10.1080/09064710.2012.711351
Austerweil M, Steiner B, Gamliel A. Permeation of soil fumigants through agricultural plastic films, Phytoparasitica, 2006; 34: 491-501. https://doi.org/10.1007/BF02981205
Oz H, Coskan A, Atilgan AJ, Determination of effects of various plastic covers and biofumigation on soil temperature and soil nitrogen form in greenhouse solarization: new solarization cover material. Journal of Polymers and the Environment 2017; 25: 370-377. https://doi.org/10.1007/s10924-016-0819-y
Lopez A, Lacasa A, Guirao P, Hernendez F. Non-chemical alternatives to methyl bromide in greenhouse-grown sweet pepper in Spain. Proc. International Conference on Alternatives to Methyl Bromide. 5-8 March 2002; Sevilla. Office for Official Publications of the European Communities: Luxembourg. pp. 280-282
Oka Y. Mechanisms of nematode suppression by organic soil amendments: A review. In: Applied Soil Ecology, 2010; 44: 101-115. https://doi.org/10.1016/j.apsoil.2009.11.003
Katan J. Integrated pest management in connection with soil disinfestation. Acta Hort. 2014; 1044: 19-28. https://doi.org/10.17660/ActaHortic.2014.1044.1
Gamliel A. Application of soil disinfestation in the view of system approach: a bottleneck or a tool for improvement? Acta Hort. (ISHS) 2014; 1044: 245-25. https://doi.org/10.17660/ActaHortic.2014.1044.29
Besri M. Leading Methyl Bromide alternatives in commercial use for tomato production in different geographic regions except the United States. Proceedings of the Fifth International Conference on Alternatives to Methyl Bromide. Lisbon. Portugal. 27-30 September 2004; 127-131.
Besri M. Methyl bromide Phase out in Morocco: Current situation and future challenges. Proceedings of the Regional Consultative Meeting for Methyl Bromide Experts in Africa. Nairobi, Kenya, 2011; 13-15 April 2011.
Besri M. Leading Methyl Bromide Alternatives in Commercial Use for vegetable Production in Different Geographic Regions and particularly in the Mediterranean area. Proceedings of "A Global Policy and Technical Workshop on Methyl Bromide. Towards a successful total phase-out of methyl bromide before January 1, 2015: Approaches and Challenges". 23-25 February 2014; (Sharm El-Sheikh, Egypt).
Vintila M, Craciun S, Popescu P, Bogoescu M. Microwave energy system used for soil disinfestations. Proceedings of the IXth international symposium on soil and substrate disinfestation. Heraklion, Greece, 9-13 September 2018; P 80.
Castellá-Lorenzo G, Savigliano R, Pizano M. Breaking the bondage to methyl bromide in agriculture. UNIDO experience. Acta Hort. (ISHS) 2014; 1044: 281-287. https://doi.org/10.17660/ActaHortic.2014.1044.35
Stapleton JJ, Duncan RA. Soil disinfestation with cruciferous amendments and sublethal heating: effects on Meloidogyne incognita, Sclerotium rolfsiiand Pythium ultimum. Plant Pathol. 1998; 47: 737-742.
Ploeg AT, Stapleton JJ. Glasshouse studies on the effects of time, temperature, and amendment of soil with broccoli plant residues on the infestation of melon plants by Meloidogyne incognita and M. javanica, Nematology 2001; 3: 855-861. https://doi.org/10.1163/156854101753625353
Besri M. Solarization of soil and agricultural materials for control of Verticillium wilt and Didymella stem canker in Morocco. In: Soil solarization. Katan J. and DevayJ E., Eds, CRS press. 1991; pp. 237 243.
Besri M. Soil solarisation as an alternative to Methyl Bromide for the control of Broomrape (Orobancheramosa) in vegetables under greenhouse conditions. Proceedings of the international research conference on methyl bromide alternatives and emissions reductions, December 7-9, 1998; Orlando, Florida, 51A-1.
Besri M, Pizano M, Porter I, Solarisation and the methyl Bromide Crisis. In: Soil Solarization: Theory and Practice., Katan Jand Gamliel A, eds. Academic Press, 2012; 77-87: 266 pp. https://doi.org/10.1094/9780890544198.011
Kanaan H, Raviv M, Medina SH, Krassnovsky AD, Minz D. The effects of solar disinfestation and compost maturation level on soil microbial activity and eradication of Macrophominaphaseolina and Verticillium dahliae. Acta Horticulture 2014; 1044: VIII International Symposium on Chemical and Non-Chemical Soil and Substrate Disinfestation. https://doi.org/10.17660/ActaHortic.2014.1044.18
Klein E, Katan J, Gamliel A. Soil suppressiveness to Meloidogyne javanica as induced by organic amendments and solarization in greenhouse crops.Crop Protection, 2012; 39: 26-32. https://doi.org/10.1016/j.cropro.2012.02.013
Mitidieri M, Brambilla V, Barbieri M, Piris E, Arpía E, Celié R, Peralta R, Ferrari M. Efecto de la biosolarización y fertilización con cianamida cálcica en la producción bajo cubierta de tomate (Solanumesculentum) en San Pedro, Buenos Aires. XXXVIII Congreso Argentino de Horticultura, 5-8 October 2015. Horticultura Argentina. 2015; 34: 85.
Mitidieri MS, Brambilla MV, Barbieri MO, Piris E, Celié R, Paunero I, Arpía E. Tratamientos combinados de biosolarización y cianamida cálcica en un invernadero hortícola. 2017http://inta.gob.ar/documentos/tratamientos-combinados-de-biosolarizacion-y-cianamida-calcica-en-un-invernadero-horticola.
Lacasa A, Guerrero MM, Guirao P, Ros C Alternatives to methyl bromide in sweet pepper crops in Spain. Proc. International Conference on Alternatives to Methyl Bromide. 5-8 March 2002; Sevilla. Office for Official Publications of the European Communities: Luxembourg. pp 187-192.
Bello A, Lopez-Perez JA, Garcia-Alvarez A, Sanz R, Lacasa A. Biofumigation and nematode control in the Mediterranean region, in: Cook R.C., Hunt D.J., Eds., Proceedings, IV.International Congress of Nematology, 2004; 133-149.
Nunez-Zofio M, Larregla S, Garbisu C, Guerrero MM, Lacasa C M, Lacasa A. Application of sugar beet vinasse followed by solarization reduces the incidence of Meloidogyne incognita in pepper crops while improving soil quality. Phytoparasitica, 2013. 41.2. 181-191. https://doi.org/10.1007/s12600-012-0277-6
Gilardi G, Demarchi S, Moizio M, Gullino ML. and Garibaldi A.Disease management strategies against Fusarium wilt of basil and rocket by combining amendments and soil solarization. Acta Hort. (ISHS) 2014; 1044: 319-324. https://doi.org/10.17660/ActaHortic.2014.1044.41
Gilardi G, Pugliese M, Colla P, Gullino ML, Garibaldi A. Management of Phytophthora capsici on bell pepper and Colletotrichum coccodeson tomato by using grafting and organic amendments. Acta Hort. (ISHS) 2014; 1044: 257-262. https://doi.org/10.17660/ActaHortic.2014.1044.31
Ozturk A, Yilmaz S, Kececi M, Unlu A, Deviren A, Zcelik A, Cetinkaya S; Cevri H, Akkaya F, Ozkan CF. Alternatives to methyl bromide for tomato and cucumber production in Turkey. Proceeding of Alternatives to Methyl Bromide. Sevilla, Spain. 2002; pp. 209-214.
Popsimonova G. Non-chemical alternatives to methyl bromide used in Macedonia on vegetables. Proc. International Conference on Alternatives to Methyl Bromide. 5-8 March 2002, Sevilla. Office for Official Publications of the European Communities: Luxembourg. pp. 299-301.
Mitidieri M; Brambilla V, Saliva V, Piris E, Piris M, Celié R, Pereyra C, Del Pardo K, Chaves E, González J. Effect of different biofumigation treatment sequences on physico-chemical and biological soil parameters and on tomato and lettuce yields undercover. Horticultura Argentina. 2009; 28: 5-17 (in Spanish).
Zakaria HM, Kassab AS, Shamseldean MM, Oraby MM, El-Mourshedy MMF. Controlling the root-knot nematode, Meloidogyne incognita in cucumber plants using some soil bioagents and some amendments under simulated field conditions. Annals of Agricultural Sciences 2013; 58(1): Pages 77-82. https://doi.org/10.1016/j.aoas.2013.01.011
Li GJ, Dong QE, Ma L, Huang Y, Zhu ML, Ji YP, Wang QH, Mo MH, Zhang KQ. Management of Meloidogyne incognita on tomato with endophytic bacteria and fresh residue of Wasabia japonica. Journal of Applied Microbiology, 2014; 117: 1159-1167. https://doi.org/10.1111/jam.12590
Wang Q J, Ma Y, Wang GF, Gu ZG, Sun D, An X, Chang ZZ. Integration of biofumigation with antagonistic microorganisms can control the Phytophthora blight of pepper plants by regulating soil bacterial community structure. In: European Journal of Soil Biology. 2014; 61: 58-67. https://doi.org/10.1016/j.ejsobi.2013.12.004
Garcia-Raya P, Michel V. Combined use of organic biofumigant materials and a biological control agent: First experience in Switzerland. In: Future IPM 3.0 towards a sustainable agriculture. 19th October, Ed. IOBC-WPRS, Riva del Garda, Italy. 2017; 1.
Jin N, Lu X, Wang X. The effect of combined application of Streptomyces rubrogriseus HDZ-9-47 with soil biofumigation on soil microbial and nematode communities. Sci Rep. 2019. 9, 16886. https://doi.org/10.1038/s41598-019-52941-9
Al-Zubi MF. Non-chemical alternatives to methyl bromide use in Jordan Proc.International Conference on Alternatives to Methyl Bromide. Sevilla. Office for Official Publications of the European Communities: Luxembourg, 5-8 March 2002; pp. 291-295.
PerniolaI OS, Chorzempa SE, Staltari S, Marta Mónica A, Gassó MM, Galian LR, del Carmen Molina M. Biofumigación con Brassicajuncea L. Czerniak y Sinapis alba L. Acción sobre el crecimiento in vitro de Trichodermaspp. y Azospirillumbrasilense Tarrand, Krieg et Döbereiner. Rev. Protección Veg. 2016; 31(1): 57-62.
Yilmaz S, Celik I, Zengin S. Combining effects of soil solarisation and grafting on plant yield and soil-borne pathogens in cucumber. International Journal of Plant Production, 2011; 5(1): 95-104.
Foster JM, Naegele RP. Evaluation of Eggplant Rootstocks and Pepper Varieties for Potential Resistance to Isolates of Phytophthora capsici from Michigan and New York. Crop protection, 2013; 97(8): 1037-1041. https://doi.org/10.1094/PDIS-06-12-0562-RE
Keinath AP, Hassell RL. Control of Fusarium Wilt of Watermelon by Grafting onto Bottle gourd or Interspecific Hybrid Squash Despite Colonization of Rootstocks by Fusarium. Plant Diseases, 2014; 98: 255-266. https://doi.org/10.1094/PDIS-01-13-0100-RE
Besri M. Current situation of tomato grafting as an alternative to Methyl Bromide for Tomato production in Morocco. Proceedings of the international research conference on methyl bromide alternatives and emissions reductions, October 29- November 1, 2007; 2007b. San Diego, California, 62-1, 62-5.
Besri M. New development with tomato grafting as alternatives to Methyl Bromide in Morocco. Journal of Plant Pathology, 2008; 90: 402.
Besri M. Cucurbits grafting as an alternative to methyl bromide for cucurbits production in Morocco, 2008: Proceedings of the international research conference on methyl bromide alternatives and emissions reductions, November 11-14, Orlando, Florida.
Besri M. Economical aspects of grafting tomato in some Mediterranean countries. Proceedings of the international research conference on methyl bromide alternatives and emissions reductions, October 29- November 1, 2007; San Diego, California, 59-1, 59-5.
Louws FJ, Rivard CL, Kubota C. Grafting fruiting vegetables to manage soil-borne pathogens, foliar pathogens, arthropods, and weeds. Scientia Horticulturae. 2010; 127. 127-146. https://doi.org/10.1016/j.scienta.2010.09.023
Schwarz D, Rouphael Y, Colla G, Venema JH. Grafting as a tool to improve tolerance of vegetables to abiotic stresses: Thermal stress, water stress, and organic pollutants. Scientia Horticulturae 2010; 127: 162-171. https://doi.org/10.1016/j.scienta.2010.09.016
Khiareddine HJ, Ben Abdallah RA, Daami-Remadi M, Nefzi A, Ayed A. Grafting Tomato Cultivars for Soil Borne Disease. Suppression and Plant Growth and Yield. J Plant Pathol Microbiol 2019; 10(1): 1-8. https://doi.org/10.18393/ejss.556780
Zeist AR, Resende JTV, Pozzebon BC, Gabriel A, Silva AA, Zeist RA. Combination of solarization, biofumigation, and grafting techniques for the management of bacterial wilt in tomato. Horticultura Brasileira. 2019; 37: 260-265. DOI - http://dx.doi.org/10.1590/S0102-053620190302 https://doi.org/10.1590/s0102-053620190302
Cao A. Rotating chloropicrin fumigation and biofumigation to control strawberry soil-borne diseases. Proceedings of the IXth international symposium on soil and substrate disinfestation. Heraklion, Greece, 9-13 September 2018; P 28.
Zhang D, Yan D, Fang W, Huang B, Wang X, Zhu J, Liu J, Ouyang C, Li Y, Wang Q, Cao A. Chloropicrin alternated with biofumigation increases crop yield and modifies soil bacterial and fungal communities in strawberry production. Science of the Total Environment. 2019; 675: 615-622. https://doi.org/10.1016/j.scitotenv.2019.04.222
Haroutunian G. The use of biofumigation crops as an alternative to Methyl Bromide for the management of the root-knot nematode in greenhouse cucumber production. Agronomy. 2013; Agro Paris-Tech.
Cristóbal-Alejo J, Mora-Aguilera G, Manzanilla-López RH, Marbán-Méndoza N, Sánchez-Garcia P, del Prado-Vera IC, Evans K. Epidemiology and integrated control of Nacobbus aberrans on tomato in Mexico. Nematology, 2006; 8(5): 727-737. https://doi.org/10.1163/156854106778877929
Franco‐Navarro F, Velasco‐Azorsa R, Cid del Prado‐Vera I. Pochoniachlamydosporia vs Nacobbus aberrans: experiences in the control of the false root‐knot nematode in Mexico. Journal of Nematology, 2016; 48: 322.
Besri M. Use of Marigolds (Tagetesspp) as a cover crop for the control of tomato root-knot nematodes (Meloidogynespp) in Morocco. Proceedings of the international symposium on biofumigation 7, Plants for Soil Health, Michel V., editor, 22-26 March 2021; Switzerland (in Press).
Kumar P. Biofumigation, concept note, and compilation of session guides on biofumigation. FAO, 2005.
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