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American Journal of Microbiological Research. 2017, 5(1), 7-14
DOI: 10.12691/ajmr-5-1-2
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Antagonistic Fungi, Soil Amendment and Soil Solarization as an Integrated Tactics for Controlling Fusarium Root Rot of Lupine (Lupinus termis)

Mohsen E. Ibrahim1, and Ahmed E. M. Abdelaziz2

1Department of Botany and Microbiology, Faculty of Science, University of Port Said, Port Said, Egypt

2Department of Biological sciences, University of Calgary, Alberta, Canada

Pub. Date: March 22, 2017

Cite this paper:
Mohsen E. Ibrahim and Ahmed E. M. Abdelaziz. Antagonistic Fungi, Soil Amendment and Soil Solarization as an Integrated Tactics for Controlling Fusarium Root Rot of Lupine (Lupinus termis). American Journal of Microbiological Research. 2017; 5(1):7-14. doi: 10.12691/ajmr-5-1-2


The efficient control of soil-borne pathogens while avoiding environmental hazards and degradation of natural resources is the paramount challenge in crop protection sciences. Lupinus termis (lupine) is a fabaceous crop grown in Egypt for food, medical and industrial uses. The management of Fusarium root rot pathogens, which are responsible for serious losses on a number of economically important crops, including lupine, is being investigated. This study aimed to control Fusarium lupine root rot, under field conditions with no or low environmental impact; by using different control measures such as: antagonistic fungi, soil amendment and solarization singly or as an integrated disease management strategy. The integration of pest management methods is not only merely worthy, but also the more powerful practical solution for controlling soil-borne pests. Results showed that the solarized treated soil as well as the fungal antagonists, as single treatment methods in controlling Fusarium root rot revealed 80% and 81% healthy plants compared with their control that showed only 41%. Integrating soil solarization with mixed fungal inocula and soil organic amendment have been improving efficacy of controlling of lupine-fusarium-root rot by increasing the percentage number of healthy plants from 81 %, 79 % in treated unsolarized soil to 86 %, 82 % respectively in treated solarized soil. Using tactics such as solarization antagonistic fungi, and organic amendment as an integrated method, proved to be efficient for controlling the Fusarium root rot pathogen in Lupinus termis.

Lupinus termis Fusarium root rot solarization soil amendment biocontrol agent

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[1]  Ibrahim, D., Khafagy, M. and El-Kheer, A. A. (1990). Some growth substances affecting the growth, chemical composition and alkaloidal content of Lupinus termis, L. Egypt. J. Applied Sci, 5, 367-381.
[2]  Van Bruggen, A. H. (1995). Plant disease severity in high-input compared to reduced-input and organic farming systems. Plant disease, 79, 976-984.
[3]  Kennedy, A. and Smith, K. (1995). Soil microbial diversity and the sustainability of agricultural soils. Plant and soil, 170, 75-86.
[4]  Sturz, A. and Christie, B. (2003). Beneficial microbial allelopathies in the root zone: the management of soil quality and plant disease with rhizobacteria. Soil and Tillage Research, 72, 107-123.
[5]  Gullino, M., Clini, C. and Garibaldi, A. (2004). Life without methyl bromide: the Italian experience in replacing the fumigant. Communications in agricultural and applied biological sciences, 70, 13-25.
[6]  Katan, J. Soil disinfestation: one minute before methyl bromide phase out. VI International Symposium on Chemical and non-Chemical Soil and Substrate Disinfestation-SD2004 698, 2004. 19-26.
[7]  Baker, C., Henis, J., Baker, R. and Dunn, P. Commercial production and formulation of microbial biocontrol agents. New directions in biological control. Alternatives for suppressing agricultural pests and diseases. Proceedings of a UCLA Colloquium held at Frisco, Colorado, January 20-27, 1989., 1990. Alan R. Liss, Inc., 333-344.
[8]  Raupach, G. S. and Kloepper, J. W. (1998). Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology, 88, 1158-1164.
[9]  Guetsky, R., Shtienberg, D., Elad, Y. and Dinoor, A. (2001). Combining biocontrol agents to reduce the variability of biological control. Phytopathology, 91, 621-627.
[10]  Roberts, D. P., Lohrke, S. M., Meyer, S. L., Buyer, J. S., Bowers, J. H., Baker, C. J., Li, W., De souza, J. T., Lewis, J. A. and Chung, S. (2005). Biocontrol agents applied individually and in combination for suppression of soilborne diseases of cucumber. Crop Protection, 24, 141-155.
[11]  Hubbard, J., Harman, G. and Hadar, Y. (1983). Effect of soilborne Pseudomonas spp. on the biological control agent. Trkhoderma hamatum, on pea seeds. Ecology and Epidemiology, 73, 655-659.
[12]  Dandurand, L. and Knudsen, G. (1993). Influence of Pseudomonas fluorescens on hyphal growth and biocontrol activity of Trichoderma harzianum in the spermosphere and rhizosphere of pea. Phytopathology, 83, 265-270.
[13]  Baker, R. and Hornby, D. An overview of current and future strategies and models for biological control. Biological control of soil-borne plant pathogens., 1990. CAB International, 375-388.
[14]  Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. and Lorito, M. (2004). Trichoderma species—opportunistic, avirulent plant symbionts. Nature reviews microbiology, 2, 43-56.
[15]  Vinale, F., Marra, R., Scala, F., Ghisalberti, E., Lorito, M. and Sivasithamparam, K. (2006). Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Letters in Applied Microbiology, 43, 143-148.
[16]  Viterbo, A., Inbar, J., Hadar, Y. and Chet, I. (2007). Plant disease biocontrol and induced resistance via fungal mycoparasites. The mycota IV: environmental and microbial relationships. Springer Verlag, Berlin, Germany, 325-340.
[17]  Punja, Z. K., Utkhede, R. S. and Arora, D. (2004). Biological control of fungal diseases on vegetable crops with fungi and yeasts. Fungal biotechnology in agricultural, food, and environmental applications, 157-171.
[18]  Marwah, R. G., Fatope, M. O., Deadman, M. L., Al-Maqbali, Y. M. and Husband, J. (2007). Musanahol: a new aureonitol-related metabolite from a Chaetomium sp. Tetrahedron, 63, 8174-8180.
[19]  Zhang, H. and Yang, Q. (2007). Expressed sequence tags-based identification of genes in the biocontrol agent Chaetomium cupreum. Applied microbiology and biotechnology, 74, 650-658.
[20]  Tomilova, O. and Shternshis, M. (2006). The effect of a preparation from Chaetomium fungi on the growth of phytopathogenic fungi. Applied Biochemistry and Microbiology, 42, 67-71.
[21]  Borrego‐Benjumea, A., Basallote‐Ureba, M. J., Abbasi, P. A., Lazarovits, G. and Melero‐Vara, J. M. (2014). Effects of incubation temperature on the organic amendment‐mediated control of Fusarium wilt of tomato. Annals of applied biology, 164, 453-463.
[22]  Borrego-Benjumea, A., Basallote-Ureba, M., Melero-Vara, J. and Abbasi, P. (2014). Characterization of Fusarium isolates from asparagus fields and influence of soil organic amendments on Fusarium crown and root rot. Phytopathology, 104.
[23]  Motisi, N., Montfort, F., Dore, T., Romillac, N. and Lucas, P. (2009). Duration of control of two soilborne pathogens following incorporation of above‐and below‐ground residues of Brassica juncea into soil. Plant pathology, 58, 470-478.
[24]  Hansen, Z. and Keinath, A. (2013). Increased pepper yields following incorporation of biofumigation cover crops and the effects on soilborne pathogen populations and pepper diseases. Applied soil ecology, 63, 67-77.
[25]  Katan, J. (1981). Solar heating (solarization) of soil for control of soilborne pests. Annual Review of Phytopathology, 19, 211-236.
[26]  Katan, J. and Devay, J. E. (1991). Soil solarization: historical perspectives, principles, and uses. Soil solarization, 23-37.
[27]  Rubin, B. and Benjamin, A. (1984). Solar heating of the soil: involvement of environmental factors in the weed control process. Weed Science, 138-142.
[28]  Spadaro, D. and Gullino, M. L. (2005). Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Protection, 24, 601-613.
[29]  Whipps, J., Van Elsas, J., Trevors, J. and Wellington, E. (1997). Ecological considerations involved in commercial development of biological control agents for soil-borne diseases. Modern soil microbiology., 525-546.
[30]  Ramirez-Villapudua, J. and Munnecke, D. E. (1987). Control of cabbage yellows (Fusarium oxysporum f. sp. conglutinans) by solar heating of field soils amended with dry cabbage residues. Plant disease, 71, 217-221.
[31]  Gamliel, A. and Stapleton, J. (1993b). Effect of chicken compost or ammonium phosphate and solarization on pathogen control, rhizosphere microorganisms, and lettuce growth. Plant Disease, 77, 886-891.
[32]  Gamliel, A. and Stapleton, J. (1993a). Characterization of antifungal volatile compounds evolved from solarized soil amended with cabbage residues. Phytopathology, 83, 899-905.
[33]  Chellemi, D., Olson, S. M., Mitchell, D., Secker, I. and Mcsorley, R. (1997). Adaptation of soil solarization to the integrated management of soilborne pests of tomato under humid conditions. Phytopathology, 87, 250-258.
[34]  Stapleton, J. J. and Devay, J. E. (1995). Soil solarization: a natural mechanism of integrated pest management. Novel approaches to integrated pest management, 309-322.
[35]  Jackson, M. L. (1958). Soil chemical analysis.
[36]  Klein, E., Katan, J. and Gamliel, A. (2011a). Combining residues of herb crops with soil heating for control of soilborne pathogens in a controlled laboratory system. Crop Protection, 30, 368-374.
[37]  Gullino, M. L., Katan, J. and Garibaldi, A. (2012). Fusarium wilts of greenhouse vegetable and ornamental crops, American Phytopathological Society.
[38]  Garibaldi, A., Gilardi, G. and Gullino, M. Critical aspects in disease management as a consequence of the evolution of soil-borne pathogens. VIII International Symposium on Chemical and Non-Chemical Soil and Substrate Disinfestation 1044, 2014. 43-50.
[39]  Gilardi, G., Demarchi, S., Gullino, M. L. and Garibaldi, A. (2014). Effect of simulated soil solarization and organic amendments on Fusarium wilt of rocket and basil under controlled conditions. Journal of Phytopathology, 162, 557-566.
[40]  Gilardi, G., Pugliese, M., Gullino, M. and Garibaldi, A. (2015). Effect of different organic amendments on lettuce fusarium wilt and on selected soilborne microorganisms. Plant Pathology.
[41]  Bonanomi, G., Antignani, V., Pane, C. and Scala, F. (2007). Suppression of soilborne fungal diseases with organic amendments. Journal of Plant Pathology, 311-324.
[42]  Klein, E., Katan, J. and Gamliel, A. (2011b). Soil suppressiveness to Fusarium disease following organic amendments and solarization. Plant Disease, 95, 1116-1123.
[43]  Chen, Y., Gamliel, A., STapleton, J. J. and Aviad, T. (1991). Chemical, physical, and microbial changes related to plant growth in disinfested soils. Soil solarization, 103-129.
[44]  Devay, J. E., Stapleton, J. J. and Elmore, C. L. (1991). Soil Solarization. FAO Plant Production and Protection Paper.
[45]  Stapleton, J. J. Modes of action of solarization and biofumigation. Second International Conference on Soil Solarization and Integrated Management of Soilborne Pests, Aleppo (Syria), 16-21 Mar 1997, 1997. ICARDA.
[46]  Stapleton, J. J. (2000). Soil solarization in various agricultural production systems. Crop protection, 19, 837-841.
[47]  Abdel-Rahim, M., Satour, M., Mickail, K., El-Eraki, S., Grinstein, A., Chen, Y. and Katan, J. (1988). Effectiveness of soil solarization in furrow-irrigated Egyptian soils. Plant Dis, 72, 143-146.
[48]  El-Shami, M., Salem, D., Fadl, F., Ashour, W. and El-Zayat, M. (1990). Soil solarization and plant disease management: II. Effect of soil solarization in comparison with soil fumigation on the management of Fusarium wilt of tomato. Agricultural Research Review, 68, 601-611.
[49]  Chellemi, D. (2006). Effect of urban plant debris and soil management practices on plant parasitic nematodes, Phytophthora blight and Pythium root rot of bell pepper. Crop Protection, 25, 1109-1116.
[50]  Wang, K.-H. and Sipes, B. S. (2009). Solarization and Cover Cropping as Alternatives to Soil Fumigants for Nematode Management in Hawai ‘i’s Pineapple Fields. CTAHR Cooperative Extension Publication SCM-29.
[51]  Gamliel, A. and Katan, J. (2012). Soil solarization: Theory and practice, APS press St. Paul.
[52]  Mahrer, Y. and Shilo, E. (2012). Physical principles of solar heating of soils. Soil solarization, theory and practice, 147-152.
[53]  Goswami, B. K., Singh, N. and Bhattacharya, C. (2013). Solar Assisted Integrated Approach for the Management of Soil Borne Fungus and Root-Knot Nematode Diseases on Tomato at Nursery Level. Int. J. Pure Appl. Sci. Technol, 19, 75-81.
[54]  Pane, C., Spaccini, R., Piccolo, A., Scala, F. and Bonanomi, G. (2011). Compost amendments enhance peat suppressiveness to Pythium ultimum, Rhizoctonia solani and Sclerotinia minor. Biological Control, 56, 115-124.
[55]  Navrozidis, E., Zartaloudis, Z., Thomidis, T., Karagiannidis, N., Roubos, K. and Michailides, Z. (2007). Effect of Soil Plowing and Fertilization on the Susceptibility of Four Olive Cultivars to the InsectBactrocera oleae and the FungiSphaeropsis dalmatica andSpilocaea oleagina. Phytoparasitica, 35, 429-432.
[56]  Singh, K. (2011). Organic amendments to soil inoculated arbuscular mycorrhizal fungi and Pseudomonas fluorescens treatments reduce the development of root-rot disease and enhance the yield of Phaseolus vulgaris L. European Journal of Soil Biology, 47, 288-295.
[57]  Hamel, C., Vujanovic, V., Jeannotte, R., Nakano-Hylander, A. and St-Arnaud, M. (2005). Negative feedback on a perennial crop: Fusarium crown and root rot of asparagus is related to changes in soil microbial community structure. Plant and Soil, 268, 75-87.
[58]  Sabet, K. K., Saber, M. M., El-Naggar, M. A.-A., El-Mougy, N. S., El-Deeb, H. M. and El-Shahawy, I. E.-S. (2013). Using commercial compost as control measures against cucumber root-rot disease. Journal of Mycology, 2013.
[59]  Bernard, E., Larkin, R. P., Tavantzis, S., Erich, M. S., Alyokhin, A., Sewell, G., Lannan, A. and Gross, S. D. (2012). Compost, rapeseed rotation, and biocontrol agents significantly impact soil microbial communities in organic and conventional potato production systems. Applied Soil Ecology, 52, 29-41.
[60]  Taylor, F. I. (2013). Control of soil borne potato pathogens using Brassica spp. mediated biofumigation. University of Glasgow.
[61]  Bonanomi, G., Giorgi, V., Neri, D. and Scala, F. (2006). Olive mill residues affect saprophytic growth and disease incidence of foliar and soilborne plant fungal pathogens. Agriculture, ecosystems & environment, 115, 194-200.
[62]  Matthiessen, J. N. and Kirkegaard, J. A. 2006. Biofumigation and enhanced biodegradation: opportunity and challenge in soilborne pest and disease management. Critical Reviews in Plant Sciences, 25, 235-265.
[63]  Mazzola, M., Brown, J., Izzo, A. D. and Cohen, M. F. (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.
[64]  Stapleton, J. and Banuelos, G. (2009). Biomass crops can be used for biological disinfestation and remediation of soils and water. California agriculture, 63, 41-46.
[65]  Larkin, R. P. and Griffin, T. S. (2007). Control of soilborne potato diseases using Brassica green manures. Crop protection, 26, 1067-1077.
[66]  Janisiewicz, W. (1988). Biocontrol of postharvest diseases of apples with antagonist mixtures. Phytopathology, 78, 194-198.
[67]  Alabouvette, C., Hoeper, H., Lemanceau, P. and Steinberg, C. (1996). Soil suppressiveness to diseases induced by soilborne plant pathogens. Soil biochemistry, 9, 371-413.
[68]  Alabouvette, C., Schippers, B., Lemanceau, P. and Bakker, P. (1998). Biological control of Fusarium wilts. Plant-Microbe Interactions and Biological Control. GJ Boland and LD Kuykendall, eds. Marcel Dekker, New York, 15-36.
[69]  Ibrahim, M. (1994). Soil fungi as biocontrol agent of tomato fusarial-wilt. MSc thesis, Faculty of Science, Suez Canal University, Ismailia.
[70]  Ibrahim, M. (1999). Management of tomato fusarial-wilt through integrated control. Ph. D Thesis, Faculty of Science, Suez Canal University.
[71]  Wahid, O. A. (2006). Improving control of Fusarium wilt of leguminous plants by combined application of biocontrol agents. Phytopathologia Mediterranea, 45, 231-237.
[72]  Bonaterra, A., Badosa, E., Cabrefiga, J., Frances, J. and Montesinos, E. (2012). Prospects and limitations of microbial pesticides for control of bacterial and fungal pomefruit tree diseases. Trees, 26, 215-226.
[73]  Gil, S. V., Pedelini, R., Oddino, C., Zuza, M., Marinelli, A. and March, G. J. (2008). The role of potential biocontrol agents in the management of peanut root rot in Argentina. Journal of plant pathology, 35-41.
[74]  El-Mehalawy, A. A., Hassanein, N. M., Khater, H. M., El-Din, E. K. and Youssef, Y. A. (2004). Influence of maize root colonization by the rhizosphere actinomycetes and yeast fungi on plant growth and on the biological control of late wilt disease. Int. J. Agric. Biol, 6, 599-605.
[75]  Hernández-Montiel, L. G., Rueda-Puente, E. O., Cordoba-Matson, M. V., Holguín-Peña, J. R. and Zulueta-Rodríguez, R. (2013). Mutualistic interaction of rhizobacteria with arbuscular mycorrhizal fungi and its antagonistic effect on Fusarium oxysporum in Carica papaya seedlings. Crop Protection, 47, 61-66.
[76]  Martínez-Medina, A., Roldán, A. and Pascual, J. A. (2011). Interaction between arbuscular mycorrhizal fungi and Trichoderma harzianum under conventional and low input fertilization field condition in melon crops: Growth response and Fusarium wilt biocontrol. Applied Soil Ecology, 47, 98-105.
[77]  Akhtar, M. and Siddiqui, Z. (2007). Biocontrol of a chickpea root-rot disease complex with Glomus intraradices, Pseudomonas putida and Paenibacillus polymyxa. Australasian Plant Pathology, 36, 175-180.
[78]  Saldajeno, M. and Hyakumachi, M. (2011). The plant growth‐promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae stimulate plant growth and reduce severity of anthracnose and damping‐off diseases in cucumber (Cucumis sativus) seedlings. Annals of Applied Biology, 159, 28-40.
[79]  Arriaga, H., Núñez-Zofio, M., Larregla, S. and Merino, P. (2011). Gaseous emissions from soil biodisinfestation by animal manure on a greenhouse pepper crop. Crop Protection, 30, 412-419.
[80]  Núñez-Zofío, M., Larregla, S. and Garbisu, C. (2011). Application of organic amendments followed by soil plastic mulching reduces the incidence of Phytophthora capsici in pepper crops under temperate climate. Crop Protection, 30, 1563-1572.
[81]  Blok, W. J., Lamers, J. G., Termorshuizen, A. J. and Bollen, G. J. (2000). Control of soilborne plant pathogens by incorporating fresh organic amendments followed by tarping. Phytopathology, 90, 253-259.