Assessment of the Effect of Environmental Factors on the Antagonism of <i>Bacillus amyloliquefaciens</i> and <i>Trichoderma harzianum</i> to <i>Colletotrichum acutatum</i> — Oak Academic Publishing
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Assessment of the Effect of Environmental Factors on the Antagonism of <i>Bacillus amyloliquefaciens</i> and <i>Trichoderma harzianum</i> to <i>Colletotrichum acutatum</i>
Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
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Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
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Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
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Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
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Axe MIB (Molécules d’Intérêt Biologique), Unité de Recherche CEnologie EA 4577, USC 1366 INRA, UFR des Sciences Pharmaceutiques, Université de Bordeaux, ISVV (Institut des Sciences de la Vigne et du Vin), Villenave-d’Ornon, France
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Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
1 Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
2 Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
3 Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
4 Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
5 Axe MIB (Molécules d’Intérêt Biologique), Unité de Recherche CEnologie EA 4577, USC 1366 INRA, UFR des Sciences Pharmaceutiques, Université de Bordeaux, ISVV (Institut des Sciences de la Vigne et du Vin), Villenave-d’Ornon, France
6 Laboratory of Plant Biotechnology, Biology Department, Faculty of Sciences, Abdelmalek Essaadi University, Tetouan, Morocco
The effect of temperature (18°C - 30°C), water activity (0.85 - 1) and pH (4 - 9) was studied by dual culture technique on the antagonism of Bacillus amyloliquefaciens and Trichoderma harzianum to Colletotrichum acutatum , responsible of strawberry ( Fragaria x ananassa (Weston) Duchesne ex Rozier) anthracnose. The antagonistic bacteria’s strains behave significantly and differently according to the parameters studied. These results reveal useful information about the applicability of their biocontrol in agricultural culture with the change of environmental factors.
Garrido, C., Carbú, M., Fernández-Acero F.J., González-Rodríguez, V.E. and Cantoral, J.M. (2011) New Insights in the Study of Strawberry Fungal Pathogens. Genes. Genomes, Genomics 5 (Spec. Iss. 1), 24-39.
Maas, J.L. (1998) Compendium of Strawberry Diseases. Second Edition, St Paul, Minn.: APS Press, 98 p.
Barclay Poling, E. (2008) Anthracnose on Strawberry: Its Etiology, Epidemiology, and Pathology, Together with Management Strategies for Strawberry Nurseries: Introduction to the Workshop. HortScience, 43, 59-65.
Tanaka, M.A.S. and Passos, F.A. (2002) Caracterização patogênica de Colletotrichum acutatum e C. fragariae associados à antracnose do morangueiro. [Characterization of the Pathogenic: Colletotrichum acutatum and C. fragariae Associated with Strawberry Anthracnose.] Fitopatologia Brasileira, 27, 484-488. https://doi.org/10.1590/S0100-41582002000500008
Smith, B.J. (2008) Epidemiology and Pathology of Strawberry Anthracnose: A North American Perspective. HortScience, 43, 69-73.
Mari, M. and Guizzardi, M. (1998) The Postharvest Phase: Emerging Technologies for the Control of Fungal Diseases. Phytoparasitica, 26, 59-66. https://doi.org/10.1007/BF02981267
Janisiewicz, W.J. and Korsten, L. (2002) Biological Control of Postharvest Diseases of Fruits. Annual Review of Phytopathology, 40, 411-441. https://doi.org/10.1146/annurev.phyto.40.120401.130158
Conway, W.S., Leverentz, B., Janisiewicz, W.J., Blodgett, A.B., Saftner, R.A. and Camp, M.J., (2004) Integrating Heat Treatment, Biocontrol and Sodium Bicarbonate to Reduce Postharvest Decay of Apple Caused by Colletotrichum acutatum and Penicillium expansum. Postharvest Biology and Technology, 34, 11-20. https://doi.org/10.1016/j.postharvbio.2004.05.011
Mochizuki, M., Yamamoto, S., Aoki, Y. and Suzuki, S. (2012) Isolation and Characterisation of Bacillus amyloliquefaciens S13-3 as a biological Control Agent for Anthracnose Caused by Colletotrichum gloeosporioides. Biocontrol Science and Technology, 22, 697-709. https://doi.org/10.1080/09583157.2012.679644
De Costa, D.M. and Erabadupitiya, H.R.U.T. (2005) An Integrated Method to Control Postharvest Diseases of Banana Using a Member of the Burkholderia cepacia Complex. Postharv. Postharvest Biology and Technology, 36, 31-39. https://doi.org/10.1016/j.postharvbio.2004.11.007
Ashwini, N. and Srividya, S. (2014) Potentiality of Bacillus subtilis as Biocontrol Agent for Management of Anthracnose Disease of Chilli Caused by Colletotrichum gloeosporioides OGC1. 3 Biotech, 4, 127-136. https://doi.org/10.1007/s13205-013-0134-4
Vivekananthan, R., Ravi, M., Ramanathan, A. and Samiyappan, R. (2004) Lytic Enzymes Induced by Pseudomonas fluorescens and Other biocontrol Organisms Mediate Defence against the Anthracnose Pathogen in Mango. World Journal of Microbiology and Biotechnology, 20, 235-244. https://doi.org/10.1023/B:WIBI.0000023826.30426.f5
Freeman, S., Minz, D., Kolesnik, I., Barbul, O., Zveibil, A., Maymon, M., Nitzani, Y., Kirshner, B., Rav-David, D., Bilu, A., Dag, A., Shafir, S. and Elad, Y. (2004) Trichoderma Biocontrol of Colletotrichum acutatum and Botrytis cinerea and Survival in Strawberry. European Journal of Plant Pathology, 110, 361-370. https://doi.org/10.1023/B:EJPP.0000021057.93305.d9
Shovan, L.R., Bhuiyan, M.K.A., Begum, J.A. and Pervez, Z. (2008) In Vitro Control of Colletotrichum dematium Causing Anthracnose of Soybean by Fungicides, Plant Extracts and Trichoderma harzianum. International Journal of Sustainable Crop Production, 3, 10-17.
Palaniyandi, S.A., Yang, S.H., Cheng, J.H., Meng, L. and Suh, J.W. (2011) Biological Control of Anthracnose (Colletotrichum gloeosporioides) in Yam by Streptomyces sp. MJM5763. Journal of Applied Microbiology, 111, 443-455. https://doi.org/10.1111/j.1365-2672.2011.05048.x
Kredics, L., Manczinger, L., Antal, Z., Pénzes, Z., Szekeres, A., Kevei, F. and Nagy, E. (2004) In Vitro Water Activity and pH Dependence of Mycelial Growth and Extracellular Enzyme Activities of Trichoderma Strains with Biocontrol Potential. Journal of Applied Microbiology, 96, 491-498. https://doi.org/10.1111/j.1365-2672.2004.02167.x
Smith, B.J. and Black, L.L. (1990) Morphological, Cultural, and Pathogenic Variation among Colletotrichum Species Isolated from Strawberry. Plant Disease, 74, 69-76. https://doi.org/10.1094/PD-74-0069
Talhinhas, P., Sreenivasaprasad, S., Neves-Martins, J. and Oliveira, H. (2002) Genetic and Morphological Characterization of Colletotrichum acutatum Causing Anthracnose of Lupins. Phytopathology, 92, 986-996. https://doi.org/10.1094/PHYTO.2002.92.9.986
Hamdache, A., Ezziyyani, M., Badoc, A. and Lamarti, A. (2012) Effect of pH, Temperature and Water Activity on the Inhibition of Botrytis cinerea by Bacillus amyloliquefaciens Isolates. African Journal of Biotechnology, 11, 2210-2217.
Flegel, T.W. (1980) Semipermanent Microscope Slides of Microfungi using a Sticky Tape Technique. Canadian Journal of Microbiology, 26, 551-553. https://doi.org/10.1139/m80-095
Maouni, A. (2002) Principaux Agents Fongiques des poires pourries en conservation: Biologie, physiologie et application de quelques moyens de lutte chimique. [Main Fungal Agents of Rotting Conserved Pears: Biology, Physiology and Application of Some Techniques of Chemical Control.] Thèse Doct. Phytopathol. Fac. Sci. Tétouan, Maroc, 152 p.
Barbosa, M.A.G., Rehn, K.G., Menezes, M. and Mariano, R.L.R. (2001) Antagonism of Trichoderma Species on Cladosporium herbarum and Their Enzymatic Characterization. Brazilian Journal of Microbiology, 32, 98-104. https://doi.org/10.1590/S1517-83822001000200005
Han, K.S., Kim, B.R., Kim, J.T., Hahm, S.S., Hong, K.H., Chung, C.K., Nam, Y.G., Yu, S.H. and Choi, J.E. (2013) Biological Control of White Rot in Garlic using Burkholderia pyrrocinia CAB08106-4. Research in Plant Disease, 19, 21-24. https://doi.org/10.5423/RPD.2013.19.1.021
Kim, S.T. and Yun, S.C. (2011) Biocontrol Activity of Myxococcus sp. KYC 1126 against Phytophthora Blight on Hot Pepper. Research in Plant Disease, 17, 121-128. https://doi.org/10.5423/RPD.2011.17.2.121
Kwak, Y.K., Kim, I.S., Cho, M.C., Lee, S.C. and Kim, S. (2012) Growth Inhibition Effect of Environment-Friendly Farm Materials in Colletotrichum acutatum in Vitro. Journal of Bio-Environment Control, 21, 127-133.
El-Ghaouth, A., Smilanick, J.L., Brown, G.E., Ippolito, A. and Wilson, C.L. (2001) Control of Decay of Apple and Citrus Fruits in Semicommercial Tests with Candida Saitoana and 2-Deoxy-D-Glucose. Biological Control, 20, 96-101. https://doi.org/10.1006/bcon.2000.0894
Lahlali, R., Hamadi, Y., El Guilli, M. and Jijakli, M.H. (2011) Efficacy Assessment of Pichia guilliermondii Strain Z1, a New Biocontrol Agent, against Citrus Blue Mould in Morocco under the Influence of Temperature and Relative Humidity. Biological Control, 56, 217-224.
Govender, V., Korsten, L. and Sivakumar, D. (2005) Semi-Commercial Evaluation of Bacillus licheniformis to Control Mango Postharvest Diseases in South Africa. Postharvest Biology and Technology, 38, 57-65.
Kim, P.I., Ryu, J., Kim, Y.H. and Chi, Y.T. (2010) Production of Biosurfactant Lipopeptides Iturin A, Fengycin, and Surfactin A from Bacillus subtilis CMB32 for Control of Colletotrichum gloeosporioides. Journal of Microbiology and Biotechnology, 20, 138-145.
Zheng, M., Shi, Z., Shi, J., Wang, Q. and Li, Y. (2013) Antimicrobial Effects of Volatiles Produced by Two Antagonistic Bacillus Strains on the Anthracnose Pathogen in Postharvest Mangos. Biological Control, 65, 200-206.
Zivkovic, S., Stojanovic, S., Ivanovic, Z., Gavrilovic, V., Popovic, T. and Jelica, B. (2010) Screening of Antagonistic Activity of Microorganisms against Colletotrichum acutatum and Colletotrichum gloeosporioides. Archives of Biological Sciences, 62, 611-623. https://doi.org/10.2298/ABS1003611Z
Martinez, A.S.C., del C. Orozco, M.M., Martinez-Pacheco, M.M., Farias-Rodriguez, R., Govindappa, M. and Santoyo, G. (2012) Isolation and Molecular Characterization of a Novel Strain of Bacillus with Antifungal Activity from the Sorghum Rhizosphere. Genetics and Molecular Research, 11, 2665-2673. https://doi.org/10.4238/2012.July.10.15
Delgado, J.J., Sousa, S., Gonzalez, F., Rey, M. and Llobell, A. (2006) ThHog1 Controls the Hyperosmotic Stress Response in Trichoderma harzianum. Microbiology, 152, 1687-700. https://doi.org/10.1099/mic.0.28729-0
Mercado, J.A., Barcelo, M. P.C., Rey, M.C.J.L., Munoz, B.J., RuanoRosa, D., Lopez, H.C., de los Santos, B., Romero, M.F., et al. (2015) Expression of the β-1,3-glucanase Gene bgn13.1 from Trichoderma harzianum in Strawberry Increases Tolerance to Crown Rot Diseases but Interferes with Plant Growth. Transgenic Research, 24, 979-989. https://doi.org/10.1007/s11248-015-9895-3
Fernando, T.H.P.S., Jayasinghe, C.K. and Wijesundera, R.L.C. (2000) Factors Affecting Spore Production, Germination and Viability of Colletotrichum acutatum Isolates from Hevea brasiliensis. Mycological Research, 104, 681-685. https://doi.org/10.1017/S0953756200002483
Grahovac, M., Indic, D., Vukovic, S., Hrustc, J., Gvozdenac, S., Mihajlovic, M. and Tanovic, B. (2012) Morphological and Ecological Features as Differentiation Criteria for Colletotrichum Species. Zemdirbyste (Agriculture), 99, 189-195.
Miles, T.D., Gillett, J.M., Jarosz, A.M. and Schilder, A.M.C. (2013) The Effect of Environmental Factors on Infection of Blueberry Fruit by Colletotrichum acutatum. Plant Pathology, 62, 1238-1247. https://doi.org/10.1111/ppa.12061
Mukherjee, P.K. and Raghu, K. (1997) Effect of Temperature on Antagonistic and Biocontrol Potential of Trichoderma sp. on Sclerotium rolfsii. Mycopathologia, 139, 151-155. https://doi.org/10.1023/A:1006868009184
Elad, Y., Zimand, G., Zaqs, Y., Zuriel, S. and Chet, I. (1993) Use of Trichoderma harzianum in Combination or Alternation with Fungicides to Control Cucumber Gray Mould (Botrytis cinerea) under Commercial Greenhouse Conditions. Plant Pathology, 42, 324-332. https://doi.org/10.1111/j.1365-3059.1993.tb01508.x
Hjeljord, L.G., Stensvand, A. and Tronsmo, A. (2001) Antagonism of Nutrient-Activated Conidia of Trichoderma harzianum (Atroviride) P1 against Botrytis cinerea. Phytopathology, 91, 1172-1180. https://doi.org/10.1094/PHYTO.2001.91.12.1172
Naar, Z. and Kecskes, M. (1995) A Method for Selecting Trichoderma Strains Antagonistic against Sclerotinia minor. Microbiological Research, 150, 239-246.
Santamarina, M.P. and Roselló, J. (2006) Influence of Temperature and Water Activity on the Antagonism of Trichoderma harzianum to Verticillium and Rhizoctonia. Crop Protection, 25, 1130-1134.
Gotor-Vila, A., Teixido, N., Sisquella, M., Torres, R. and Usall, J. (2017) Biological Characterization of the Biocontrol Agent Bacillus amyloliquefaciens CPA-8: The Effect of Temperature, pH and Water Activity on Growth, Susceptibility to Antibiotics and Detection of Enterotoxic Genes. Current Microbiology, 74, 1089-1099. https://doi.org/10.1007/s00284-017-1289-8
Mossel, D.A.A., Corry, J.E.L., Struijk, C.B. and Baird, R.M. (1995) Essentials of the Microbiology of Foods: A Textbook for Advanced Studies. Wiley, New York.
Etcheverry, M.G., Scandolara, A., Nesci, A., Vilas Boas Ribeiro, M.S., Pereira, P., Battilani and Paola (2009) Biological Interactions to Select Biocontrol Agents against Toxigenic Strains of Aspergillus flavus and Fusarium verticillioides from Maize. Mycopathologia, 167, 287-295. https://doi.org/10.1007/s11046-008-9177-1
Bluma, R.V. and Etcheverry, M.G. (2006) Influence of Bacillus spp. Isolated from Maize Agroecosystem on Growth and Aflatoxin B1 Production by Aspergillus Section Flavi. Pest Management Science, 62, 242-251. https://doi.org/10.1002/ps.1154
Valero, A., Sanchis, V., Ramos, A.J. and Marin, S. (2007) Studies on the Interaction between Grape-Associated Filamentous Fungi on a Synthetic Medium. International Journal of Food Microbiology, 113, 271-276.
Kredics, L., Antal, Z. and Manczinger, L. (2000) Influence of Water Potential on Growth, Enzyme Secretion and in Vitro Enzyme Activities of Trichoderma harzianum at Different Temperatures. Current Microbiology, 40, 310-314. https://doi.org/10.1007/s002849910062
De Costa, D.M. and Chandima, A.A.G. (2014) Effect of Exogenous pH on Development and Growth of Colletotrichum musae and Development of Anthracnose in Different Banana Cultivars in Sri Lanka. Journal of the National Science Foundation of Sri Lanka, 42, 229-240. https://doi.org/10.4038/jnsfsr.v42i3.7396
Padan, E., Bibi, E., Ito, M. and Krulwich, T.A. (2005) Alkaline pH Homeostasis in Bacteria: New Insights. Biochimica Et Biophysica Acta-Biomembranes, 1717, 67-88.
Hyunsu, S. and Kim, M.-D. (2016) Antipathogenic Activity of Bacillus amyloliquefaciens Isolated from Korean Traditional Rice Wine. Han’guk Misaengmul-Saengmyongkong Hakhoechi, 44, 98-105.
Zhang, S.M., Wang, X.M., Meng, L.Q., Li, J., Zhao, X.Y., Cao, X., Chen, X.L., Wang, A.X. and Li, J.F. (2012) Isolation and Characterization of Antifungal Lipopeptides Produced by Endophytic Bacillus amyloliquefaciens TF28. African Journal of Microbiology Research, 6, 1747-1755.
Zouari, I., Jlaiel, L., Tounsi, S. and Trigui, M. (2016) Biocontrol Activity of the Endophytic Bacillus amyloliquefaciens Strain CEIZ-11 against Pythium aphanidermatum and Purification of Its Bioactive Compounds. Biological Control, 100, 54-62.
Jackson, A.M., Whipps, J.M. and Lynch, J.M. (1991) Effects of Temperature, pH and Water Potential on Growth of Four Fungi with Disease Biocontrol Potential. World Journal of Microbiology and Biotechnology, 7, 494-501. https://doi.org/10.1007/BF00303376