Verticillium wilt caused by Verticillium dahliae, is one of the most devastating diseases in pistachio orchards in the world including Iran. In search for an effective non-chemical strategy for the management of this disease, we evaluated the biocontrol potential of Trichoderma harzianum isolates obtained from the rhizosphere of healthy pistachio trees in different locations of the Kerman province of Iran against V. dahliae under laboratory and greenhouse conditions. Dual culture tests in the laboratory were conducted in a completely randomized design using 72 T. harzianum isolates. Twenty isolates showed the highest in vitro antagonistic activity. The results indicated that all 20 isolates were capable of inhibiting the mycelial growth of V. dahliae significantly. Among them, isolates Tr8 and Tr19 were the most effective by 88.89% and 85.12% inhibition, respectively. Extracted cell free metabolites of all effective isolates also inhibited the growth of V. dahliae in the culture medium significantly. According to the results, isolates Tr4 and Tr6 inhibited fungal pathogen growth by 94.94% and 88.15% respectively, through production of non-volatile metabolites. In the evaluation of volatile metabolites, isolates Tr5 and Tr4 were the most effective by 26.27% and 24.49% growth inhibition, respectively. Based on the results of the in vitro experiments, the five most effective isolates were selected for evaluation under greenhouse conditions for their biocontrol potential in controlling Verticillium wilt of pistachio. Results of the greenhouse, (in vivo) experiments were positive and indicated that the occurrence of wilt disease in plants treated with the antagonists alone or in combination with pathogenic fungus was lower than in plants inoculated with pathogen alone. The overall results of this study suggest that Trichoderma fungal antagonist may be an effective biocontrol agent for the control of Verticillium wilt of pistachio.
Anita S., Ponmurugan P., Ganesh Babu R. 2012. Significance of secondary metabolites and enzymes secreted by Trichoderma atroviride isolates for the biological control of phomopsis canker disease. African Journal of Biotechnology 11 (45): 10350–10357. DOI: https://doi.org/10.5897/ajb12.599
Ashworth L.J., George A.D., McCutcheon O.D. 1982. Disease-induced potassium deficiency and Verticillium wilt in cotton. Californian Agriculture 36 (9–10): 18–20.
Ayoubi N., Zafari D., Mirabolfathy M. 2014. Evaluation of β-1,3-glucanase and β-1,4-glucanase enzymes production in some Trichoderma species. Archives of Phytopathology and Plant Protection 47 (16): 1929–1941. DOI: https://doi.org/10.1080/03235408.2013.862457
Basin H., Ozturk S.B., Yegen O. 1999. Efficacy of a biological fungicide (Planter Box Trichoderma harzianum Rifai T=22) against seedling root rot pathogens (Rhizoctonia solani, Fusarium sp.) of cotton. GAP (Great Anatolia Project) – Environmental Symposium, 17–19 February, Sanleurfa, Turkey: 137–144. https://www.researchgate.net/publication/277341782
Christen A.A. 1981. A selective medium for isolating Verticillium albo-atrum from soil. Phytopathology 72: 47–49. DOI: 10.1094/Phyto-72-47
Dennis C., Webster J. 1971a. Antagonistic properties of species-groups of Trichoderma: I. Production of non-volatile antibiotics. Transactions of the British Mycological Society 57 (1): 25–39. DOI: https://doi.org/10.1016/S0007-1536(71)80077-3
Dennis C., Webster J. 1971b. Antagonistic properties of species groups of Trichoderma: II. Production of volatile antibiotics. Transactions of the British Mycological Society 57 (1): 41–48. DOI: https://doi.org/10.1016/S0007-1536(71)80078-5
El-Katatny M., Abdelzaher H., Shoulkamy M. 2006. Antagonistic actions of Pythium oligandrum and Trichoderma harzianum against phytopathogenic fungi (Fusarium oxysporum and Pythium ultimum var. ultimum). Archives of Phytopathology and Plant Protection 39 (4): 289–301. DOI: http://dx.doi.org/10.1080/03235400500222396
El-Naggar M., Kövics G.J., Sándor E., Irinyi L. 2008. Mycoparasitism and antagonistic efficiency of Trichoderma reesei against Botrytis spp. Contributii Botanice 43: 141–147. DOI: http://real.mtak.hu/id/eprint/10917
Fotoohiyan Z., Rezaee S., Shahidi Bonjar Gh.H., Mohammadi A.H., Moradi M. 2015. Induction of systemic resistance by Trichoderma harzianum isolates in pistachio plants infected with Verticillium dahliae. Journal of Nuts 6 (2): 95–111. http://ijnrs.damghaniau.ac.ir/article_516317_111039.html
Frommel M.I., Pazos G.S., Nowak J. 1991. Plant-growth stimulation and biocontrol of Fusarium wilt (Fusarium oxysporum f. sp. lycopersici) by co-inoculation of tomato seeds with Serratia plymuthica and Pseudomonas sp. Phytopathology 26: 66–73. DOI: https://eurekamag.com/research/002/187/002187032.php
Hadar Y., Chet I., Henis Y. 1979. Biological control of Rizhoctonia solani damping-off with wheat bran culture of Trichoderma harzianum. Phytopathology 69 (1): 64. DOI: https://doi.org/10.1094/phyto-69-64
Howell C.R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease 87 (1): 4–10. DOI: http://dx.doi.org/10.1094/PDIS.2003.87.1.4
Huang L.C., Ryan A.F., Cockayne D.A., Housley G.D. 2006. Developmentally regulated expression of the P2X(3) receptor in the mouse cochlea. Histochem. Cell Biology. 125: 681–692.
Jabnoun-Khiareddine H., Daami-Remadi M., Ayed F., El-Mahjoub M. 2009. Biological control of tomato Verticillium wilt by using indigenous Trichoderma spp. The African Journal of Plant Science and Biotechnology 3 (1): 26–36.
Jamdar Z., Mohammadi A.H., Mohammadi S. 2013. Study of antagonistic effects of Trichoderma species on growth of Verticillium dahliae, the causal agent of Verticillium wilt of pistachio under laboratory condition. Journal of Nuts 4 (4): 53–56.
Jorjani M., Heydari A., Zamanizadeh H.R., Rezaee S., Naraghi L., Zamzami P. 2012. Controlling sugar beet mortality disease by application of new bioformulations. Journal of Plant Protection Research 52 (3): 303–307. DOI: https://doi.org/10.2478/v10045-012-0049-9
Kakvan N., Heydari A., Zamanizadeh H.R., Rezaee S., Naraghi L. 2013. Development of new bioformulations using Trichoderma and Talaromyces fungal antagonists for biological control of sugar beetdamping-off disease. Crop Protection 53: 80–84. DOI: https://doi.org/10.1016/j.cropro.2013.06.009
Kataoka R., Yokota K., Goto I. 2010. Biocontrol of yellow disease of Brassica campestris caused by Fusarium oxysporum with Trichoderma viride under field conditions. Archives of Phytopathology and Plant Protection 43 (9): 900–909. DOI: http://dx.doi.org/10.1080/03235400802075583
Kexiang G., Xiaoguang L., Yonghong L., Tianbo Z., Shuliang W. 2002. Potential of Trichoderma harzianum and T. atroviride to control Botryosphaeria berengeriana f. sp. piricola, the cause of apple ring rot. Journal of Phytopathology 150 (4–5): 271–276. DOI: 10.1046/j.1439-0434.2002.00754.x
Mahdizadehnaraghi R., Heydari A., Zamanizadeh H.R., Rezaee S., Nikan J. 2015. Biological control of garlic (Allium) white rot disease using antagonistic fungi-based bioformulations. Journal of Plant Protection Research 55 (2): 136–141. DOI: https://doi.org/10.1515/jppr-2015-0017
Mishra B.K., Mishra R.K., Mishra R.C., Tiwari A.K., Yadav R.S., Dikshit A. 2011. Biocontrol efficacy of Trichoderma viride isolates against fungal plant pathogens causing disease in Vigna radiata L. Archives of Applied Science Research 3 (2): 361–369.
Morton D.T., Stroube W.H. 1955. Antagonistic and stimulatory effects of microorganism upon Sclerotium rolfsii. Phytopathology 45 (8): 419–420.
Naraghi L., Heydari A., Rezaee S., Razavi M., Mahmoodi Khaledi E. 2010. Biological control of tomato Verticillium wilt disease by Talaromyces flavus. Journal of Plant Protection Research 50 (4): 341–346. DOI: https://doi.org/10.2478/v10045-010-0061-x
Papavizas G.C. 1985. Trichoderma and Gliocladium: biology, ecology and potential for the biocontrol. Annual Review of Phytopathology 23: 23–54. DOI: 10.1146/annurev.py.23.090185.000323
Rahel Ratnakumari Y., Nagamani A., Bhramaramba S., Sunil kumar R., Chandra Kumar U., Shaik M. 2011. Non-volatile and volatile metabolites of antagonistic Trichoderma against collar rot pathogen of Mentha arvensis. International Journal of Pharmaceutical and Biomedical Research 2 (2): 56–58.
Rifai M.A. 1969. A revision of the genus Trichoderma. Commonwealth Mycological Institute, Mycological Papers 116, 56 pp.
Samavat S. Heydari A., Zamanizadeh H.R., Rezaee S., Alizadeh Aliabadi A. 2014. Comparison between Pseudomonas aureofaciens (chlororaphis) and P. fluorescens in biological control of cotton seedling damping-off disease. Journal of Plant Protection Research 54 (2): 115–121. DOI: https://doi.org/10.2478/jppr-2014-0019
Thrane C., Jensen D.F., Tronsmo A. 2000. Substrate colonization, strain competition, enzyme production in vitro, and Biocontrol of Pythium ultimum by Trichoderma spp. Isolates P1 and T3. European Journal of Plant Pathology 106: 215–225. DOI: 10.1023/A:1008798825014
Tong-Kwee L., Boon Keng T. 1990. Antagonism in vitro of Trichoderma species against several basidiomycetous soil-borne pathogens and Sclerotium rolfsii. Plant Disease and Protection 97 (10): 33–41.
Tsror L., Levin E.G. 2003. Vegatative compatibility and pathogenecity of Verticillium dahliae Kleb. Isolation from Israel. Journal of Phytopathology 151 (7–8): 451–455. DOI: 10.1046/j.1439-0434.2003.00749.x
Vinale F., Ghisalberti E.L., Sivasithamparam K., Marra R., Ritieni A., Ferracane R., Woo S., Lorito M. 2009. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters in Applied Microbiology 48 (6): 705–711. DOI: 10.1111/j.1472-765X.2009.02599.x
Williams G.E., Asher M.J.C. 1996. Selection of rhizobacteria for the control of Pythium ultimum and Aphanomyces cochlioides on sugar-beet seedlings. Crop Protection 15 (5): 479–486. DOI: https://doi.org/10.1016/0261-2194(96)00014-2
Williamson B., Tudzynski B., Tudzynski P., Van Kan J.A.L. 2007. Botrytis cinerea: the cause of grey mould disease. Molecular of Plant Pathology 8 (5): 561–580. DOI: 10.1111/j.1364-3703.2007.00417.x
Zakaria M.H. 1989. Some aspects of the biology and chemically assisted biological control of Ganoderma species in Malaysia, Ph.D., University of Putra, Malaysia.
Ziedan E.H., Saad M., Farrag (Eman) S. 2005. Biological control of grapevine root-rot by antagonistic microorganisms. Africal Journal of Mycology and Biotechnology 13 (3): 19–36.
Zhou J., Wang Y.H., Chu J., Zhuang Y.P., Zhang S.L., Yin P. 2008. Identification and purification of the main components of cellulases from a mutant strain of 474 Trichoderma viride T100-14. Bioresource Technology 99 (15): 6826–6833. DOI: https://doi.org/10.1016/j.biortech.2008.01.077