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Potential of Some Bacteria for Biological Control of Postharvest Citrus Green Mould Caused by Penicillium Digitatum

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Potential of Some Bacteria for Biological Control of Postharvest Citrus Green Mould Caused by Penicillium Digitatum Plant Protect. Sci. Vol. 53, 2017, No. 3: 00– doi: 10.17221/55/2016-PPS Potential of Some Bacteria for Biological Control of Postharvest Citrus Green Mould Caused by Penicillium digitatum Parisa MOHAMMADI 1, Elif TOZLU 1*, Recep KOTAN 1 and Merve ŞENOL KOTAN 2 1Department of Plant Protection and 2Department of Agricultural Biotechnology, Faculty of Agriculture, Ataturk University, Erzurum, Turkey *Corresponding author. [email protected] Abstract Mohammadi P., Tozlu E., Kotan R., Kotan Şenol M. (2017): Potential of some bacteria for biological control of postharvest citrus green mould caused by Penicillium digitatum. Plant Protect. Sci., 53 Ten bacteria isolate (4 Bacillus subtilis, 2 Bacillus pumilus, 2 Bacillus cereus, 1 Bacillus megaterium, and 1 Agrobac- terium radiobacter) were tested in vitro for antagonistic properties against Penicillium digitatum, the causal agent of citrus green mould. The effect of these bacteria was also observed on mycelial growth, spore germination, and spore production of the pathogenic fungus in broth culture. Extracellular enzyme activities of the bacteria were determined. According to the results of in vitro antagonistic tests and enzymes activities, the most promising bacteria were Bacillus subtilis and Agrobacterium radiobacter. These bacteria were tested for disease suppression on lemon fruits. In addition, these bacterial isolates also showed remarkable antifungal activity against the pathogen on lemon fruits. The results of this study showed that Bacillus subtilis and Agrobacterium radiobacter showed remarkable antifungal activity against the pathogen. Chitinase and glucanase enzyme activity of all the tested bacteria was positive. Protease enzyme activity was positive in all tested bacteria with the exception of Agrobacterium radiobacter. In addition, all bacteria inhibited mycelial growth and spore germination (except Agrobacterium radiobacter) of the fungus. Bacillus subtilis, Bacillus cereus, and Agrobacterium radiobacter inhibited spore production in broth culture. Bacillus subtilis and Agrobacterium radiobacter were tested on lemon fruits significantly reduced disease severity. Consequently, these isolates can be used as new biocontrol agents in controlling the post-harvest decay of citrus fruits caused by Penicillium digitatum. Keywords: Bacillus spp.; biocontrol; citrus green mould; postharvest disease; Agrobacterium radiobacter Citrus is one of the most widely produced fruits the postharvest handling of fruits (Macarisin et al. globally. It is grown commercially in more than 2007; Moss 2008; Zamani et al. 2009). 137 countries around the world (Ismail & Zhang The postharvest disease has been primarily con- 2004) with worldwide crop production of about trolled worldwide by the application of synthetic fun- 115.525 thousand tons in 2015 (FAO 2015). Citrus gicides such as imazalil, sodium ortho-phenylphenate, fruits can be infected by many fungal pathogens, and thiabendazole pyrimethanil, azoxystrobin and fludi- these pathogens cause considerable losses during oxonil (Schirra et al. 2005, 2010; D’Aquino et al. storage and transportation (Maldonado et al. 2009). 2006; Smilanick et al. 2006; Kanetis et al. 2007). Green mould, caused by the pathogen P. digitatum, is The fruit surface is completely covered by the fungi- the most economically important postharvest disease cides, and their residues remain on the fruit surface of citrus fruits in all production areas (Eckert & (Holmes & Eckert 1999). The increasing concern Eaks 1989). The pathogen is the most devastating for health hazards and environmental pollution due one, causing about 90% of production losses during to the use of chemicals has required the development 1 Vol. 53, 2017, No. 3: 00– Plant Protect. Sci. doi: 10.17221/55/2016-PPS of alternative strategies for the control of postharvest in the refrigerator. Bacterial cultures were grown on citrus diseases. Management of postharvest diseases Nutrient Agar (NA) for routine use, and maintained using microbial antagonists, natural plant-derived in Nutrient Broth (NB; all Difco, Le Pont de Claix, products and compounds that are generally recognised France) with 15% glycerol at –80°C for long-term as safe has been demonstrated to be most suitable to storage. replace the synthetic fungicides, which are either being The identity of nine bacterial isolates [B. subtilis banned or recommended for limited use (Smilanick (TV-6F, TV-12H, TV-17C, and BA-140); B. pumilus et al. 2005; Sharma et al. 2009; Talibi et al. 2014). (RK-103 and TV-73F); B. cereus (EK-7 and TV-79B), Biological control is becoming an important al- and B. megaterium (TV-103B)] in a previous study ternative in the fight against postharvest diseases and of A. radiobacter (A 16) and pathogenic fungus of fruits and as a result, there is an urgent need for in this study was confirmed according to fatty acid further research in order to develop new and more methyl ester (FAME) analysis using Sherlock Micro- efficient strategies for bio-control (Pimenta et al. bial Identification System (Microbial ID, Newark, 2008). Successful control of infections caused by a USA) (Miller 1982; Sasser 1990) and Biolog number of postharvest pathogens using antagonistic systems (Holmes et al. 1994). FAMEs were separated bacteria has been reported on citrus fruits, including by gas chromatography (HP6890; Hewlett Packard, Paenibacillus brasilensis, Bacillus subtilis, Burkholde- Palo Alto, USA) with a fused-silica capillary column ria gladioli pv. agaricicola, and Streptomyces sp. (25 m × 0.2 mm) with cross-linked 5% phenyl methyl (Kotan et al. 2009; Ketabchi et al. 2012; Elshafei silicone. FAME profiles of each bacterial isolate were et al. 2012; Mohammedi et al. 2014). identified by comparing the commercial databases This study aimed to evaluate the antifungal ac- (TSBA 40) with the MIS software package. Biolog tivities of B. subtilis (TV-6F, TV-12H, TV-17C, and identification was performed using BIOLOG420/ BA-140), B. pumilus (RK-103 and TV-73F), B. cereus Databases/GN601 and GP601 KID software. (EK-7 and TV-79B), B. megaterium (TV-103B) and Hypersensitivity test. The potential biocontrol A. radiobacter (A-16) against P. digitatum under in bacterial isolates were tested for hypersensitivity on vitro conditions. Also promising bacteria were tested tobacco (Nicotina tabacum L. var. Samsun) plants as biocontrol agents in in vivo conditions. as described by Klement et al. (1964) in previous studies. The bacterial suspension (1 × 108 CFU/ml) was prepared in sterile distilled water and infiltrated MATERIAL AND METHODS into the intercostal area of the leaves of tobacco plants using a 3-cc syringe without needle (Becton Dickin- Tested fruits. In this study, lemon fruits (Citrus son, Franklin Lakes, USA). The inoculated plants limon L.) belonging to Meyer cultivars used in the were incubated in a completely randomized design experiments were obtained from a local market. The on the greenhouse bench for 24–48 h at 20–28°C. The fruits were selected free of wounds and rots and as presence of rapid tissue necrosis at the inoculation homogeneous as possible in size, and were stored site was recorded within 24–48 h after infiltration. at 5°C under dry conditions until use. This test was repeated at least three times for each Pathogen and growth conditions. The pathogenic isolate. Sterilised distilled water (sdH2O) was used fungus P. digitatum that had been isolated from a as a negative control. decayed lemon fruit and potential biocontrol bac- Pathogenicity test. Pathogenicity tests of the antago- teria were obtained from the culture collection unit nistic bacteria and pathogenic fungus were performed in the Department of Plant Protection, Faculty of on lemon fruits belonging to Meyer cultivars. The cell Agriculture at Ataturk University, Turkey (Table 1). suspension of the antagonistic bacterial isolates (1 × Tested bacteria and growth conditions. The bio- 108 CFU/ml) and spore suspension (1 × 105 CFU/ml) control bacteria had been isolated from the rhizo- were supplemented with Tween 20. The lemon fruits sphere and phyllosphere of wild and traditionally were washed under tap water and then surface sterilised cultivated plants growing in the Eastern Anatolia with 70% ethanol and washed twice by immersion in Region of Turkey (Kotan 1998; Kotan et al. 2009; distilled and sterilised distilled water. They were left in Çakmakçi et al. 2010; Tozlu et al. 2016). The fun- a dry place to remove excess water on the surface until gal pathogen was grown on Potato Dextrose Agar being used for pathogenicity test. Fruits were dipped (PDA) and maintained on PDA slant cultures at 4°C into a cell suspension of the antagonistic bacterial cul- 2 Plant Protect. Sci. Vol. 53, 2017, No. 3: 00– doi: 10.17221/55/2016-PPS tures and spore suspension of the pathogenic fungus. Petri plates with PDA medium. The bacteria were Afterwards, the fruits were sealed in polyethylene- grown in 50-ml Erlenmeyer flasks containing 20 ml lined plastic boxes, and they were stored at 10°C, at of Nutrient Broth (NB) medium on a rotary shaker at 80% humidity under a photoperiod of 12-h light and 28°C for 24 hours. Dilution to about 1 × 108 CFU/ml 12-h dark. After incubation for 7 days, decay on the of bacterial suspension. Bacterial suspensions were fruit surface and/or fungal mycelial growth or spore individually streaked with a sterile swap on the Petri germination were determined as a positive pathogenicity plates as a circular inner edge of the plate. The plates test. Distilled water wasalone was used as a negative were wrapped together with parafilm, and were incu- control. Treatments were arranged in a randomised bated at 28°C until fungal mycelia completely covered block design. Each treatment was applied to three the agar surface in a control plate and the diameters of replicates of 5 fruits in each experiment. the fungal colonies were scored and measured in mm. Estimation of chitinase. Chitinase enzyme activi- The antifungal activity of cell-free filtrates of bac- ties were determined according to Senol et al. (2014). teria against fungi grown on PDA was observed us- Enzyme solution (0.2 ml) and 0.5 ml 0.5% (w/v) of ing the diffusion method (Mehmood et al.
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