ORIGINAL ARTICLE
Inhibitory effects of antagonistic bacteria inhabiting the rhizosphere of the sugarbeet plants, on Cercospora beticola Sacc., the causal agent of Cercospora leaf spot disease on sugarbeet
 
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1
Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, P.O. Box 5166614766, Iran
2
Department of Plant Breeding and Biotechnology, Faculty of Agriculture, University of Tabriz, Tabriz, P.O. Box 5166614766, Iran
CORRESPONDING AUTHOR
Mahdi Arzanlou
Department of Plant Protection, Faculty of Agriculture, University of Tabriz, Tabriz, P.O. Box 5166614766, Iran
Submission date: 2015-06-20
Acceptance date: 2016-01-11
 
Journal of Plant Protection Research 2016;56(1):6–14
KEYWORDS
TOPICS
ABSTRACT
In the present study, the antagonistic capability of bacterial agents inhabiting the rhizosphere of sugarbeet plants were evaluated against Cercospora beticola Sacc. under laboratory and greenhouse conditions. After preliminary screening using the dual culture method, 14 strains with higher antagonistic capability were selected for further inhibitory assays against C. beticola. Bacterial strains were identified based on the sequence data of the small subunit-rDNA (SSU-rDNA) gene. Based on the SSU sequence data, the identity of bacterial strains were determined as Bacillus (10 strains: RB1, RB2, RB3, RB4, RB5, RB6, RB7, RB8, RB9, RB10), Paenibacillus (two strains: RP1, RP2), Enterobacter (one strain: RE), and Pseudomonas (one strain: RPs). The results obtained in this study showed that in all of the assays (dual culture, volatile and non-volatile metabolites) bacterial antagonists significantly inhibited the growth of C. beticola compared to the control. Bacillus (RB2) showed the highest inhibition rate on C. beticola in all of the assays. Based on the results of the laboratory assays, three bacterial strains RB2 (Bacillus), RPs (Pseudomonas), and RE (Paenibacillus) were selected for greenhouse assays. The experiment was designed based on a completely randomised design (CRD) with the application of antagonists prior to, simultaneously, and after inoculation with C. beticola on sugarbeet leaves. The reduction in disease severity was evaluated seven days after inoculation. The results of greenhouse assays were consistent with the results of laboratory studies. The obtained results showed that bacterial antagonists significantly reduced the disease severity when compared to the control.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
 
REFERENCES (37)
1.
Arabi F., Nikravesh Z., Babaeizad V., Rezaeian V., Rahimian H. 2006. Occurrence of bacterial leaf spot of garden beet caused by Pseudomonas syringae pv. aptata in Iran. Iranian Journal of Plant Pathology 42: 655–671. (in Farsi with English summary).
 
2.
Anith K.N., Radhakrishnan N.V., Manmohandas T.P. 2003. Screening of antagonistic bacteria for biological control of nursery wilt of black pepper (Piper nigrum). Microbiologial Research 158: 91–97.
 
3.
Arzanlou M., Khodaei S., Narmani A., Bababi-ahari A., Motallebi Azar A. 2014. Inhibitory effect of Trichoderma isolates on growth of Alternaria alternata, the causal agent of leaf spot disease on sunflower, under laboratory conditions. Archives of Phytopathology and Plant Protection 47 (13): 1592–1599.
 
4.
Bargabus R.L., Zidack N.K., Sherwood J.E., Jacobsen B.J. 2002. Characterization of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiological and Molecular Plant Pathology 61 (5): 289–298.
 
5.
Bargabus R.L., Zidack N.K., Sherwood J.W., Jacobsen B.J. 2004. Screening for the identification of potential biological control agents that induce systemic acquired resistance in sugar beet. Biological Control 30 (2): 342–350.
 
6.
Chantawannakul P., Oncharoen A., Klanbut K., Chukeatirote E., Lumyong S. 2002. Characterization of protease of Bacillus subtilis strain 38 isolated from traditionally fermented soybean in Northern Thailand. Science Asia 28: 241–245.
 
7.
Cohn B., Wolff M., Cirillo P., Sholtz R. 2007. DDT and breast cancer in young women: new data on the significance of age at exposure. Environmental Health Perspectives 115 (10): 1406–1412.
 
8.
Collins D.P., Jacobsen B.J. 2003. Optimizing a Bacillus subtilis isolate for biological control of sugar beet Cercospora leaf spot. Biological Control 26 (2): 153–161.
 
9.
Emmert E.A.B., Handelsman J. 1999. Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiology Letters 171 (1): 1–9.
 
10.
Fiddaman P.J., Rossall S. 1993. The production of antifungal volatiles by Bacillus subtilis. Journal of Applied Bacteriology 74 (2): 119–126.
 
11.
Fridlender M., Inbar J., Chet I. 1993. Biological control of soil borne plant pathogens by a β-1,3 glucanase-producing Pseudomonas cepacia. Soil Biology and Biochemistry 25 (9): 1121–1221.
 
12.
Galletti S., Luigi Burzi P., Cerato C., Marinello S., Sala E. 2008. Trichoderma as a potential biocontrol agent for Cercospora leaf spot of sugar beet. Biological Control 53 (6): 917–930.
 
13.
Glick B.R. 1995. The enhancement of plant growth by free living bacteria. Canadian Journal of Microbiology 41 (2): 109–114.
 
14.
Holtschulte B. 2000. Cercospora beticola worldwide distribution and incidence. p. 5–16. In: “Cercospora beticola Sacc. Biology, Agronomic Influence and Control Measures in Sugar Beet” (M.J.C. Asher, B. Holtschulte, M.R. Molard, F. Rosso, G. Steinrücken, R. Beckers, eds.), Volume 2, International Institute for Beef Research, Brussels, Belgium, 215 pp.
 
15.
Karaoglanidis G.S., Ioannidis P.M., Thanassoulopoulos C.C. 2001. Influence of fungicide spray schedules on the sensitivity to the sterol demethylation-inhibiting fungicides in Cercospora beticola. Journal of Crop Protection 20 (10): 941–947.
 
16.
Kloepper J.W., Lifshitz R., Zablotowicz R.M. 1989. Free-living bacterial inocula for enhancing crop productivity. Trends in Biotechnology 7 (2): 39–43.
 
17.
Kloepper J.W., Ryu C.M., Zhang S. 2004. Induce systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94 (11): 1259–1266.
 
18.
Korsten L., De-Jager E.S., De-Villers E.E., Lourens A., Kotze J.M., Wehner F.C. 1995. Evaluation of bacterial epiphytes isolated from avocado leaf and fruit surfaces for biocontrol of avocado postharvest diseases. Plant Disease 79 (11): 1149–1156.
 
19.
Kraus J., Loper J.E. 1990. Biocontrol of Pythium damping-off of cucumber by Pseudomonas fluorescens PF-5: mechanistic studies. p. 172–175. In: “Plant Growth Promoting Rhizobacter” (C. Keel, B. Koller, G. Defago, eds.). The Second International Workshop on Plant Growth Promoting Rhizobacteria. Interlaken, Switzerland, 14–19 October, 1990, 237 pp.
 
20.
Lartey RT. 2003. Friendly fungi help in war against Cercospora. Available on: http://www.ars.usda.gov/sp2use... [Accessed: 20 May, 2015].
 
21.
Leroux P. 2003. [Modes of action of agrochemicals against plant pathogenic organisms]. Comptes Rendus Biologies 326 (1): 9–21. (in French, with English summary).
 
22.
McSpadden Gardener B.B. 2004. Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94 (11): 1252–1258.
 
23.
Ongena M., Jourdan E., Adam A., Paquot M., Brans A., Joris B., Arpigny J.L., Thonart P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology 9 (4): 1084–1090.
 
24.
Punja Z.K., Utkhede R.S. 2003. Using fungi and yeasts to manage vegetable crop diseases. Trends in Biotechnology 21 (9): 400–407.
 
25.
Racca P., Jörg E., Mittler S., Petersen J. 2002. Sugarbeet leaf diseases forecasting approaches for the optimization of fungicide application. Zuckerindustrie 127 (12): 949–958.
 
26.
Raupach G.S., Kloepper J.W. 2000. Biocontrol of cucumber diseases in the field by plant growth-promoting rhizobacteria with and without methyl bromide fumigation. Plant Disease 84 (10): 1073–1075.
 
27.
Rossi V., Battilani P. 1991. CERCOPRI: a forecasting model for primary infections of Cercospora leaf spot of sugarbeet. EPPO Bulletin 21 (3): 527–531.
 
28.
Shane W.W., Teng P.S. 1992. Impact of leaf spot on root weight, sugar yield and purity of Beta vulgaris. Plant Disease 76 (8): 812–820.
 
29.
Skaracis G.N., Biancardi E. 2000. Breeding for Cercospora resistance in sugar beet. p. 177–195. In: “Cercospora beticola Sacc. Biology, Agronomic Influence and Control Measures in Sugar Beet” (M.J.C. Asher, B. Holtschulte, M.R. Molard, F. Rosso, G. Steinrücken, R. Beckers, eds.), Volume 2, International Institute for Beef Research, Brussels, Belgium, 215 pp.
 
30.
Smith G.A. 1985. Response of sugarbeet in Europe and the USA to Cercospora beticola infection. Agronomy Journal 77 (1): 126–129.
 
31.
Smith G.A., Gaskill J.O. 1970. Inheritance of resistance to Cercospora leaf spot in sugarbeet. Journal of the American Society of Sugar Beet Technologists 16: 172–180.
 
32.
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA 6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30 (12): 2725–2729.
 
33.
Walker R., Innes C.M.J., Allan E.J. 2001. The potential biocontrol agent Pseudomonas antimicrobica inhibits germination of conidia and outgrowth of Botrytis cinerea. Letters in Applied Microbiology 32 (5): 346–348.
 
34.
Weiland J., Koch G. 2004. Sugar beet leaf spot disease (Cercospora beticola Sacc.). Molecular Plant Pathology 5 (3): 157–166.
 
35.
Weller D.M., Cook R.J. 1983. Suppression of take-all of wheat by seed treatments with fluorescent pseudomonads. Phytopathology 73 (3): 463–469.
 
36.
Wolf P.F.J., Verreet J.A. 2002. An integrated pest management system in Germany for the control of fungal leaf diseases in sugar beet: the IPM sugar beet model. Plant Disease 86 (4): 336–343.
 
37.
Zhang S., Reddy M.S., Kloepper J.W. 2004. Tobacco growth enhancement and blue mold disease protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90–166. Plant and Soil 262 (1): 277–288.
 
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