Eurasian Journal of Soil Science

Volume 5, Issue 3, Jul 2016, Pages 182 - 191
DOI: 10.18393/ejss.2016.3.182-191
Stable URL: http://ejss.fess.org/10.18393/ejss.2016.3.182-191
Copyright © 2016 The authors and Federation of Eurasian Soil Science Societies



Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea

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Abed,H., Rouag,N., Mouatassem,D., Rouabhi,A., 2016. Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea. Eurasian J Soil Sci 5(3):182 - 191. DOI : 10.18393/ejss.2016.3.182-191
Abed,H.Rouag,N.,Mouatassem,D.,& Rouabhi,A. Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea Eurasian Journal of Soil Science, DOI : 10.18393/ejss.2016.3.182-191
Abed,H.Rouag,N.,Mouatassem,D., and ,Rouabhi,A."Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea" Eurasian Journal of Soil Science, DOI : 10.18393/ejss.2016.3.182-191
Abed,H.Rouag,N.,Mouatassem,D., and ,Rouabhi,A. "Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea" Eurasian Journal of Soil Science, DOI : 10.18393/ejss.2016.3.182-191
H,Abed.N,Rouag.D,Mouatassem.A,Rouabhi "Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea" Eurasian J. Soil Sci, vol., no., pp., DOI : 10.18393/ejss.2016.3.182-191
Abed,Hannane ;Rouag,Noureddine ;Mouatassem,Dahou ;Rouabhi,Amar Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea. Eurasian Journal of Soil Science,. DOI : 10.18393/ejss.2016.3.182-191

How to cite

Abed, H., Rouag, N., Mouatassem, D., Rouabhi, A., 2016. Screening for Pseudomonas and Bacillus antagonistic rhizobacteria strains for the biocontrol of Fusarium wilt of chickpea. Eurasian J. Soil Sci. 5(3): 182 - 191. DOI : 10.18393/ejss.2016.3.182-191

Author information

Hannane Abed , Department of Microbiology, Faculty of Nature and Life Sciences, University of Ferhat Abbas Sétif 1, Sétif, Algeria
Noureddine Rouag , Department of Agronomy, Faculty of Nature and Life Sciences, University of Ferhat Abbas Sétif 1, Sétif, Algeria
Dahou Mouatassem , Department of Agronomy, Faculty of Nature and Life Sciences, University of Mohamed El Bachir El Ibrahimi (UMBI), de Bordj Bou Arreridj, Algeria
Amar Rouabhi , Department of Agronomy, Faculty of Nature and Life Sciences, University of Ferhat Abbas Sétif 1, Sétif, Algeria

Publication information

Issue published online: 01 Jul 2016
Article first published online : 23 Jan 2016
Manuscript Accepted : 20 Jan 2016
Manuscript Received: 12 Dec 2015
DOI: 10.18393/ejss.2016.3.182-191
Stable URL: http://ejss.fesss.org/10.18393/ejss.2016.3.182-191

Abstract

The aim of this work is to study the ability of several isolates belonging to Rhizobacteria (Pseudomonas and Bacillus) collected from several chickpea growing areas in Algeria, to control the mycelium growth of Fusarium oxysporum f. sp. ciceris. Interesting isolates were characterized for their morphological characteristics, physiological and biochemical activities as potential bio-control agent. Fungal inhibition tests were performed using plate assay and each isolate were tested for the production of protease, cyanide hydrogen, indole acetic acid, antifungal volatile and extracellular compound. According to API 50 CH, we are able to identify six Bacillus species (B. subtilis, B. circulans, B. lentus, B. aneurinilyticus, B. firmus, B. licheniformis; and with API 20NE test we have identified three Pseudomonas species (P. aeruginosa, P. luteola, P. fluorescens). The ability of bacterial isolates was varied in production of Protease, Gelatinase, Amylase, Cellulase, Acid Indole acetic, Lipase, Catalase and Cyanid Hydrogen. This is traduced in different rate of inhibition growth due to various extracellular compounds, where B61 (Bacillus aneurinilyticus) and P39 (Pseudomonas luteola) and P70 (Pseudomonas fluorescens) were the most efficient with 77 and 55.5% respectively, while B39 (Bacillus firmus) and P41 (Pseudomonas luteola) were the most efficient by volatile compounds with 70.5 and 77.5% respectively. Our results indicate that these bacteria isolates can be used in the biocontrol of Fusarium oxysporum f. sp. ciceris.

Keywords

Antagonistic, Bacillus, Bio-control, Chickpea, Fusarium oxysporum, Pseudomonas

Corresponding author

References

Adebayo, O.S., Ekpo, E.J.A., 2004. Efficiency of fungal and bacterial biocontrol organisms for the control of fusarium wilt of tomato. Nigerian Journal of Horticultural Sciences 9: 63-68.

Ahmad, F., Ahmad, I., Khan, M.S., 2005. Indole acetic acid production by the indigenous isolates of Azotobacter and Fluorescent Pseudomonas in the presence and absence of tryptophan. Turkish Journal of Biology 29(1): 29-34.

Ahmadzadeh, M., Tehrani, A.S., 2009. Evaluation of fluorescent pseudomonads for plant growth promotion, antifungal activity against Rhizoctonia solani on common bean, and biocontrol potential. Biological Control 48(2): 101–107.

Akhtar, M.S., Shakeel, U., Siddiqui, Z.A., 2010. Biocontrol of Fusarium wilt by Bacillus pumilus, Pseudomonas alcaligenes, and Rhizobium sp. on lentil. Turkish Journal of Biology 34(1): 1-7.

Alström, S., 1987. Factors associated with detrimental effects of rhizobacteria on plant growth. Plant and Soil 102(1): 3-9.

Athukorala, S.N., Fernando, W.G., Rashid, K.Y., 2009. Identification of antifungal antibiotics of Bacillus species isolated from different microhabitats using polymerase chain reaction and MALDI-TOF mass spectrometry. Canadian Journal of Microbiology 55(9): 1021-1032.

Bric, J.M., Bosrock, R.M., Silversone, S.E., 1991. Rapid in situ assay for indole acetic acid production by bacteria immobilization on a nitrocellulose membrane. Applied and Enviromental Microbiology 57(2): 535-538.

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 Northen Thailand. ScienceAsia 28(3): 241-245.

Chen, X., Scholz, R., Borriss, M., Junge, H., Mogel, G., Kunz, S., Borriss, R., 2009. Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens dare efficient in controlling fire blight disease. Journal of Biotechnology 140(1-2): 38-44.

Ekundayo, E.A., Adetuyi, F.C., Ekundayo, F.O., 2011. In vitro antifungal activities of Bacteria associated with maize husks and cobs. Research Journal of Microbiology 6(4): 418-424.

Erdogan, O., Benlioglu, K., 2010. Biological control of Verticillium wilt on cotton by the use of fluorescent Pseudomonas spp. under field conditions. Biological Control 53(1): 39-45.

Fatima, Z., Saleemi, M., Zia, M., Sultan, T., Aslam, M., Rehman, R., Chaudhary, M.F., 2009. Antifungal activity of plant growth-promoting rhizobacteria isolates against Rhizoctonia solani in wheat. African Journal of Biotechnology 8(2): 219-225.

Fiddaman, P.J., Rossall, S., 1993. The production of antifungal volatiles from Bacillus subtilis. Journal of Applied Microbiology 74: 119-126.

Fravel, D.R., 2005. Commercialization and implementation of biocontrol. Annual Review of Phytopathology 43: 337-359.

Godinho, A., Ramesh, R., Bhosle, S., 2010. Bacteria from sand dunes of Goa promoting growth in Eggplant. World journal of Agricultural Science 6(5): 555-564.

Gopalakrishnan, S., Beale, M.H., Ward, J.L., Strange, R.N., 2005. Chickpea wilt: identification and toxicity of 8-O-methl-fusarubin from Fusarium acutatum. Phytochemistry 66(13): 1536-1539.

Grover, M., Nain, L., Saxena, A.K., 2009. Comparison between Bacillus subtilis RP24 and its antibiotic defective mutants. World Journal of Microbiology and Biotechnology 25(8): 1329-1335.

Halila, M.H., Strange, R.N., 1996. Identification of the causal agent of wilt of chickpea in Tunisia as Fusarium oxysporum f. sp ciceris race 0. Phytopathologia Mediterranea 35(2): 67-74.

Haware, M.P., Nene, Y.L., Natarajan, M., 1996. Survival of Fusarium oxysporum f.sp ciceris in the soil in the absence of chickpea. Phytopathologia Mediterranea 35(1): 9-12

Haware, M.P., Nene, Y.L., Rajeswari, R., 1978. Eradication of Fusarium oxysporum f. sp. ciceri transmitted in chickpea seed. Phytopathology 68: 1364-1367.

Jalali, B.L., Chand, H., 1992. Chickpea wilt. In: Plant Diseases of International Importance. Vol. 1. Diseases of Cereals and Pulses. Singh, U.S., Mukhopadhayay, A.N., Kumar, J., Chaube, H.S. (Eds.), Prentice Hall, Englewood Cliffs, New York, USA. pp. 429-444.

Joseph, B., Patra, R.R., Lawrence, R., 2007. Characterization of plant growth promoting Rhizobacteria associated with chickpea (Cicer arietinum L). International Journal of Plant Production 1(2): 141-152.

Jukanti, A.K., Gaur, P.M., Gowda, C.L.L., Chibbar, R.N., 2012Nutritional quality and health benefits of chickpea (Cicer arietinum L.): A review. British Journal of Nutrition 108(S1): S11-S26.

Khot, G.G., Taur, P., Daderwal, K.R., 1996. Rhizobacteria from chickpea (Cicer arietinum L.) rhizosphere effective in wilt control and promote nodulation. Indian Journal of Microbiology 36: 217-222.

Killani, A.S., Abaidoo, R.C., Akintokun, A.K., Abiala, M.A., 2011. Antagonistic effect of indigenous Bacillus subtilis on root-/soil-borne fungal pathogens of cowpea. Researcher 3(3): 11-18.

Kloepper, J.W., Ryu, C.M., Zhang, S., 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94(11): 1259-1266.

Kloepper, J.W., Tuzun, S., Kuć, J.A., 1992. Proposed definitions related to induced disease resistance. Biocontrol Science and Technology 2(4): 349–351.

Labdi M. (1990). Chickpea in Algeria. Options Méditerranéennes, Série Séminaires 9: 137–140.

Landa, B.B., Navas-Cortés, J.A., Jiménez-Dîaz, R.M., 2004. Integrated management of fusarium wilt of chickpea with sowing date, host resistance, and biological control. Phytopathology 94(9): 946-960.

Logan, N.A., Berkeley, R.C., 1984. Identification of Bacillus Strains Using the API System. Journal of General Microbiology 130(7): 1871-1882.

Moeinzadeh, A., Sharif-Zadeh, F., Ahmadzadeh, M., Heidari Tajabadi, F., 2010. Biopriming of sunflower (Helianthus annuus L.) seed with Pseudomonas fluorescens for improvement of seed invigoration and seedling growth. Australian Journal of Crop Science  4(7): 564-570.

Montealegre J.R., Herrera, R., Velásquez, J.C., Silva, P., Besoaín, X., Pérez, L.M., 2005. Biocontrol of root and crown rot in tomatoes under greenhouse conditions using Trichoderma harzianum and Paenibacillus lentimorbus. Additional effect of solarisation. Electronic Journal of Biotechnology 8(3): 249-257.

Mudawi, H.I., Idris, M.O., 2014. The efficacy of Trichoderma spp. and Bacillus isolates in the control of chickpea wilt pathogens. Agriculture, Forestry and Fisheries 3(5): 346-351.

Nene, Y.L., Sheila, V.K., Sharma, S.B., 1996. A world list of chickpea and pigeonopea pathogens, 5th ed. ICRISAT, Patancheru, India, pp. 27.

Nene, Y.L., Haware, M.P., Reddy, N.M.V., Philps, J.P., Castro, E.L., Kotasthane, S.R., Gupta, O., Singh, G., Shukia, P., Sah, R.P. 1989. Identification of broad-based and stable resistance to wilt and root-rots in chickpea. Indian Phytopathology 42: 499-505.

Raaijmakers, J.M., Vlami, M., de Souza, J.T., 2002. Antibiotic production by bacterial biocontrol agents. Antonie Leeuwenhoek 81(1): 537-547.

Reino, J.L., Guerro, R.F., Hernández-Galán, R., Collado, I.G., 2008. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochemistry Reviews 7(1): 89–123.

Romanenko, V.M., Alimov, M., 2000. Ability of representatives of Pantoea agglomerans as well as Bacillus subtilis and some species of Pseudomonas genus to inhibit growth of phytopathogenic bacteria and micromycetes and regulate the plant growth. Mikrobiolohichnyĭ Zhurnal 62(4): 29-37 [in Ukrainian].

Saharan, B.S., Nehra, V., 2011. Plant growth promoting rhizobacteria: A critical review.  Life Sciences and Medicine Research 21: 1-30.

Sarhan, M.M., Ezzat, S.M., Tohamy, A.A., El-Essawy, A.A., Mohamed, F.A., 2001. Biocontrol of Fusarium tomato wilt diseases by Bacillus subtilis. Egyptian Journal of Microbiology 36: 376-386.

Shaad, N.W., 1988. Laboratory guide for identification of plant pathogenic bacteria. 2nd edition. St. Paul, Minn., APS Press, 164p.

Singh, K.B., Dahiya, B.S., 1973. Breeding for wilt resistance in chickpea. In: Symposium on wilt problems and breeding for wilt resistance in Bengal gram. Indian Agriculture Research Institute, New Delhi, India, pp.1-14.

Tjamos, E.C., Tsitsigiannis, D.I., Tjamos, S.E., Antoniou, P.P., Katinakis, P., 2004. Selection and screening of endorhizosphere bacteria from solarised soils as biocontrol agents against Verticillium dahlia of solanaceous hosts. European Journal of Plant Pathology 110(1): 35-44.

Tsavkelova, E.A., Cherdyntseva, T.A., Klimova, S.Y., Shestakov, A.I., Botina, S.G., Netrusov, A.I., 2007 Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Archives of Microbiology 188(6): 655-664.

Wahyudi, A.T., Astuti, R.P., Widyawati, A., Meryandini, A.A., Nawangsih, A.A., 2011. Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting rhizobacteria. Journal of Microbiology and Antimicrobials 3(2): 34-40.

Wani, P.A., Khan, M.S., Zaidi, A., 2007. Co-inoculation of nitrogen-fixing and phosphate-solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agronomica Hungarica 55(3): 315-323.

Weller, D.M., 1988. Biological control of soilborn plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology 26: 379-407.

Westerlund, F.V., Campbell, R.N., Kimble, K.A., 1974. Fungal root rot and wilt of chickpea in California. Phytopathology 64: 432–436.

Xie, H., Pasternak, J.J., Glick, B.R., 1996. Isolation and characterization of mutants of plant growth promoting rhizobacterium Pseudomonas putida GR 12-2 that over produce indoleacetic acid. Current Microbiology 32(2): 67-71.

Zeller, S.L., Brand, H., Schmid, B., 2007. Host-plant selectivity of rhizobacteria in a crop/weed model system. PLoS ONE 2(9): e846.

Abstract

The aim of this work is to study the ability of several isolates belonging to Rhizobacteria (Pseudomonas and Bacillus) collected from several chickpea growing areas in Algeria, to control the mycelium growth of Fusarium oxysporum f. sp. ciceris. Interesting isolates were characterized for their morphological characteristics, physiological and biochemical activities as potential bio-control agent. Fungal inhibition tests were performed using plate assay and each isolate were tested for the production of protease, cyanide hydrogen, indole acetic acid, antifungal volatile and extracellular compound. According to API 50 CH, we are able to identify six Bacillus species (B. subtilis, B. circulans, B. lentus, B. aneurinilyticus, B. firmus, B. licheniformis; and with API 20NE test we have identified three Pseudomonas species (P. aeruginosa, P. luteola, P. fluorescens). The ability of bacterial isolates was varied in production of Protease, Gelatinase, Amylase, Cellulase, Acid Indole acetic, Lipase, Catalase and Cyanid Hydrogen. This is traduced in different rate of inhibition growth due to various extracellular compounds, where B61 (Bacillus aneurinilyticus) and P39 (Pseudomonas luteola) and P70 (Pseudomonas fluorescens) were the most efficient with 77 and 55.5% respectively, while B39 (Bacillus firmus) and P41 (Pseudomonas luteola) were the most efficient by volatile compounds with 70.5 and 77.5% respectively. Our results indicate that these bacteria isolates can be used in the biocontrol of Fusarium oxysporum f. sp. ciceris.

Keywords: Antagonistic, Bacillus, Bio-control, Chickpea, Fusarium oxysporum, Pseudomonas

References

Adebayo, O.S., Ekpo, E.J.A., 2004. Efficiency of fungal and bacterial biocontrol organisms for the control of fusarium wilt of tomato. Nigerian Journal of Horticultural Sciences 9: 63-68.

Ahmad, F., Ahmad, I., Khan, M.S., 2005. Indole acetic acid production by the indigenous isolates of Azotobacter and Fluorescent Pseudomonas in the presence and absence of tryptophan. Turkish Journal of Biology 29(1): 29-34.

Ahmadzadeh, M., Tehrani, A.S., 2009. Evaluation of fluorescent pseudomonads for plant growth promotion, antifungal activity against Rhizoctonia solani on common bean, and biocontrol potential. Biological Control 48(2): 101–107.

Akhtar, M.S., Shakeel, U., Siddiqui, Z.A., 2010. Biocontrol of Fusarium wilt by Bacillus pumilus, Pseudomonas alcaligenes, and Rhizobium sp. on lentil. Turkish Journal of Biology 34(1): 1-7.

Alström, S., 1987. Factors associated with detrimental effects of rhizobacteria on plant growth. Plant and Soil 102(1): 3-9.

Athukorala, S.N., Fernando, W.G., Rashid, K.Y., 2009. Identification of antifungal antibiotics of Bacillus species isolated from different microhabitats using polymerase chain reaction and MALDI-TOF mass spectrometry. Canadian Journal of Microbiology 55(9): 1021-1032.

Bric, J.M., Bosrock, R.M., Silversone, S.E., 1991. Rapid in situ assay for indole acetic acid production by bacteria immobilization on a nitrocellulose membrane. Applied and Enviromental Microbiology 57(2): 535-538.

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 Northen Thailand. ScienceAsia 28(3): 241-245.

Chen, X., Scholz, R., Borriss, M., Junge, H., Mogel, G., Kunz, S., Borriss, R., 2009. Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens dare efficient in controlling fire blight disease. Journal of Biotechnology 140(1-2): 38-44.

Ekundayo, E.A., Adetuyi, F.C., Ekundayo, F.O., 2011. In vitro antifungal activities of Bacteria associated with maize husks and cobs. Research Journal of Microbiology 6(4): 418-424.

Erdogan, O., Benlioglu, K., 2010. Biological control of Verticillium wilt on cotton by the use of fluorescent Pseudomonas spp. under field conditions. Biological Control 53(1): 39-45.

Fatima, Z., Saleemi, M., Zia, M., Sultan, T., Aslam, M., Rehman, R., Chaudhary, M.F., 2009. Antifungal activity of plant growth-promoting rhizobacteria isolates against Rhizoctonia solani in wheat. African Journal of Biotechnology 8(2): 219-225.

Fiddaman, P.J., Rossall, S., 1993. The production of antifungal volatiles from Bacillus subtilis. Journal of Applied Microbiology 74: 119-126.

Fravel, D.R., 2005. Commercialization and implementation of biocontrol. Annual Review of Phytopathology 43: 337-359.

Godinho, A., Ramesh, R., Bhosle, S., 2010. Bacteria from sand dunes of Goa promoting growth in Eggplant. World journal of Agricultural Science 6(5): 555-564.

Gopalakrishnan, S., Beale, M.H., Ward, J.L., Strange, R.N., 2005. Chickpea wilt: identification and toxicity of 8-O-methl-fusarubin from Fusarium acutatum. Phytochemistry 66(13): 1536-1539.

Grover, M., Nain, L., Saxena, A.K., 2009. Comparison between Bacillus subtilis RP24 and its antibiotic defective mutants. World Journal of Microbiology and Biotechnology 25(8): 1329-1335.

Halila, M.H., Strange, R.N., 1996. Identification of the causal agent of wilt of chickpea in Tunisia as Fusarium oxysporum f. sp ciceris race 0. Phytopathologia Mediterranea 35(2): 67-74.

Haware, M.P., Nene, Y.L., Natarajan, M., 1996. Survival of Fusarium oxysporum f.sp ciceris in the soil in the absence of chickpea. Phytopathologia Mediterranea 35(1): 9-12

Haware, M.P., Nene, Y.L., Rajeswari, R., 1978. Eradication of Fusarium oxysporum f. sp. ciceri transmitted in chickpea seed. Phytopathology 68: 1364-1367.

Jalali, B.L., Chand, H., 1992. Chickpea wilt. In: Plant Diseases of International Importance. Vol. 1. Diseases of Cereals and Pulses. Singh, U.S., Mukhopadhayay, A.N., Kumar, J., Chaube, H.S. (Eds.), Prentice Hall, Englewood Cliffs, New York, USA. pp. 429-444.

Joseph, B., Patra, R.R., Lawrence, R., 2007. Characterization of plant growth promoting Rhizobacteria associated with chickpea (Cicer arietinum L). International Journal of Plant Production 1(2): 141-152.

Jukanti, A.K., Gaur, P.M., Gowda, C.L.L., Chibbar, R.N., 2012Nutritional quality and health benefits of chickpea (Cicer arietinum L.): A review. British Journal of Nutrition 108(S1): S11-S26.

Khot, G.G., Taur, P., Daderwal, K.R., 1996. Rhizobacteria from chickpea (Cicer arietinum L.) rhizosphere effective in wilt control and promote nodulation. Indian Journal of Microbiology 36: 217-222.

Killani, A.S., Abaidoo, R.C., Akintokun, A.K., Abiala, M.A., 2011. Antagonistic effect of indigenous Bacillus subtilis on root-/soil-borne fungal pathogens of cowpea. Researcher 3(3): 11-18.

Kloepper, J.W., Ryu, C.M., Zhang, S., 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94(11): 1259-1266.

Kloepper, J.W., Tuzun, S., Kuć, J.A., 1992. Proposed definitions related to induced disease resistance. Biocontrol Science and Technology 2(4): 349–351.

Labdi M. (1990). Chickpea in Algeria. Options Méditerranéennes, Série Séminaires 9: 137–140.

Landa, B.B., Navas-Cortés, J.A., Jiménez-Dîaz, R.M., 2004. Integrated management of fusarium wilt of chickpea with sowing date, host resistance, and biological control. Phytopathology 94(9): 946-960.

Logan, N.A., Berkeley, R.C., 1984. Identification of Bacillus Strains Using the API System. Journal of General Microbiology 130(7): 1871-1882.

Moeinzadeh, A., Sharif-Zadeh, F., Ahmadzadeh, M., Heidari Tajabadi, F., 2010. Biopriming of sunflower (Helianthus annuus L.) seed with Pseudomonas fluorescens for improvement of seed invigoration and seedling growth. Australian Journal of Crop Science  4(7): 564-570.

Montealegre J.R., Herrera, R., Velásquez, J.C., Silva, P., Besoaín, X., Pérez, L.M., 2005. Biocontrol of root and crown rot in tomatoes under greenhouse conditions using Trichoderma harzianum and Paenibacillus lentimorbus. Additional effect of solarisation. Electronic Journal of Biotechnology 8(3): 249-257.

Mudawi, H.I., Idris, M.O., 2014. The efficacy of Trichoderma spp. and Bacillus isolates in the control of chickpea wilt pathogens. Agriculture, Forestry and Fisheries 3(5): 346-351.

Nene, Y.L., Sheila, V.K., Sharma, S.B., 1996. A world list of chickpea and pigeonopea pathogens, 5th ed. ICRISAT, Patancheru, India, pp. 27.

Nene, Y.L., Haware, M.P., Reddy, N.M.V., Philps, J.P., Castro, E.L., Kotasthane, S.R., Gupta, O., Singh, G., Shukia, P., Sah, R.P. 1989. Identification of broad-based and stable resistance to wilt and root-rots in chickpea. Indian Phytopathology 42: 499-505.

Raaijmakers, J.M., Vlami, M., de Souza, J.T., 2002. Antibiotic production by bacterial biocontrol agents. Antonie Leeuwenhoek 81(1): 537-547.

Reino, J.L., Guerro, R.F., Hernández-Galán, R., Collado, I.G., 2008. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochemistry Reviews 7(1): 89–123.

Romanenko, V.M., Alimov, M., 2000. Ability of representatives of Pantoea agglomerans as well as Bacillus subtilis and some species of Pseudomonas genus to inhibit growth of phytopathogenic bacteria and micromycetes and regulate the plant growth. Mikrobiolohichnyĭ Zhurnal 62(4): 29-37 [in Ukrainian].

Saharan, B.S., Nehra, V., 2011. Plant growth promoting rhizobacteria: A critical review.  Life Sciences and Medicine Research 21: 1-30.

Sarhan, M.M., Ezzat, S.M., Tohamy, A.A., El-Essawy, A.A., Mohamed, F.A., 2001. Biocontrol of Fusarium tomato wilt diseases by Bacillus subtilis. Egyptian Journal of Microbiology 36: 376-386.

Shaad, N.W., 1988. Laboratory guide for identification of plant pathogenic bacteria. 2nd edition. St. Paul, Minn., APS Press, 164p.

Singh, K.B., Dahiya, B.S., 1973. Breeding for wilt resistance in chickpea. In: Symposium on wilt problems and breeding for wilt resistance in Bengal gram. Indian Agriculture Research Institute, New Delhi, India, pp.1-14.

Tjamos, E.C., Tsitsigiannis, D.I., Tjamos, S.E., Antoniou, P.P., Katinakis, P., 2004. Selection and screening of endorhizosphere bacteria from solarised soils as biocontrol agents against Verticillium dahlia of solanaceous hosts. European Journal of Plant Pathology 110(1): 35-44.

Tsavkelova, E.A., Cherdyntseva, T.A., Klimova, S.Y., Shestakov, A.I., Botina, S.G., Netrusov, A.I., 2007 Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Archives of Microbiology 188(6): 655-664.

Wahyudi, A.T., Astuti, R.P., Widyawati, A., Meryandini, A.A., Nawangsih, A.A., 2011. Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting rhizobacteria. Journal of Microbiology and Antimicrobials 3(2): 34-40.

Wani, P.A., Khan, M.S., Zaidi, A., 2007. Co-inoculation of nitrogen-fixing and phosphate-solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agronomica Hungarica 55(3): 315-323.

Weller, D.M., 1988. Biological control of soilborn plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology 26: 379-407.

Westerlund, F.V., Campbell, R.N., Kimble, K.A., 1974. Fungal root rot and wilt of chickpea in California. Phytopathology 64: 432–436.

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Eurasian Journal of Soil Science