Abstract
Thirty-five isolates of actinomycetes were characterized for their antagonistic potential against phyto-pathogens of chickpea by dual-culture and metabolite production assays. The seven most promising isolates of Streptomyces were evaluated for their physiological and plant growth-promoting traits under in vitro and in vivo conditions. All the seven isolates exhibited good growth at temperatures between 20 and 40 °C, pH between 7 and 11 and saline concentrations up to 4%; all the isolates were highly tolerant to fungicide Bavistin, three isolates were moderately tolerant to Captan and all the isolates were susceptible to Thiram, Benlate and Ridomil. All the seven isolates of Streptomyces produced siderophore, chitinase (except isolate CAI-133), cellulase, lipase, protease (except isolates BCA-689 and CAI-133), hydrocyanic acid (except isolate CAI-133), indole acetic acid and β-1,3-glucanase. The greenhouse studies revealed that the isolates of Streptomyces enhanced the plant growth by promoting root length and weight, nodule numbers, shoot weight, pod numbers and pod weight over the un-inoculated control. Under field conditions, the Streptomyces treated plots increased the nodule numbers, root weight, stover yield and grain yield over the un-inoculated control plots. In the rhizosphere, the Streptomyces were also found to enhance the total nitrogen, available phosphorus and organic carbon compared to un-inoculated control. The colonizing capability of the Streptomyces on the roots of chickpea was confirmed by scanning electron microscopic analysis. All the isolates were identified as Streptomyces species by 16S rDNA analysis; five of the seven isolates clustered in one clade, whereas the other two belonged to two different clades in phylogenetic analysis.
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References
Akhtar MS, Siddiqui ZA (2010) Effect of AM fungi on plant growth and root-rot diseases of chickpea. Am Eurasian J Agric Environ Sci 8:544–549
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Anjaiah V, Koedam N, Nowak-Thompson B, Loper JE, Hofte M, Tambong JT, Cornelis P (1998) Involvement of phenazines and anthranilate in the antagonism of Pseudomonas aeruginosa PNA1 and Tn5 derivative toward Fusarium spp. and Pythium spp. Mol Plant Microbe Int 11:847–854
Bazzicalupo M, Fani R (1995) The use of RAPD for generating specific DNA probes for microorganisms. In: Clap JP (ed) Methods in molecular biology, species diagnostic protocols: PCR and other nucleic acid methods. Humana Press Inc., Totowa, pp 112–124
Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051
Bhattacharya A, Chandra S, Barik S (2009) Lipase and protease producing microbes from the environment of sugar beet field. Ind J Agric Biochem 22:26–30
Bressen W (2003) Biological control of maize seed pathogenic fungi by use of actinomycetes. Biocontrol 48:233–240
De Boer W, Gunnewiek PJAK, Lafeber P, Janse JH, Spit BE, Woldendorp JW (1998) Anti-fungal properties of chitinolytic dune soil bacteria. Soil Boil Biochem 30:193–203
El-Tarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupine caused by Plectosporium tabacinum. Aust J Bot 51:257–266
Evangelista-Martínez Z (2014) Isolation and characterization of soil Streptomyces species as potential biological control agents against fungal plant Pathogens. World J Microbiol Biotechnol 30:1639–1647
Gopalakrishnan S, Keerthi KB, Pagidi H, Vidya MS, Deepthi K, Simi J, Srinivas V, Alekhya G, Rupela OP (2011) Biocontrol of charcoal-rot of sorghum by actinomycetes isolated from herbal vermicompost. Afr J Biotechnol 79:18142–18152
Gopalakrishnan S, Suresh P, Mamta S, Humayun P, Keerthi KB, Sandeep D, Vidya MS, Deepthi K, Rupela OP (2011) Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30:1070–1078
Gopalakrishnan S, Upadhyaya HD, Humayun P, Srinivas V, Sreevidya M, Alekhya G, Vijayabharathi R, Bhimineni RK, Seema M, Abhishek R, Rupela OP (2012) Plant growth-promoting traits of biocontrol potential bacteria isolated from rice rhizosphere. Springer Plus 1:71
Gopalakrishnan S, Srinivas V, Shravya A, Prakash B, Vijayabharathi R, Bhimineni RK, Rupela OP (2013) Evaluation of Streptomyces spp. for their plant-growth-promotion traits in rice. Can J Microbiol 59:534–539
Goudjal Y, Toumatia O, Sabaou N, Barakate M, Mathieu F, Zitouni A (2013) Endophytic actinomycetes from spontaneous plants of Algerian Sahara: indole-3-acetic acid production and tomato plants growth promoting activity. World J Microbiol Biotechnol 29:1821–1829
Hemissi I, Yassine M, Abdi N, Bouraoui M, Sifi B (2011) Effects of some Rhizobium strains on chickpea growth and biological control of Rhizoctonia solani. Afr J Microbiol Res 5:4080–4090
Hendricks CW, Doyle JD, Hugley B (1995) A new solid medium for enumerating cellulose-utilizing bacteria in soil. Appl Environ Microbiol 61:2016–2019
Hsu SC, Lockwood JL (1975) Powdered chitin Agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 29:422–426
Juan Z, Xue Q, Niu G, Lei X, Shen G, Jun-zhi D (2013) Extracellular enzyme production and fungal mycelia degradation of antagonistic Streptomyces induced by fungal mycelia preparation of cucurbit plant pathogens. Ann Microbiol 63:809–812
Khamna S, Yokota A, Peberdy JF, Lumyong S (2010) Indole-3-acetic acid production by Streptomyces spp. Isolated from some Thai medicinal plant rhizosphere soils. Eur Asia J BioSci 4:23–32
Liu YX, Shi JX, Feng YG, Yang XM, Li X, Shen QR (2013) Tobacco bacterial wilt can be biologically controlled by the application of antagonistic strains in combination with organic fertilizer. Biol Fert Soils 49:447–464
Lorck H (1948) Production of hydrocyanic acid by bacteria. Plant Physiol 1:142–146
Miller JJ, Liljeroth E, Williamsen-De Klein MJEIM, Veen JAV (1990) The dynamics of actinomycetes and fluorescent pseudomonads in wheat rhizoplane and rhizosphere. Symbiosis 9:389–391
Nagpure A, Choudhary B, Kumar S, Gupta RK (2014) Isolation and characterization of chitinolytic Streptomyces spp. MT7 and its antagonism towards wood-rotting fungi. Ann Microbiol 64:531–541
Namvar A, Sharifi RS, Khandan T (2011) Growth analysis and yield of chickpea (Cicer arietinum L.) in relation to organic and inorganic nitrogen fertilization. Ekologija 57:97–108
Nassar AH, El-Tarabily KA, Sivasithamparam K (2003) Growth promotion of bean (Phaseolus vulgaris L.) by a polyamine-producing isolate of Streptomyces griseoluteus. Plant Growth Regul 40:97–106
Nelson LM (2004) Plant growth-promoting rhizobacteria (PGPR): prospects for new inoculants. Crop Manag Netw. doi:10.1094/Cm-2004-0301-05-RV
Nelson DW, Sommers LE (1982) Total organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 3, chemical and microbiological properties. SSSA, Madison, pp 539–579
Novozamsky I, Houba VJG, Van ECKR, VanVark W (1983) A novel digestion technique for multiple element analysis. Commun Soil Sci Plant Anal 14:239–249
Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL (ed) Methods of soil analysis, Agron No 9, Part 2, ‘chemical and microbial properties, 2nd edn. American Society of Agronomy, Madison, pp 403–430
Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J Appl Microbiol 117:766–773
Pandey P, Kang SC, Maheswari DK (2005) Isolation of endophytic plant growth-promoting Burkholderia spp. MSSP from root nodules of Mimosa pudica. Curr Sci 89:177–180
Patten C, Glick BR (2002) Role of Pseudomonas putida in indole acetic acid in development of host plant root system. Appl Environ Microbiol 68:3795–3801
Poovarasan S, Mohandas S, Paneerselvam P, Saritha B, Ajay KM (2013) Mycorrhizae colonizing actinomycetes promote plant growth and control bacterial blight disease of pomegranate (Punica granatum L. cv Bhagwa). Crop Prot 53:175–181
Ranjeet KT, Janice LS, Carina MJ, Don LC, Michelle HS, Lee AD, Franklin BJ, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol 4:406–425
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Shahidi BGH, Fooladi MH, Mahdavi MJ, Shahghasi A (2004) Broad spectrum, a novel antibacterial from Streptomyces spp. Biotechnology 3:126–130
Sharma M, Mangla UN, Krishnamurthy M, Vedez V, Pande S (2010) Drought and dry root rot of chickpea. Paper presented in 5th international food legumes research conference (IFLRCV) and European conference on Grain Legumes (AEP II), pp 26–30
Shrivastava S, Souza SFD, Desai PD (2008) Production of indole-3-acetic acid by immobilized actinomycetes (Kitasatospora spp.) for soil application. Curr Sci 94:1595–1604
Siddiqui ZA (2006) PGPR: prospective biocontrol agents of plant pathogens. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 111–142
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thompson JD, Gibsom TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Verma JPB, Janardan Y, Kavindra NT, Ashok Kumar B (2013) Effect of indigenous Mesorhizobium spp. and plant growth-promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286
Wei G, Kloepper JW, Sadik T (1991) Induction of systemic resistance of cucumber to Colletotrichum orbiculare by selected strains of plant growth-promoting rhizobacteria. Phytopathology 81:1508–1512
Zhao J, Xue QH, Shen GH, Xue L, Duan JL, Wang DS (2012) Evaluation of Streptomyces spp. for biocontrol of gummy stem blight (Didymella bryoniae) and growth promotion of Cucumis melo L. Biocontrol Sci Technol 22:23–37
Acknowledgements
We are thankful to DST-INSPIRE for the financial support provided to G. Alekhya for her Ph.D. fellowship. This work has been undertaken as part of the CGIAR Research Program on Grain Legumes. ICRISAT is a member of CGIAR consortium. We also thank the staff of the Biocontrol Unit of ICRISAT, including V Srinivas, M Sreevidya, A Sathya, R Vijayabharathi, B Prakash, PVS Prasad, P Manohar, B Nagappa, D Barath, A Jabbar and S Rohini, for their significant inputs to the laboratory and field studies.
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Alekhya, G., Gopalakrishnan, S. Biological Control and Plant Growth-Promotion Traits of Streptomyces Species Under Greenhouse and Field Conditions in Chickpea. Agric Res 6, 410–420 (2017). https://doi.org/10.1007/s40003-017-0278-2
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DOI: https://doi.org/10.1007/s40003-017-0278-2
Keywords
- Actinomycetes
- Plant growth-promotion
- Biocontrol
- Chickpea