Abstract
Fourteen Streptomyces strains reported earlier as plant growth promoters (PGP) in chickpea were characterized for production of ammonia and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase and solubilization of silica and zinc. The results showed that nine (CAI-17, CAI-78, KAI-26, CAI-21, CAI-26, MMA-32, CAI-140, CAI-155 and KAI-180) and six (CAI-17, CAI-21, CAI-26, CAI-13, CAI-93 and KAI-180) strains were found to produce ammonia and ACC deaminase, respectively, while one (KAI-180) and eight (CAI-17, CAI-21, CAI-26, MMA-32, CAI-13, CAI-85, CAI-93 and KAI-180) strains solubilized silica and zinc, respectively. The selected 14 Streptomyces strains were categorized into three consortia groups, consortium-1 (CAI-17, CAI-68, CAI-78, KAI-26 and KAI-27), consortium-2 (CAI-21, CAI-26 and MMA-32) and consortium-3 (CAI-13, CAI-85, CAI-93, CAI-140, CAI-155 and KAI-180), based on their compatibility, and evaluated for their PGP traits in chickpea. The experiment was conducted under field conditions with two chickpea varieties over two years. The consortia-treated plots enhanced nodule number up to 23%, nodule weight up to 36%, root weight up to 27% and shoot weight up to 26% at 30 days after sowing and pod weight up to 35%, pod number up to 34% and grain yield up to 24% at harvest over the un-inoculated control plots. The harvested grains of consortia treatments were found to enhance crude protein up to 14%, crude fibre up to 17% and crude fat up to 16% over the grains from un-inoculated control. The rhizosphere soils of the consortia-treated plots enhanced total nitrogen up to 21%, organic carbon up to 8% and available phosphorous up to 16% over the un-inoculated control plots. This investigation demonstrated the potential use of the selected consortium of Streptomyces strains in the farmers’ fields to improve the chickpea yields and soil fertility.
This is a preview of subscription content, access via your institution.

Abbreviations
- PGP:
-
Plant growth promotion
- PGPM:
-
Plant growth-promoting microorganisms
- ACC:
-
1-Aminocyclopropane-1-carboxylate
- SCB:
-
Starch casein broth
- DAS:
-
Days after sowing
References
Anwar S, Ali B, Sajid I (2016) Screening of rhizospheric actinomycetes for various in-vitro and in-vivo plant growth promoting traits and for agro-active compounds. Front Microbiol 7:1334. https://doi.org/10.3389/fmicb.2016.01334
AOAC (2005) Official Methods of Analysis of Association of Official Analytical Chemists, 18th edn. Washington, DC
Baliyan N, Dheeman S, Maheshwari DH, Dubey RC, Vishnoi VK (2018) Rhizobacteria isolated under field first strategy improved chickpea growth and productivity. Environ Sustain 1:461–469. https://doi.org/10.1007/s42398-018-00042-0
Behera B, Das TK, Raj R, Ghosh S, Raza MB, Sen S (2020) Microbial consortia for sustaining productivity of non-legume crops: prospects and challenges. Agric Res 1:1–14. https://doi.org/10.1007/s40003-020-00482-3
Bhatt K, Maheshwari DK (2019) Decoding multifarious role of cow dung bacteria in mobilization of zinc fractions along with growth promotion of C. annuum. Sci Rep 9:1–10. https://doi.org/10.1038/s41598-019-50788-8
Bradacova K, Florea AS, Bar-Tal A, Minz D, Yermiyahu U, Shawahna R, Kraut-Cohen J, Zolti A, Erel R, Dietel K, Weinmann M, Zimmermann B, Berger N, Ludewig U, Neumann G, Posta G (2019) Microbial consortia versus single-strain inoculants: an advantage in PGPM-assisted tomato production? Agronomy 9:105. https://doi.org/10.3390/agronomy9020105
Bradacova K, Kandeler E, Berger N, Ludewig U, Neumann G (2020) Microbial consortia inoculants stimulate early growth of maize depending on nitrogen and phosphorous supply. Plant Soil Environ 66:105–112. https://doi.org/10.17221/382/2019-PSE
El-Tarabily KA (2008) Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase–producing Streptomycete actinomycetes. Plant Soil 308:161–174. https://doi.org/10.1007/s11104-008-9616-2
Gopalakrishnan S, Kiran BK, Humayun P, Vidya MS, Deepthi K, Rupela O (2011) Biocontrol of charcoal-rot of sorghum by actinomycetes isolated from herbal vermicompost. Afr J Biotech 10(79):18142–18152. https://doi.org/10.5897/AJB11.2710
Gopalakrishnan S, Humayun P, Srinivas S, Vijayabharathi R, Ratnakumari B, Rupela O (2012) Plant growth-promoting traits of biocontrol potential Streptomyces isolated from herbal vermicompost. Biocontrol Sci Technol 22(10):1199–1210. https://doi.org/10.1080/09583157.2012.719151
Gopalakrishnan S, Srinivas V, Shravya A, Prakash B, Ratnakumari B, Vijayabharathi R, Rupela O (2013) Evaluation of Streptomyces spp. for their plant growth-promoting traits in rice. Can J Microbiol 59:534–539. https://doi.org/10.1139/cjm-2013-0287
Gopalakrishnan S, Srinivas V, Prakash B, Arumugam S, Vijayabharathi R, Rupela O, Kudapa H, Krishnamohan K, Varshney RK (2014) Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res 169:40–48. https://doi.org/10.1016/j.micres.2013.09.008Get
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, Varshney RK (2015a) The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. Springerplus 4(31):1–10. https://doi.org/10.1186/s40064-015-0811-3
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Varshney RK (2015b) Evaluation of broad-spectrum Streptomyces sp. for plant growth promotion traits in chickpea (Cicer arietinum L.). Philipp Agric Sci 98(3):270–278. https://hdl.handle.net/20.500.11766/6999
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B (2015c) Effect of plant growth-promoting Streptomyces sp. on growth promotion and grain yield in chickpea (Cicer arietinum L.). 3 Biotech 5:799–806. https://doi.org/10.1007/s13205-015-0283-8
Gopalakrishnan S, Sathya A, Vijayabharathi R (2016a) A book entitled “Plant Growth-Promoting Actinobacteria: A New Avenue for Enhancing the Productivity & Soil Fertility of Grain Legumes”. Springer, Singapore. ISBN 978-981-10-0705-7
Gopalakrishnan S, Srinivas V, Sameer Kumar CV (2016b) Plant growth-promotion traits of Streptomyces sp. in pigeonpea. Legume Perspect 11:43–44
Gopalakrishnan S, Rajendran V, Arumugam S, Sharma HC, Vadlamudi S, Bhimineni RK, Gonzalez SV, Melø TM, Simic N (2016c) Insecticidal activity of a novel fatty acid amide derivative from Streptomyces species against Helicoverpa armigera. Nat Prod Res 30:2760–2769. https://doi.org/10.1080/14786419.2016.1154055
Gopalakrishnan S, Sharma R, Srinivas V, Naresh N, Mishra SP, Ankati S, Pratyusha S, Govindaraj M, Gonzalez SV, Nervik S, Simic N (2020a) Identification and characterization of a Streptomyces albus strain and its secondary metabolite organophosphate against charcoal rot of sorghum. Plants 9:1727. https://doi.org/10.3390/plants9121727
Gopalakrishnan S, Thakur V, Saxena RK, Vadlamudi S, Purohit S, Kumar V, Rathore A, Chitikineni A, Varshney RK (2020b) Complete genome sequence of sixteen plant growth promoting Streptomyces strains. Sci Rep 10(1):10294. https://doi.org/10.1038/s41598-020-67153-9
Gopalakrishnan S, Srinivas V, Naresh N, Mishra SP, Ankati S, Pratyusha S, Madhuprakash J, Govindaraj M, Sharma R (2021) Deciphering the antagonistic effect of Streptomyces spp. and host-plant resistance induction against charcoal rot of sorghum. Planta 253:57. https://doi.org/10.1038/s41598-020-67153-9
Joshi B, Chaudhary A, Singh H, Kumar PA (2020) Prospective evaluation of individual and consortia plant growth-promoting rhizobacteria for drought stress amelioration in rice (Oryza sativa L.). Plant Soil 457:225–240. https://doi.org/10.1007/s11104-020-04730-x
Ju W, Liu L, Fang L, Cui Y, Dyan C, Wu H (2019) Impact of co-inoculation with plant growth-promoting rhizobacteria and Rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxical Environ Saf 167:218–226. https://doi.org/10.1016/j.ecoenv.2018.10.016
Kang S, Waqas M, Shahzad R, You Y, Asaf S, Khan MA, Lee K, Joo G, Kim S, Lee I (2017) Isolation and characterization of a novel silicate-solubilizing bacterial strain Burkholderia eburnea CS4–2 that promotes growth of japonica rice (Oryza sativa L. cv. Dongjin). Soil Sci Plant Nutr 63(3):233–241. https://doi.org/10.1080/00380768.2017.1314829
Kumar P, Aeron A, Shaw N, Singh A, Bajpai VK, Pant S, Dubey RC (2020) Seed bio-priming with tri-species consortia of phosphate solubilizing rhizobacteria (PSR) and its effect on plant growth-promotion. Heliyon 6:e05701. https://doi.org/10.1016/j.heliyon.2020.e05701
Lopes SP, Azevedo NF, Pereira MO (2018) Quantitative assessment of individual populations within polymicrobial biofilms. Sci Rep 8:9494. https://doi.org/10.1038/s41598-018-27497-9
Molina-Romero D, Juarez-Sanchez S, Venegas B, Ortiz-Gonzalez CS, Baez A, Morales-Garcia YE, Munoz-Rojas J (2021) A bacterial consortium interacts with different varieties of maize promotes the plant growth and reduces the application of chemical fertilizer under field conditions. Front Sustain Food Syst 4:616757. https://doi.org/10.3389/fsufs.2020.616757
Nawaz A, Shahbaz M, Asadullah IA, Marghoob MU, Imitaz M, Mubeen F (2020) Potential salt tolerant PGPR in growth and yield augmentation of wheat (Triticum aestivum L.) under saline conditions. Front Microbiol. https://doi.org/10.3389/fmicb.2020.02019
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 39–579. https://doi.org/10.2134/agronmonogr9.2.2ed.c29
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
Olanrewaju OS, Babalola OO (2019) Bacterial consortium for improved maize production. Microorganisms 7:519. https://doi.org/10.3390/microorganisms7110519
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, Am Soc Agron, Madison, pp 403−430
Pandey S, Gupta S, Ramawat N (2019) Unravelling the potential of microbes isolated from rhizospheric soil of chickpea (Cicer arietinum L.) as plant growth promoter. 3 Biotech 9:277. https://doi.org/10.1007/s13205-019-1809-2
Patil R, Jeyasekaran G, Shanmugam S (2016) Bio-activity of marine actinomycetes against food-borne human pathogens. Int J Sci Nat 7:582–586
Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15. https://doi.org/10.1034/j.1399-3054.2003.00086.x
Rana A, Saharan B, Nain L, Prasanna R, Shivay YS (2012) Enhancing micronutrient uptake and yield of wheat through bacterial PGPR consortia. Soil Sci Plant Nutr 58:573–582. https://doi.org/10.1080/00380768.2012.716750
Richardson AE, Barea JM, Mcneill AM, Combaret CP (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth-promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Sadeghi A, Karimi E, Dahazi PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth-promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil condition. World J Microbiol Biotechnol 28:1503–1509. https://doi.org/10.1007/s11274-011-0952-7
Sagar A, Sayyed RZ, Ramteke PW, Sharma S, Marraiki N, Elgorban AM, Syed A (2020) ACC deaminase and antioxidant enzymes producing halophilic Enterobacter sp. PR14 promotes the growth of rice and millets under salinity stress. Physiol Mol Biol Plants 26:1847–1854. https://doi.org/10.1007/s12298-020-00852-9
Santoyo G, Guzman-Guzman P, Parra-Cota FI, Santos-Villalobos S, Orozco-Mosqueda MC, Glick BR (2021) Plant growth-stimulation by microbial consortia. Agronomy 11:219. https://doi.org/10.3390/agronomy11020219
Sathya A, Vijayabharathi R, Srinivas V, Gopalakrishnan S (2016) Plant growth-promoting actinobacteria on chickpea seed mineral density: an upcoming complementary tool for sustainable biofortification strategy. 3 Biotech 6:138. https://doi.org/10.1007/s13205-016-0458-y
Sharma SK, Sharma MP, Ramesh A, Joshi OP (2012) Characterization of zinc solubilizing Bacillus isolates and their potential to influence zinc assimilation in soybean seeds. J Microbiol Biotechnol 22:352–359. https://doi.org/10.4014/jmb.1106.05063
Shaukat K, Affrasayab S, Hasnain S (2006) Growth responses of Triticum aestivum to plant growth-promoting rhizobacteria used as a biofertilizer. Res J Microbiol 1:330–338. https://doi.org/10.17311/jm.2006.330.338
Shutsrirung A, Chromkaew Y, Pathom-Aree W, Choonluchanon S, Boonkerd N (2013) Diversity of endophytic actinomycetes in mandarin grown in northern Thailand, their phytohormone production potential and plant growth promoting activity. Soil Sci Plant Nutr 59:322–330. https://doi.org/10.1080/00380768.2013.776935
Sravani A, Vadlamudi S, Sambangi P, Gopalakrishnan S (2021) Streptomyces consortia-mediated plant defense against Fusarium wilt and plant growth-promotion in chickpea. Microb Pathogenesis 157:104961. https://doi.org/10.1016/j.micpath.2021.104961
Sreevidya M, Gopalakrishnan S, Kudapa H, Varshney RK (2016) Exploring PGP actinomycetes from vermicompost and rhizosphere soil for yield enhancement in chickpea. Braz J Microbiol 47:85–95. https://doi.org/10.1016/j.bjm.2015.11.030
Srinivas V, Gopalakrishnan S, Kamidi JP, Chander G (2020) Effect of plant growth-promoting Streptomyces sp. on plant growth and yield of tomato and chilli. Andhra Pradesh J Agric Sci 6(2):65–70. http://oar.icrisat.org/id/eprint/11668
Srinivas V, Naresh, Pratyusha S, Ankati S, Govindaraj M, Gopalakrishnan S (2022) Enhancing pearl millet hybrids performance for yield and nutrients through plant growth-promoting Streptomyces spp.: an agronomic biofortification approach. Crop Pasture Sci 73(5):484‒493. https://doi.org/10.1071/CP21438
Swamy MK, Akhtar MS, Sinniah UR (2016) Response of PGPR and Am fungi toward growth and secondary metabolite production in medicinal and aromatic plants. In: Plant soil and microbes. Springer, Cham, Switzerland; pp 145‒168. https://doi.org/10.1007/978-3-319-29573-2_19
Tan HM, Cao LX, He ZF, Su GJ, Lin B, Zhou SN (2006) Isolation of endophytic actinomycetes from different cultivars of tomato and their activities against Ralstonia solanacearum in vitro. World J Microbiol Biotechnol 22:1275–1280. https://doi.org/10.1007/s11274-006-9172-y
Vijayabharathi R, Gopalakrishnan S, Sathya A, Kumar MV, Srinivas V, Sharma M (2018) Deciphering the tri-dimensional effect of endophytic Streptomyces sp. on chickpea for plant growth promotion, helper effect with Mesorhizobium ciceri on nodulation and host-plant resistance induction against Botrytis cinerea. Microb Pathog 122:98–107. https://doi.org/10.1080/09583157.2018.1515890
Acknowledgements
This work has been undertaken as part of the CGIAR Research Program on Grain Legumes and Dry Land Cereals.
Funding
No funding available.
Author information
Authors and Affiliations
Contributions
SG and SS designed, supervised and finalized the experiments; VS and UC completed the experiments; SG wrote the original draft and SP, VS, UC and SS reviewed and finalized the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All the authors state that there is no conflict of interest.
Ethical approval
This manuscript does not contain any experiments involving human or animal participants.
Consent to participate
The authors declare consent to participate in this work.
Consent for publication
The authors declare consent to publish this work.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gopalakrishnan, S., Srinivas, V., Chand, U. et al. Streptomyces consortia-mediated plant growth-promotion and yield performance in chickpea. 3 Biotech 12, 318 (2022). https://doi.org/10.1007/s13205-022-03389-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-022-03389-8
Keywords
- Streptomyces
- Consortia
- Plant growth promotion
- Chickpea
- Soil health