Exploring plant growth-promoting Streptomyces spp. for yield and nutrition traits in pearl millet hybrids
Vadlamudi Srinivas A , Nimmala Naresh A , Sambangi Pratyusha A , Sravani Ankati A , Mahalingam Govindaraj
A * and Subramaniam Gopalakrishnan A *
+ Author Affiliations
- Author Affiliations
A International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru 502324, Telangana, India.
* Correspondence to: s.gopalakrishnan@cgiar.org, m.govindaraj@cgiar.org
Handling Editor: Shahid Hussain
Crop & Pasture Science 73(5) 484-493 https://doi.org/10.1071/CP21438
Submitted: 23 June 2021 Accepted: 27 September 2021 Published: 14 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The present study aimed to demonstrate the use of two strains of Streptomyces albus (CAI-24 and KAI-27) and one strain of S. griseus (MMA-32) for plant growth-promotion (PGP) and improving pearl millet yield and nutrient content under greenhouse and field conditions. Two hybrids, a low-Fe (PA-9444; non-biofortified hybrid) and high-Fe (ICMH-1201; biofortified hybrid), treated with selected Streptomyces strains, significantly enhanced a range of traits including grain yield in the glasshouse (13–23%) and field (9–12%) over the control. In the greenhouse experiments an enhanced stover and grain nutrient concentrations were observed in ICMH-1201 (Fe 53% and 40%; Zn 15% and 10%; Ca 11% and 29%) over the control, while such nutrition augmentations were not found in PA-9444. The field harvested stover and grain nutrient concentrations were also increased over the control in both hybrids. A higher stover nutrient concentration was found in ICMH-1201 while PA-9444 had an increase in grain nutrient concentration indicating the significance of these Streptomyces strains’ PGP role in the non-biofortified hybrid. Based on this study, strains KAI-27 and MMA-32 significantly improved shoot weight, root weight and grain yield while CAI-24 and MMA-32 improved nutrient concentrations including Fe contents (up to 49%) in grain as well as in stover. Further, the stover samples of pearl millet contained a higher Fe concentration (150–200%) compared to grain samples. This study confirms that the selected Streptomyces strains have the potential for enhancing PGP and stover and grain nutrient concentrations in pearl millet and can complement the existing conventional biofortification strategies.
Keywords: beneficial bacteria, biofortification, iron, nutrition, pearl millet, PGP, PGP microbes, Streptomyces.
References
Ankati S, Srinivas V, Pratyusha S, Gopalakrishnan S (2021) Streptomyces consortia-mediated plant defense against Fusarium wilt and plant growth-promotion in chickpea. Microbial Pathogenesis 157, 104961| Streptomyces consortia-mediated plant defense against Fusarium wilt and plant growth-promotion in chickpea.Crossref | GoogleScholarGoogle Scholar | 34033892PubMed |
Directorate of Millets Development (2020) ‘Department of Agriculture, Co-operation & Farmers’ Welfare Ministry of Agriculture and Farmers’ Welfare, Government of India’. (Directorate of Millets Development)
Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, Vidya MS, Deepthi K, Rupela O (2011a) Evaluation of actinomycete isolates obtained from herbal vermicompost for biological control of Fusarium wilt of chickpea. Crop Protection 30, 1070–1078.
| Evaluation of actinomycete isolates obtained from herbal vermicompost for biological control of Fusarium wilt of chickpea.Crossref | GoogleScholarGoogle Scholar |
Gopalakrishnan S, Kiran BK, Humayun P, Vidya MS, Deepthi K, Jacob S, Vadlamudi S, Alekhya G, Rupela O (2011b) Biocontrol of charcoal-rot of sorghum by actinomycetes isolated from herbal vermicompost. African Journal of Biotechnology 10, 18142–18152.
| Biocontrol of charcoal-rot of sorghum by actinomycetes isolated from herbal vermicompost.Crossref | GoogleScholarGoogle Scholar |
Gopalakrishnan S, Humayun P, Vadlamudi S, Vijayabharathi R, Bhimineni RK, Rupela O (2012) Plant growth-promoting traits of Streptomyces with biocontrol potential isolated from herbal vermicompost. Biocontrol Science and Technology 22, 1199–1210.
| Plant growth-promoting traits of Streptomyces with biocontrol potential isolated from herbal vermicompost.Crossref | GoogleScholarGoogle Scholar |
Gopalakrishnan S, Srinivas V, Vidya MS, Rathore A (2013a) Plant growth-promoting activities of Streptomyces spp. in sorghum and rice. SpringerPlus 2, 574
| Plant growth-promoting activities of Streptomyces spp. in sorghum and rice.Crossref | GoogleScholarGoogle Scholar | 24255867PubMed |
Gopalakrishnan S, Vadlamudi S, Apparla S, Bandikinda P, Vijayabharathi R, Bhimineni RK, Rupela O (2013b) Evaluation of Streptomyces spp. for their plant growth-promoting traits in rice. Canadian Journal of Microbiology 59, 534–539.
| Evaluation of Streptomyces spp. for their plant growth-promoting traits in rice.Crossref | GoogleScholarGoogle Scholar | 23898996PubMed |
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
| The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea.Crossref | GoogleScholarGoogle Scholar | 25646153PubMed |
Gopalakrishnan S, Vadlamudi S, 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.). The Philippine Agricultural Scientist 98, 270–278.
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Varshney RK (2015c) Evaluation of Streptomyces sp. obtained from herbal vermicompost for broad spectrum of plant growth-promoting activities in chickpea. Organic Agriculture 5, 123–133.
| Evaluation of Streptomyces sp. obtained from herbal vermicompost for broad spectrum of plant growth-promoting activities in chickpea.Crossref | GoogleScholarGoogle Scholar |
Gopalakrishnan S, Vadlamudi S, Samineni S, Sameer Kumar CV (2016a) Plant growth-promotion and biofortification of chickpea and pigeonpea through inoculation of biocontrol potential bacteria, isolated from organic soils. SpringerPlus 5, 1882
| Plant growth-promotion and biofortification of chickpea and pigeonpea through inoculation of biocontrol potential bacteria, isolated from organic soils.Crossref | GoogleScholarGoogle Scholar | 27833841PubMed |
Gopalakrishnan S, Srinivas V, Sameer Kumar CV (2016b) Plant growth-promotion traits of Streptomyces sp. in pigeonpea. Legume Perspectives 11, 43–44. http://ils.nsseme.com/assets/LegumPerspect11.pdf
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
| Identification and characterization of a Streptomyces albus strain and its secondary metabolite organophosphate against charcoal rot of sorghum.Crossref | GoogleScholarGoogle Scholar |
Gopalakrishnan S, Srinivas V, Prasanna SL (2020b) Streptomyces. In ‘Beneficial microbes in agro-ecology: bacteria and fungi’. (Eds N Amaresan, K Annapurna, A Sankaranarayanan, M Senthil Kumar, K Kumar) pp. 55–71. (Academic Press Inc.)
| Crossref |
Gopalakrishnan S, Srinivas V, Naresh N, Pratyusha S, Ankati 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
| Deciphering the antagonistic effect of Streptomyces spp. and host-plant resistance induction against charcoal rot of sorghum.Crossref | GoogleScholarGoogle Scholar | 33532924PubMed |
Govindaraj M, Rai KN, Cherian B, Pfeiffer WH, Kanatti A, Shivade H (2019) Breeding biofortified pearl millet varieties and hybrids to enhance millet markets for human nutrition. Agriculture 9, 106
| Breeding biofortified pearl millet varieties and hybrids to enhance millet markets for human nutrition.Crossref | GoogleScholarGoogle Scholar |
Govindaraj M, Yadav OP, Rajpurohit BS, Kanatti A, Rai KN, Dwivedi SL (2020) Genetic variability, diversity and interrelationship for twelve grain minerals in 122 commercial pearl millet cultivars in India. Agricultural Research 9, 516–525.
| Genetic variability, diversity and interrelationship for twelve grain minerals in 122 commercial pearl millet cultivars in India.Crossref | GoogleScholarGoogle Scholar |
Hamdali H, Bouizgarne B, Hafidi M, Lebrihi A, Virolle MJ, Ouhdouch Y (2008) Screening for rock phosphate solubilizing actinomycetes from moroccan phosphate mines. Applied Soil Ecology 38, 12–19.
| Screening for rock phosphate solubilizing actinomycetes from moroccan phosphate mines.Crossref | GoogleScholarGoogle Scholar |
Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160, 778–788.
| Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth.Crossref | GoogleScholarGoogle Scholar | 24430493PubMed |
Jog R, Nareshkumar G, Rajkumar S (2016) Enhancing soil health and plant growth promotion by actinomycetes. In ‘Plant growth promoting actinobacteria’. (Eds S Gopalakrishnan, A Sathya, R Vijayabharathi) pp. 33–45. (Springer: Singapore)
| Crossref |
Kaur T, Rana KL, Kour D, Sheikha I, Yadav N, Kumar V, Yadav AN, Dhaliwal HS, Saxena AK (2020) Microbe-mediated biofortification for micronutrients: present status and future challenges. In ‘New and future developments in microbial biotechnology and bioengineering’. (Eds AA Rastegari, AN Yadav, N Yadav) pp. 1–17. (Elsevier Inc.)
| Crossref |
Khamna S, Yokota A, Lumyoung S (2009) Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World Journal of Microbiology and Biotechnology 25, 649–655.
| Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production.Crossref | GoogleScholarGoogle Scholar |
Khamna S, Yokota A, Peberdy JF, Lumyong S (2010) Indole-3-acetic acid production by Streptomyces sp. isolated from some Thai medicinal plant rhizosphere soils. EurAsian Journal of BioSciences 4, 23–32.
| Indole-3-acetic acid production by Streptomyces sp. isolated from some Thai medicinal plant rhizosphere soils.Crossref | GoogleScholarGoogle Scholar |
Kumar A, Choudhary AK, Pooniya V, Suri VK, Singh U (2016) Soil factors associated with micronutrient acquisition in crops-biofortification perspective. In ‘Biofortification of food crops’. (Eds U Singh, CS Praharaj, SS Singh, NP Singh) pp. 159–176. (Springer India)
| Crossref |
Nosheen S, Ajmal I, Song Y (2021) Microbes as biofertilizers, a potential approach for sustainable crop production. Sustainability 13, 1868
| Microbes as biofertilizers, a potential approach for sustainable crop production.Crossref | GoogleScholarGoogle Scholar |
Panhwar QA, Othman R, Rahman ZA, Meon S, Ismail MR (2012) Isolation and characterization of phosphate-solubilizing bacteria from aerobic rice. African Journal of Biotechnology 11, 2711–2719.
| Isolation and characterization of phosphate-solubilizing bacteria from aerobic rice.Crossref | GoogleScholarGoogle Scholar |
Prasanna R, Nain L, Rana A, Shivay YS (2016) Biofortification with microorganisms: present status and future challenges. In ‘Biofortification of food crops’. (Eds U Singh, CS Praharaj, SS Singh, NP Singh) pp. 249–262.
| Crossref |
Rana A, Kabi SR, Verma S, Adak A, Pal M, Shivay YS, Prasanna R, Nain L (2015) Prospecting plant growth promoting bacteria and cyanobacteria as options for enrichment of macro and micronutrients in grains in rice–wheat cropping sequence. Cogent Food & Agriculture 1, 1037379
| Prospecting plant growth promoting bacteria and cyanobacteria as options for enrichment of macro and micronutrients in grains in rice–wheat cropping sequence.Crossref | GoogleScholarGoogle Scholar |
Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World Journal of Microbiology and Biotechnology 28, 1503–1509.
| Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions.Crossref | GoogleScholarGoogle Scholar | 22805932PubMed |
Saleem M, Law AD, Moe LA (2016) Nicotiana roots recruit rare rhizosphere taxa as major root-inhabiting microbes. Microbial Ecology 71, 469–472.
| Nicotiana roots recruit rare rhizosphere taxa as major root-inhabiting microbes.Crossref | GoogleScholarGoogle Scholar | 26391804PubMed |
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
| Plant growth-promoting actinobacteria on chickpea seed mineral density: an upcoming complementary tool for sustainable biofortification strategy.Crossref | GoogleScholarGoogle Scholar | 28330210PubMed |
Singh D, Geat N, Rajawat MVS, Prasanna R, Kar A, Singh AM, Saxena AK (2018) Prospecting endophytes from different Fe or Zn accumulating wheat genotypes for their influence as inoculants on plant growth, yield, and micronutrient content. Annals of Microbiology 68, 815–833.
| Prospecting endophytes from different Fe or Zn accumulating wheat genotypes for their influence as inoculants on plant growth, yield, and micronutrient content.Crossref | GoogleScholarGoogle Scholar |
Sousa CS, Soares ACF, Garrido MS (2008) Characterization of Streptomyces with potential to promote plant growth and biocontrol. Scientia Agricola 65, 50–55.
| Characterization of Streptomyces with potential to promote plant growth and biocontrol.Crossref | GoogleScholarGoogle Scholar |
Sreevidya M, Gopalakrishnan S, Kudapa H, Varshney RK (2016) Exploring plant growth-promotion actinomycetes from vermicompost and rhizosphere soil for yield enhancement in chickpea. Brazilian Journal of Microbiology 47, 85–95.
| Exploring plant growth-promotion actinomycetes from vermicompost and rhizosphere soil for yield enhancement in chickpea.Crossref | GoogleScholarGoogle Scholar | 26887230PubMed |
Subramaniam G, Thakur V, Saxena RK, Vadlamudi S, Purohit S, Kumar V, Rathore A, Chitikineni A, Varshney RK (2020) Complete genome sequence of sixteen plant growth promoting Streptomyces strains. Scientific Reports 10, 10294
| Complete genome sequence of sixteen plant growth promoting Streptomyces strains.Crossref | GoogleScholarGoogle Scholar | 32581303PubMed |
Tukey JW (1977) ‘Exploratory data analysis’, (Addison-Weeley Publishing Company: Reading, MA, CA)
Vijayabharathi R, Gopalakrishnan S, Sathya A, 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 and host-plant resistance induction against Botrytis cinerea. Microbial Pathogenesis 122, 98–107.
| Deciphering the tri-dimensional effect of endophytic Streptomyces sp. on chickpea for plant growth promotion, helper effect with Mesorhizobium ciceri and host-plant resistance induction against Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 29894808PubMed |
Wakeel A, Farooq M, Bashir K, Ozturk L (2018) Micronutrient malnutrition and biofortification: recent advances and future perspectives. In ‘Plant micronutrient use efficiency’. (Eds MA Hossain, T Kamiya, DJ Burritt, L-SP Tran, T Fujiwara) pp. 225–243. (Academic Press: London, UK)
| Crossref |
WHO (2020) Children: reducing mortality. Available at https://www.who.int/en/news-room/fact-sheets/detail/children-reducing-mortality. [Accessed 8 September 2020]
Yadav OP, Rai KN (2013) Genetic improvement of pearl millet in India. Agricultural Research 2, 275–292.
| Genetic improvement of pearl millet in India.Crossref | GoogleScholarGoogle Scholar |
Yadav AN, Rastegari AA, Yadav N, Kour D (Eds) (2020a) ‘Advances in plant microbiome and sustainable agriculture: functional annotation and future challenges’. Vol. 2. (Springer: Singapore)
| Crossref |
Yadav AN, Singh J, Rastegari AA, Yadav N (Eds) (2020b) ‘Plant microbiomes for sustainable agriculture’, (Springer International Publishing: Cham, Switzerland)
Yasin M, El-Mehdawi AF, Anwar A, Pilon-Smits EAH, Faisal M (2015) Microbial enhanced selenium and iron biofortification of wheat (Triticum aestivum L.) - applications in phytoremediation and biofortification. International Journal of Phytoremediation 17, 341–347.
| Microbial enhanced selenium and iron biofortification of wheat (Triticum aestivum L.) - applications in phytoremediation and biofortification.Crossref | GoogleScholarGoogle Scholar | 25409246PubMed |
