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Amelioration effect of salt-tolerant plant growth-promoting bacteria on growth and physiological properties of rice (Oryza sativa) under salt-stressed conditions

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Abstract

For sustainable agriculture in saline soil, extensive exploitation of salt-tolerant plant growth-promoting (PGP) bacteria and other symbiotic bacteria is required. This study was carried out to evaluate the efficiency of native salt-tolerant rice rhizobacteria for plant growth promotion under salt stress. A total of 188 bacteria were screened for assessing salt-tolerant capacity and nine isolates tolerating 12% NaCl (w/v) concentration were selected. Biochemical and molecular identification revealed that the salt-tolerant bacteria belonged to Bacillus sp, Exiguobacterium sp, Enterobacter sp, Lysinibacillus sp, Stenotrophomonas sp, Microbacterium sp, and Achromobacter sp. The increase in NaCl concentration from 2 to 4% decreases the PGP activities such as IAA production, P solubilization, K solubilization, and nitrate reduction. The effects of inoculation of salt-tolerant bacteria on the growth and different physiological properties of rice (Oryza sativa) were studied. It was found that the salinity affected the root and shoot length of the control plants; however, bacterial inoculant were found to effectively promote the growth of paddy under salinity stress. Further, bacterial inoculants substantially enhanced total chlorophyll, proline, total phenol, and oxidative damage such as electrolyte leakage and membrane stability index under salt stress. This study suggests that salt-tolerant PGP bacteria may be used for cultivation of O. sativa in salinized agricultural lands.

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References

  • Ali MN, Ghosh B, Gantait S, Chakraborty S (2014) Selection of rice genotypes for salinity tolerance through morpho-biochemical assessment. Rice Sci 21:288–298

    Google Scholar 

  • Altschul SF, Maddan TL, Schaffer AA, Zang J, Zang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programmes. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Amaresan N, Kumar K, Madhuri K, Usharani GK (2016) Isolation and characterization of salt tolerant plant growth promoting rhizobacteria from plants grown in Tsunami affected regions of Andaman and Nicobar Islands. Geomicrobiol J 33:942–947

    CAS  Google Scholar 

  • Ansari M, Shekari F, Mohammadi MH, Juhos K, Végvári G, Biró B (2019) Salt-tolerant plant growth-promoting bacteria enhanced salinity tolerance of salt-tolerant alfalfa (Medicago sativa L) cultivars at high salinity. Acta Physiol Plant 41:195

    CAS  Google Scholar 

  • Asch F, Wopereis MCS (2001) Responses of field-grown irrigated rice cultivars to varying levels of floodwater salinity in a semi-arid environment. Field Crops Res 70:127–137

    Google Scholar 

  • Barnawal D, Bharti N, Maji D, Chanotiya CS, Kalra A (2014) ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum. J Plant Physiol 171:884–894

    CAS  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Brick JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Appl Environ Microbiol 57:535–538

    Google Scholar 

  • Dastager SG, Pandey A, Lee JC, Li WJ, Kim CJ (2009) Polyphasic taxonomy of novel actinobacteria showing macromolecule degradation potentials in Bigeum Island, Korea. Curr Microbiol 59:21–29

    CAS  PubMed  Google Scholar 

  • Egamberdieva D, Wirth S, Bellingrath-Kimura SD, Mishra J, Arora NK (2019) Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Front Microbiol 10:2791

    PubMed  PubMed Central  Google Scholar 

  • Farhangi-Abriz S, Tavasolee A, Ghassemi-Golezani K, Torabian S, Monirifar H, Rahmani HA (2020) Growth-promoting bacteria and natural regulators mitigate salt toxicity and improve rapeseed plant performance. Protoplasma. https://doi.org/10.1007/s00709-020-01493-1

    Article  PubMed  Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    CAS  Google Scholar 

  • Grattan SR, Linghe L, Shannon MC, Roberts SR (2002) Rice is more sensitive to salinity than previously thought. Calif Agric 56:189–198

    Google Scholar 

  • Grover M, Ali Sk Z, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240

    Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598

    Google Scholar 

  • Hu X, Chen J, Guo J (2006) Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22:983–990

    CAS  Google Scholar 

  • Jackson ML (1973) Soil chemical analysis. Prentice Hall of India (P) Ltd, New Delhi

    Google Scholar 

  • Kammoun R, Naili B, Bejar S (2008) Application of statistical design to the optimization of parameters and culture medium for -amylase production by Aspergillus oryzae CBS 819.72 grown on gruel (wheat grinding by product). Biores Technol 99:5602–5609

    CAS  Google Scholar 

  • Kang S, Radhakrishnan R, Khan AL, Kim M, Park J, Kim B, Shin D, Lee I (2014) Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 84:115–124

    CAS  PubMed  Google Scholar 

  • Karagöz K, Ateş F, Karagöz H, Kotan R, Çakmakç R (2012) Characterization of plant growth-promoting traits of bacteria isolated from the rhizosphere of grapevine grown in alkaline and acidic soils. Eur J Soil Biol 50:144–150

    Google Scholar 

  • Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A (2008) A rapid and easy method for the detection of microbial cellulases on agar plates using grams iodine. Curr Microbiol 57:503–507

    CAS  PubMed  Google Scholar 

  • Kotuby AJ, Koenig R, Kitchen B (2000) Salinity and plant tolerance. All Archived Publications. Paper 43

  • Kudoyarova GR, Melentiev AI, Martynenko EV, Timergalina LN, Arkhipova TN, Shendel GV, Kuz'mina LY, Dodd IC, Veselov SY (2014) Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiol Biochem 83:285–291

    CAS  PubMed  Google Scholar 

  • Kumar K, Manigundan K, Amaresan N (2017) Influence of salt tolerant Trichoderma spp. on growth of maize (Zea mays) under different salinity conditions. J Basic Microbiol 57:141–150

    CAS  PubMed  Google Scholar 

  • Kumazawa S, Hamasaka T, Nakayama T (2004) Antioxidant activity of propolis of various geographic origins. Food Chem 84:329–339

    CAS  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    CAS  Google Scholar 

  • Maheshwari DK, Dubey RC, Aeron A, Kumar B, Kumar S, Tewari S, Arora NK (2012) Integrated approach for disease management and growth enhancement of Sesamum indicum L. utilizing Azotobacter chroococcum TRA2 and chemical fertilizer. World J Microbiol Biotechnol 28:3015–3024

    CAS  PubMed  Google Scholar 

  • Mahmood S, Daur I, Al-Solaimani SG, Ahmad S, Madkour MH, Yasir M, Hirt H, Ali S, Ali Z (2016) Plant growth promoting rhizobacteria and silicon synergistically enhance salinity tolerance of mung bean. Front Plant Sci 7:876

    PubMed  PubMed Central  Google Scholar 

  • Mark T, Romola D (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Google Scholar 

  • Nadeem SM, Ahmad ZZ, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149

    CAS  PubMed  Google Scholar 

  • Osman JR, Fernandes G, DuBow MS (2017) Bacterial diversity of the rhizosphere and nearby surface soil of rice (Oryza sativa) growing in the Camargue (France). Rhizosphere 3:112–122

    Google Scholar 

  • Pierzynski GM, Sims JT, Vance GF (2005) Soils and environmental quality, 3rd edn. CRC Press Taylor & Francis Group, Florida

    Google Scholar 

  • Pikovaskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Microbiology 17:363–370

    Google Scholar 

  • Qi W, Zhao L (2013) Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol 53:355–364

    CAS  PubMed  Google Scholar 

  • Rana M, Mark T (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Google Scholar 

  • Roychoudhury A, Basu S (2008) Overexpression of an abiotic-stress inducible plant protein in the bacteria Escherichia coli. Afr J Biotechnol 7:3231–3234

    CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Ann Biochem 160:47–56

    CAS  Google Scholar 

  • Sharma A, Singh P, Kumar S, Kashyap P, Srivastava AK, Chakdar H, Singh R, Kaushik R, Saxena AK, Sharma AK (2015) Deciphering diversity of salt-tolerant bacilli from saline soils of Eastern Indo-gangetic plains of India. Geomicrobiol J 32:170–180

    CAS  Google Scholar 

  • Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol 7:1600

    PubMed  PubMed Central  Google Scholar 

  • Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131

    CAS  PubMed  Google Scholar 

  • Singh RP, Jha P, Jha PN (2017) Bio-inoculation of plant growth-promoting rhizobacterium Enterobacter cloacae ZNP-3 increased resistance against salt and temperature stresses in wheat plant (Triticum aestivum L.). J Plant Growth Regul 36:783–798

    CAS  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhard PRGE, Wood MWA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607–655

    Google Scholar 

  • Sohaiba M, Zahir ZA, Khan MY, Ans M, Asghar HN, Yasin S, Al-Barakah FNI (2020) Comparative evaluation of different carrier-based multi-strain bacterial formulations to mitigate the salt stress in wheat. Saudi J Biol Sci 27:777–787

    Google Scholar 

  • Turan V (2019) Confident performance of chitosan and pistachio shell biochar on reducing Ni bioavailability in soil and plant plus improved the soil enzymatic activities, antioxidant defense system and nutritional quality of lettuce. Ecotoxicol Environ Saf 183:109594

    CAS  PubMed  Google Scholar 

  • Turan V, Schröder P, Bilen S, Insam H, Fernández-Delgado Juárez M (2019) Co-inoculation effect of Rhizobium and Achillea millefolium L. oil extracts on growth of common bean (Phaseolus vulgaris L.) and soil microbial-chemical properties. Sci Rep 9:15178

    PubMed  PubMed Central  Google Scholar 

  • Viraktamath B, Bentur J, Rao K, Sain M (2011) Vision 2030. Directorate of rice research, Hyderabad, pp 1–32

    Google Scholar 

  • Yang G, Rhodes D, Joly RJ (1996) Effect of high temperature on membrane stability and chlorophyll fluorescence in glycine betaine-containing maize lines. Aust J Plant Physiol 23:431–443

    Google Scholar 

Download references

Acknowledgements

The authors thank UTU management and Director, CGBIBT, for constant support and providing necessary facilities to carry out the work. The authors also thank GSBTM for 16S rRNA gene sequencing and Mahuva Sugar Factory, Mahuva, for physicochemical studies.

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Correspondence to Natarajan Amaresan.

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Communicated by Erko Stackebrandt.

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Prittesh, P., Avnika, P., Kinjal, P. et al. Amelioration effect of salt-tolerant plant growth-promoting bacteria on growth and physiological properties of rice (Oryza sativa) under salt-stressed conditions. Arch Microbiol 202, 2419–2428 (2020). https://doi.org/10.1007/s00203-020-01962-4

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