Skip to main content
Log in

Tailoring the rhizospheric microbiome of Vigna radiata by adaptation to salt stress

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Sustainable management practices are the need of the hour to counter the ever-deteriorating environmental conditions in agro-ecosystems. While bioinoculants have served as eco-friendly means to mitigate stresses, their survivability and competitiveness in field conditions have been a major challenge. The present study aimed to adopt a multi-generational approach to adapt the rhizospheric microbiome of Vigna radiata, a legume consumed worldwide, under salt stress. A multi-generational plant growth experiment was set-up with induced salinity stress, employing the rhizosphere of best-performing plants from the preceding generation as inoculum for the next generation. The plant health and mitigation of salinity stress by the adapted microbiome was analyzed using plant biometrics, bacterial diversity, and stress markers. Decreased levels of salt-induced stress markers, and simultaneous improvement in plant attributes were observed with the progression of the generations. The shifts in bacterial community were prominent upon inoculation of the adapted microbiome. The treatments with the adapted microbiome in the presence of salinity stress were closer to the control sets compared to salinity-stressed treatments, indicating the efficiency of the adapted microbiome towards mitigation of salinity stress. The study demonstrates the promising potential of such an eco-friendly, microbiome-based approach for plant growth promotion and mitigation of salinity stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods in enzymology. Academic Press, Cambridge, pp 121–126

    Google Scholar 

  • Agrawal AA, Johnson MT, Hastings AP, Maron JL (2013) A field experiment demonstrating plant life-history evolution and its eco-evolutionary feedback to seed predator populations. Am Nat 181:35–45

    Article  Google Scholar 

  • Ahmed S (2009) Effect of soil salinity on the yield and yield components of mungbean. Pak J Bot 41:263–268

    Google Scholar 

  • Alharby HF, Al-Zahrani HS, Hakeem KR, Iqbal M (2018) Identification of physiological and biochemical markers for salt (NaCl) stress in the seedlings of mungbean [Vigna radiata (L.) Wilczek] genotypes. Saudi J Biol Sci 26:633–872

    Google Scholar 

  • Andreae WA, Van Ysselstein MW (1960) Studies on 3-indoleacetic acid metabolism. VI. 3-Indoleacetic acid uptake and metabolism by pea roots and epicotyls. Plant Physiol 35:225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arias-Sánchez FI, Vessman B, Mitri S (2019) Artificially selecting microbial communities: if we can breed dogs, why not microbiomes? PLoS Biol 17:e3000356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arnon DI (1948) Localization of polyphenol oxidase in the chloroplasts of Beta vulgaris. Nature 162:341–342

    Article  CAS  PubMed  Google Scholar 

  • Arora NK, Singhal V, Maheshwari DK (2006) Salinity-induced accumulation of poly-β-hydroxybutyrate in Rhizobia indicating its role in cell protection. World J Microbiol Biotechnol 22:603–606

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bouskill NJ, Lim HC, Borglin S, Salve R, Wood TE, Silver WL (2013) Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J 7:384–394

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Mitra S, Paul A (2015) Physiochemical studies of sodium chloride on mungbean (Vigna radiata L. Wilczek) and its possible recovery with spermine and gibberellic acid. Sci World J 2015:8

    Article  Google Scholar 

  • Goicoechea N, Merino S, Sánchez-Díaz M (2005) Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules of Anthyllis cytisoides L. subjected to drought. J Plant Physiol 162:27–35

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Heuer H, Smalla K (1997) Application of denaturing gradient gel electrophoresis for studying soil microbial communities. In: van Elsas JD, Trevors JT, Wellington EMH (eds) Modern soil microbiology. Marcel Dekker Inc., New York, pp 353–373

    Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hussain S, Zhu C, Huang J et al (2020) Ethylene response of salt stressed rice seedlings following Ethephon and 1-methylcyclopropene seed priming. Plant Growth Regul. https://doi.org/10.1007/s10725-020-00632-1

    Article  Google Scholar 

  • Irigoyen JJ, Einerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60

    Article  CAS  Google Scholar 

  • Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458

    Article  Google Scholar 

  • Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189–195

    Article  CAS  PubMed  Google Scholar 

  • Kumar AS, Kunju, A (2014) Rhizosphere engineering for improving productivity and quality constituents in Asparagus racemosus (September 9, 2014). Available at SSRN 1-13. https://ssrn.com/abstract=2493622 or https://doi.org/10.2139/ssrn.2493622

  • McCue KF, Hanson AD (1990) Drought and salt tolerance, towards understanding and application. Trends Biotechnol 8:358–362

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Morella NM, Weng FC, Joubert PM, Metcalf CJ, Lindow S, Koskella B (2020) Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. Proc Natl Acad Sci USA 117:1148–1159

    Article  CAS  PubMed  Google Scholar 

  • Morrissey EM, Gillespie JL, Morina JC, Franklin RB (2014) Salinity affects microbial activity and soil organic matter content in tidal wetlands. Glob Change Biol 20:1351–1362

    Article  Google Scholar 

  • Mueller UG, Juenger T, Kardish M, Carlson A, Burns K, Smith C, De Marais D (2016) Artificial microbiome-selection to engineer microbiomes that confer salt-tolerance to plants. bioRxiv. 081521

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Naylor D, Coleman-Derr D (2018) Drought stress and root-associated bacterial communities. Front Plant Sci 8:2223

    Article  PubMed  PubMed Central  Google Scholar 

  • Niether W, Glawe A, Pfohl K et al (2020) The effect of short-term vs. long-term soil moisture stress on the physiological response of three cocoa (Theobroma cacao L.) cultivars. Plant Growth Regul. https://doi.org/10.1007/s10725-020-00638-9

    Article  Google Scholar 

  • Panke-Buisse A, Poole C, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9:980–989

    Article  CAS  PubMed  Google Scholar 

  • Pütter J (1974) Peroxidases. In: Methods of enzymatic analysis. Academic Press, Cambridge, pp 685–690

    Chapter  Google Scholar 

  • Quiza L, St-Arnaud M, Yergeau E (2015) Harnessing phyto-microbiome signaling for rhizosphere microbiome engineering. Front Plant Sci 6:1–30

    Article  Google Scholar 

  • Rietz DN, Haynes RJ (2003) Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol Biochem 35:845–854

    Article  CAS  Google Scholar 

  • Sarkar A, Pramanik K, Mitra S, Soren T, Maiti TK (2018) Enhancement of growth and salt tolerance of rice seedlings by ACC deaminase producing Burkholderia sp. MTCC 12259. J Plant Physiol 231:434–442

    Article  CAS  PubMed  Google Scholar 

  • Sehrawat N, Bhat KV, Sairam RK, Jaiwal PK (2013) Identification of salt resistant wild relatives of mungbean (Vigna radiata L. Wilczek). Asian J Plant Sci Res 3:41–49

    Google Scholar 

  • Sharma S, Mehta R, Gupta R, Schloter M (2012) Improved protocol for the extraction of bacterial mRNA from soils. J Microbiol Methods 91:62–64

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Jha PN (2016a) The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat (Triticum aestivum L.). PLoS ONE 11:e0155026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singh RP, Jha PN (2016b) Mitigation of salt stress in wheat plant (Triticum aestivum) by ACC deaminase bacterium Enterobacter sp. SBP-6 isolated from Sorghum bicolor. Acta Physiol Plant 38:110

    Article  CAS  Google Scholar 

  • Swenson W, Wilson DS, Elias R (2000) Artificial ecosystem selection. PNAS 97:9110–9114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trexler RV, Bell TH (2019) Testing sustained soil-to-soil contact as an approach for limiting the abiotic influence of source soils during experimental microbiome transfer. FEMS Microbiol Lett 366:fnz228

    Article  CAS  PubMed  Google Scholar 

  • Tripepi RR, George MW (1991) Identification of bacteria infecting seedlings of mungbean used in rooting bioassays. J Am Soc Hortic Sci 116:80–84

    Article  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Wang C, Zhu S et al (2020) Characterizing the metabolites related to rice salt tolerance with introgression lines exhibiting contrasting performances in response to saline conditions. Plant Growth Regul. https://doi.org/10.1007/s10725-020-00627-y

    Article  Google Scholar 

  • Yan N, Marschner P, Cao W, Zuo C, Qin W (2015) Influence of salinity and water content on soil microorganisms. Int Soil Water Conserv Res 3:316–323

    Article  Google Scholar 

  • Yong M, Solis CA, Rabbi B et al (2020) Leaf mesophyll K+ and Cl- fluxes and reactive oxygen species production predict rice salt tolerance at reproductive stage in greenhouse and field conditions. Plant Growth Regul 92:53–64

    Article  CAS  Google Scholar 

  • Yuan Z, Druzhinina IS, Labbé J, Redman R, Qin Y, Rodriguez R, Lin F (2016) Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci Rep 6:32467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors VG, GA, and SD acknowledge Indian Institute of Technology Delhi for their fellowship.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

Authors

Contributions

VG, SS: Conceptualization and Methodology, VG, GA, SD: Experimentation. All authors contributed towards analysis of data, drafting of manuscript and revising it, and finally all approve it for submission.

Corresponding author

Correspondence to Shilpi Sharma.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1114 kb)

Supplementary file2 (PDF 231 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Anand, G., Goel, V., Dubey, S. et al. Tailoring the rhizospheric microbiome of Vigna radiata by adaptation to salt stress. Plant Growth Regul 93, 79–88 (2021). https://doi.org/10.1007/s10725-020-00667-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-020-00667-4

Keywords

Navigation