Skip to main content

Advertisement

SpringerLink
Log in

Assessing the Plant Growth Promoting and Arsenic Tolerance Potential of Bradyrhizobium japonicum CB1809

  • Published:
Environmental Management Aims and scope Submit manuscript

Abstract

Accumulation of heavy metals in soil is of concern to the agricultural production sector, because of the potential threat to food quality and quantity. Inoculation with plant growth-promoting bacteria (PGPR) has previously been shown to alleviate heavy metal stress but the mechanisms are unclear. Potential mechanisms by which inoculation with Bradyrhizobium japonicum CB1809 affected the legume soybean (Glycine max cv. Zeus) and the non-legume sunflower (Helianthus annus cv. Hyoleic 41) were investigated in solution culture under 5 μM As stress. Adding As resulted in As tissue concentrations of up to 5 mg kg−1 (shoots) and 250 mg kg−1 (roots) in both species but did not reduce shoot or root biomass. Inoculation increased root biomass but only in the legume (soybean) and only with As. Inoculation resulted in large (up to 100%) increases in siderophore concentration but relatively small changes (±10–15%) in auxin concentration in the rhizosphere. However, the increase in siderophore concentration in the rhizosphere did not result in the expected increases in tissue N or Fe, especially in soybean, suggesting that their function was different. In conclusion, siderophores and auxins may be some of the mechanisms by which both soybean and sunflower maintained plant growth in As-contaminated media.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15010059

  • Ambrosini A, Beneduzi A, Stefanski T, Pinheiro FG, Vargas LK, Passaglia LMP (2012) Screening of plant growth promoting rhizobacteria isolated from sunflower (Helianthus annuus L.). Plant Soil 356:245–264. https://doi.org/10.1007/s11104-011-1079-1

    Article  CAS  Google Scholar 

  • Angle JS, McGrath SP, Chaudri AM, Chaney RL, Giller KE (1993) Inoculation effects on legumes grown in soil previously treated with sewage-sludge. Soil Biol Biochem 25:575–580

    Article  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67. https://doi.org/10.1023/a:1004326910584

    Article  CAS  Google Scholar 

  • Australian State of Environment Committee, Australia (2001) State of the environment independent report to the Commonwealth Minister for the Environment and Heritage. CSIRO Publ/Dept Environ Heritage, Canberra, p. 130

  • Bakker PA, Berendsen RL, Doornbos RF, Wintermans PC, Pieterse CM (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:165. https://doi.org/10.3389/fpls.2013.00165

    Article  Google Scholar 

  • Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051

    Article  CAS  Google Scholar 

  • Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001

    Article  CAS  Google Scholar 

  • Bianucci E, Godoyi A, Fulani A, Peralta J-M, Hernández LE, Carpena-Ruiz O, Castro S (2018) Arsenic toxicity in soybean alleviated by a symbiotic species of Bradyrhizobium. Symbiosis 74:167–176. https://doi.org/10.1007/s13199-017-0499-y

    Article  CAS  Google Scholar 

  • Cardon DL, Villafan SM, Tovar AR, Jimenez SP, Zuniga LAG, Allieri MAA, Perez NO, Dorantes AR (2010) Growth response and heavy metals tolerance of Axonopus affinis, inoculated with plant growth-promoting rhizobacteria. Afr J Biotechnol 9:8772–8782

    CAS  Google Scholar 

  • Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, Lopez R, Chamber MA, Palomares AJ (2005) Isolation and characterization of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Azanalcollar pyrite mine. Soil Biol Biochem 27:1131–1140

    Article  Google Scholar 

  • Finnegan P, Chen W (2012) Arsenic effects on plant metabolism. Front Physiol 3:182

    Article  CAS  Google Scholar 

  • Garcia-Fraile P, Carro L, Robledo M, Ramirez-Bahena MH, Flores-Felix JD, Fernandez MT, Mateos PF, Rivas R, Igual JM, Martinez-Molina E, Peix A, Velazquez E (2012) Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans PLoS ONE 7:e38122. https://doi.org/10.1371/journal.pone.0038122

    Article  CAS  Google Scholar 

  • Geetha SJ, Joshi SJ (2013) Engineering rhizobial bioinoculants: a strategy to improve iron nutrition. Sci World J 2013(article 315890):15

    Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339. https://doi.org/10.1007/s10658-007-9162-4

    Article  CAS  Google Scholar 

  • Glickmann E, Dessaux Y (1995) A critical-examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    Article  CAS  Google Scholar 

  • Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377. https://doi.org/10.1007/s13205-014-0241-x

    Article  Google Scholar 

  • Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK(2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture Microbiol Res 206:131–140. https://doi.org/10.1016/j.micres.2017.08.016

    Article  Google Scholar 

  • GRDC—Grains Research and Development Corporation (2016) Grownotes: Soybeans—Northern Region. GRDC. https://grdc.com.au/__data/assets/pdf_file/0035/364877/grdc-grownotes-soybeans-northern.pdf. Accessed 6 July 2020

  • Hinsinger P, Plassard C, Jaillard B (2006) Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 88:210–213

    Article  CAS  Google Scholar 

  • Kennedy IR, PeregGerk LL, Wood C, Deaker R, Gilchrist K, Katupitiya S (1997) Biological nitrogen fixation in non-leguminous field crops: facilitating the evolution of an effective association between Azospirillum and wheat. Plant Soil 194:65–79. https://doi.org/10.1023/a:1004260222528

    Article  CAS  Google Scholar 

  • Kloepper JW, Schroth MN, Leong J, Teintze M (1980) Enhanced plant-growth by siderophores produced by plant growth-promoting rhizobacteria. Abstracts Papers. Am Chem Soc 180:147

    Google Scholar 

  • Kopittke PM, Blamey FPC, Asher CJ, Menzies NW (2010) Trace metal phytotoxicity in solution culture: a review. J Exp Bot 61:945–954

    Article  CAS  Google Scholar 

  • Lafuente A, Pajuelo E, Caviedes MA, Rodriguez-Llorente ID (2010) Reduced nodulation in alfalfa induced by arsenic correlates with altered expression of early nodulins. Plant Physiol 167:286–291

    Article  CAS  Google Scholar 

  • Macur RE, Wheeler JT, McDermott TR, Inskeep WP (2001) Microbial populations associated with the reduction and enhanced mobilization of arsenic in mine tailings. Environ Sci Technol 35:3676–3682

    Article  CAS  Google Scholar 

  • Madejón P, Pérez-de-Mora A, Burgos P, Cabrera F, Lepp NW, Madejón E (2010) Do amended, polluted soils require re-treatment for sustainable risk reduction?—Evidence from field experiments. Geoderma 159:174–181

    Article  Google Scholar 

  • Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N (2015) Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Front Microbiol 6:198. https://doi.org/10.3389/fmicb.2015.00198

    Article  Google Scholar 

  • Malik H, Khan ZM, Mahmood Q, Nasreen S, Bhatti ZA (2009) Perspectives of low cost arsenic remediation of drinking water in Pakistan and other countries. J Hazard Mater 168:1–12

    Article  CAS  Google Scholar 

  • Mandal SM, Pati B, Das R, Amit K, Ghosh KA (2008) Characterization of a symbiotically effective Rhizobium resistant to arsenic: isolated from root nodules of Vigna mungo (L.) Hepper grown in arsenic-contaminated field. J Gen Appl Microbiol 54:93–99

    Article  CAS  Google Scholar 

  • Marroqui S, Zorreguieta A, Santamaria C, Temprano F, Soberon M, Megias M, Downie JA (2001) Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. J Bacteriol 183:854–864. https://doi.org/10.1128/jb.183.3.854-864.2001

    Article  CAS  Google Scholar 

  • Matiru VN, Jaffer MA, Dakora FD (2005) Rhizobial infection of African landraces of sorghum (Sorghum bicolor L.) and finger millet (Eleucine coracana L.) promotes plant growth and alters tissue nutrient concentration under axenic conditions. Symbiosis 40:7–15

    CAS  Google Scholar 

  • Mehboob I, Naveed M, Zahir ZA (2009) Rhizobial association with non-legumes: mechanisms and applications. Crit Rev Plant Sci 28:432–456. https://doi.org/10.1080/07352680903187753

    Article  CAS  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. https://doi.org/10.1111/1574-6976.12028

    Article  CAS  Google Scholar 

  • Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706. https://doi.org/10.3389/fmicb.2017.01706

    Article  Google Scholar 

  • Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Pollut 180:199–212. https://doi.org/10.1007/s11270-006-9263-2

    Article  CAS  Google Scholar 

  • Neumann H, Bode-Kirchhoff A, Madeheim A, Wetzel A (1998) Toxicity testing of heavy metals with the Rhizobium-legume symbiosis: high sensitivity to cadmium and arsenic compounds. Environ Sci Pollut Res Int 5:28–36

    Article  CAS  Google Scholar 

  • Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14:E1504. https://doi.org/10.3390/ijerph14121504

  • Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535

    Article  CAS  Google Scholar 

  • Pajuelo E, Rodriguez-Llorente ID, Dary M, Palomares AJ (2008) Toxic effects of arsenic on Sinorhizobium-Medicago sativa symbiotic interaction. Environ Pollut 154:203–211. https://doi.org/10.1016/j.envpol.2007.10.015

    Article  CAS  Google Scholar 

  • Panigrahi DP, Singh Randhawa G (2010) A novel method to alleviate arsenic toxicity in alfalfa plants using a deletion mutant strain of Sinorhizobium meliloti. Plant Soil 336:459–467

    Article  CAS  Google Scholar 

  • Perez-Montano F, Alias-Villegas C, Bellogin RA, del Cerro P, Espuny MR, Jimenez-Guerrero I, Lopez-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336. https://doi.org/10.1016/j.micres.2013.09.011

    Article  CAS  Google Scholar 

  • Ramirez MDA, Espana M, Aquirre C, Kojima K, Ohkama-Ohtsu N, Sekimoto H, Yokoyama T (2019) Burkholderia and Paraburkholderia are predominant soybean rhizobial genera in Venezuelan soils in different climatic and topographical regions. Microbes Environ 34:43–58. https://doi.org/10.1264/jsme2.ME18076

    Article  Google Scholar 

  • Reichman SM (2007) The potential use of the legume-Rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593

    Article  CAS  Google Scholar 

  • Reichman SM (2014) Probing the plant growth-promoting and heavy metal tolerance characteristics of Bradyrhizobium japonicum CB1809. Eur J Soil Biol 63:7–13

    Article  CAS  Google Scholar 

  • Reichman SM, Asher CJ, Mulligan DR, Menzies NW (2001) Seedling responses of three Australian tree species to toxic concentrations of zinc in solution culture. Plant Soil 235:151–158. https://doi.org/10.1023/a:1011903430385

    Article  CAS  Google Scholar 

  • Reichman SM, Parker DR (2007) Critical evaluation of three indirect assays for quantifying phytosiderophores released by the roots of Poaceae. Eur J Soil Sci 58:844–853

    Article  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180

    Article  Google Scholar 

  • Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Hoflich G, Hartmann A (1997) Root colonization of different plants by plant-growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63:2038–2046

    Article  CAS  Google Scholar 

  • Sekar S, Kandavel D (2010) Interaction of plant growth promoting rhizobacteria (PGPR) and endophytes with medicinal plants—new avenues for phytochemicals. J Phytol 2:91–100

    Google Scholar 

  • Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67:2229–2240

    Article  CAS  Google Scholar 

  • Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568. https://doi.org/10.1016/s0883-2927(02)00018-5

    Article  CAS  Google Scholar 

  • Souza R, Ambrosini A, Passaglia LM (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/S1415-475738420150053

    Article  Google Scholar 

  • Suhadolnik MLS, Salgado APC, Scholte LLS, Bleicher L, Costa PS, Reis MP, Dias MF, Avila MP, Barbosa FAR, Chartone-Souza E, Nascimento AMA (2017) Novel arsenic-transforming bacteria and the diversity of their arsenic-related genes and enzymes arising from arsenic-polluted freshwater sediment. Sci Rep 7:11231. https://doi.org/10.1038/s41598-017-11548-8

    Article  CAS  Google Scholar 

  • Tang L, Hamid L, Zehra A, Sahito ZZ, He ZL, Hussain B, Gurajala HK, Yang XE (2019) Characterization of fava bean (Vicia faba L.) genotypes for phytoremediation of cadmium and lead co-contaminated soils coupled with agro-production. Ecotoxicol Environ Saf 171:190–198. https://doi.org/10.1016/j.ecoenv.2018.12.083

    Article  CAS  Google Scholar 

  • Vázquez S, Goldsbrough P, Carpena RO (2009) Comparative analysis of the contribution of phytochelatins to cadmium and arsenic tolerance in soybean and white lupin. Plant Physiol Biochem 47:63–67

    Article  Google Scholar 

  • Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules. https://doi.org/10.3390/molecules21050573

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Vincent JM (1980) A manual for the practical study of root-nodule bacteria. IBP Handbook No. 15. Blackwell, Oxford

    Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408

    Article  CAS  Google Scholar 

  • Wittenbe JB, Bergerse FJ, Appleby CA, Turner GL (1974) Facilitated oxygen diffusion—role of leghemoglobin in nitrogen-fixation by bacteroids isolated from soybean root nodules. J Biol Chem 249:4057–4066

    Google Scholar 

  • Yang HC, Cheng J, Finan TM, Rosen BP, Bhattacharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187:6991e7

    Google Scholar 

  • Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Garcia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust J Plant Physiol 28:845–870

    CAS  Google Scholar 

  • Zhuang XL, Chen J, Shim H, Bai ZH (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413. https://doi.org/10.1016/j.envint.2006.12.005

    Article  Google Scholar 

Download references

Acknowledgements

Thanks to Mr Cameron Crombie for his technical assistance with instruments and chemicals. Thanks also to laboratory staff: Dr Sandro Longano, Dr Muthu Pannirselvam and Mrs Peggy Chang for technical support. Thanks to Paul Morrison for assisting with the ICP-MS analysis. Thanks also for donations of soybean seeds and sunflower seeds by Luke Gaynor and Loretta Serafin respectively, Department of Primary Industries, New South Wales, Australia, and of bradyrhizobial inoculum by Joe Millar from New-Edge Microbials, Australia.

Funding

The authors received an internal seed grant from the then School of Civil, Environmental and Chemical Engineering, RMIT University, to undertake this work.

Author information

Authors and Affiliations

  1. School of Engineering, RMIT University, Melbourne, VIC, Australia

    Md Ferdous Seraj & Suzie M. Reichman

  2. Department of Environmental Science and Management, North South University, Dhaka, Bangladesh

    Md Ferdous Seraj

  3. Department of Biochemistry and Molecular Biology, University of Dhaka, Dhaka, Bangladesh

    Tania Rahman

  4. School of Science, RMIT University, Bundoora, VIC, Australia

    Ann C. Lawrie

  5. Centre for Anthropogenic Pollution Impact and Management, School of BioSciences, University of Melbourne, Parkville, VIC, Australia

    Suzie M. Reichman

Authors
  1. Md Ferdous Seraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tania Rahman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ann C. Lawrie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Suzie M. Reichman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suzie M. Reichman.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seraj, M.F., Rahman, T., Lawrie, A.C. et al. Assessing the Plant Growth Promoting and Arsenic Tolerance Potential of Bradyrhizobium japonicum CB1809. Environmental Management 66, 930–939 (2020). https://doi.org/10.1007/s00267-020-01351-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00267-020-01351-z

Keywords

Search

Navigation