Skip to main content

Advertisement

Log in

Mine land valorization through energy maize production enhanced by the application of plant growth-promoting rhizobacteria and arbuscular mycorrhizal fungi

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The use of heavy metals (HM) contaminated soils to grow energy crops can diminish the negative impact of HM in the environment improving land restoration. The effect of two PGPR (B1—Chryseobacterium humi ECP37T and B2—Pseudomonas reactans EDP28) and an AMF (F—Rhizophagus irregularis) on growth, Cd and Zn accumulation, and nutritional status of energy maize plants grown in a soil collected from an area adjacent to a Portuguese mine was assessed in a greenhouse experiment. Both bacterial strains, especially when co-inoculated with the AMF, acted as plant growth-promoting inoculants, increasing root and shoot biomass as well as shoot elongation. Cadmium was not detected in the maize tissues and a decrease in Zn accumulation was observed for all microbial treatments in aboveground and belowground tissues—with inoculation of maize with AMF and strain B2 leading to maximum reductions in Zn shoot and root accumulation of up to 48 and 43 %, respectively. Although microbial single inoculation generally did not increase N and P levels in maize plants, co-inoculation of the PGPR and the AMF improved substantially P accumulation in roots. The DGGE analysis of the bacterial rhizosphere community showed that the samples inoculated with the AMF clustered apart of those without the AMF and the Shannon-Wiener Index (H′) increased over the course of the experiment when both inoculants were present. This work shows the benefits of combined inoculation of AMF and PGPR for the growth energy maize in metal contaminated soils and their potential for the application in phytomanagement strategies.

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
Fig. 4

Similar content being viewed by others

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylic acid

AMF:

Arbuscular mycorrhizal fungi

BCF:

Bioconcentration factor

DGGE:

Denaturing gradient gel electrophoresis

EDTA:

Ethylenediaminetetraacetic acid

ERM:

Extraradical mycelium

FAAS:

Flame atomic absorption spectrometry

IAA:

Indole-3-acetic acid

H′:

Shannon-Wiener index

HM:

Heavy metals

NH4-Ac:

Ammonium acetate

PCA:

Principal component analysis

PGPR:

Plant growth-promoting rhizobacteria

TF:

Translocation factor

UPGMA:

Unweighted pair group method with arithmetic mean

References

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91(7):869–881

    Article  CAS  Google Scholar 

  • Aloui A, Dumas-Gaudot E, Daher Z, Tuinen D, Aschi-Smit S, Morandi D (2012) Influence of arbuscular mycorrhizal colonisation on cadmium induced Medicago truncatula root isoflavonoid accumulation. Plant Physiol Biochem 60:233–239

    Article  CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  CAS  Google Scholar 

  • Ávila PF, da Silva EF, Salgueiro AR, Farinha JA (2008) Geochemistry and mineralogy of mill tailings impoundments from the Panasqueira mine (Portugal): implications for the surrounding environment. Mine Water Environ 27:210–224

    Article  Google Scholar 

  • Bergmann W (1993) Bergmann Ernährungsstörungen bei Kulturplanzen, 3rd edn. Spektrum Akademischer Verlag, Stuttgart

    Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  Google Scholar 

  • De Koe T (1994) Agrostis castellana and Agrostis delicatula on heavy metal and arsenic enriched sites in NE Portugal. Sci Total Environ 145:103–109

    Article  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    Article  CAS  Google Scholar 

  • Gamalero E, Trotta A, Massa N, Copetta A, Martinotti MG, Berta G (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza 14:185–192

    Article  Google Scholar 

  • Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30:581–599

    Article  CAS  Google Scholar 

  • Garg N, Kaur H (2013) Impact of cadmium-zinc interactions on metal uptake, translocation and yield in pigeonpea genotypes colonized by arbuscular mycorrhizal fungi. J Plant Nutr 36:67–90

    Article  CAS  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15

    Article  Google Scholar 

  • Gomes HI (2012) Phytoremediation for bioenergy: challenges and opportunities. Environ Technol Rev 1:59–66

    Article  CAS  Google Scholar 

  • Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3(4):267–273

    Article  Google Scholar 

  • Houba VJG, Van der Lee JJ, Novozamsky I (1995) Soil analysis procedures. Wageningen: Department of Soil Science and Plant Nutrition. Wageningen Agricultural University, Syllabus

  • Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16

    Google Scholar 

  • Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164

    Article  CAS  Google Scholar 

  • Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2011) Trace elements on soils and plants, 4th edn. CRC Press, New York

    Google Scholar 

  • Khan S, Hesham AEL, Qiao M, Rehman S, He JZ (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296

    Article  CAS  Google Scholar 

  • Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484

    Article  CAS  Google Scholar 

  • Liang C-C, Li T, Xiao Y, Liu MJ, Zhang HB, Zhao ZW (2009) Effects of inoculation with arbuscular mycorrhizal fungi on maize grown in multi-metal contaminated soils. Int J Phytoremediation 11:692–703

    Article  CAS  Google Scholar 

  • Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206

    Article  CAS  Google Scholar 

  • Liu LZ, Gong ZQ, Zhang YL, Li PJ (2011) Growth, cadmium accumulation and physiology of marigold (Tagetes erecta L.) as affected by arbuscular mycorrhizal fungi. Pedosphere 21(3):319–327

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manag 90:831–837

    Article  Google Scholar 

  • Marques APGC, Pires C, Moreira H, Rangel AOSS, Castro PML (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235

    Article  CAS  Google Scholar 

  • Marques APGC, Moreira H, Franco AR, Rangel AOSS, Castro PML (2013) Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria—effects on phytoremediation strategies. Chemosphere 92:74–83

    Article  CAS  Google Scholar 

  • Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28:23–36

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Meers E, Van Slycken S, Adriaensen K, Ruttens A, Vangronsveld J, Du Laing G, Witters N, Thewys T, Tack FMG (2010) The use of bio-energy crops (Zea mays) for ‘phytoattenuation’ of heavy metals on moderately contaminated soils: a field experiment. Chemosphere 78:35–41

    Article  CAS  Google Scholar 

  • Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775

    Article  CAS  Google Scholar 

  • Moreira H, Marques APGC, Franco AR, Rangel AOSS, Castro PML (2014) Phytomanagement of Cd-contaminated soils using maize (Zea mays L.) assisted by plant growth-promoting rhizobacteria. Environ Sci Pollut Res 21:9742–9753

    Article  CAS  Google Scholar 

  • Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448

    Article  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    Article  CAS  Google Scholar 

  • Novozamsky I, Houba VJG, Van Eck R, Van Vark W (1983) A novel digestion technique for multi‐element plant analysis. Commun Soil Sci Plant Anal 14:239–248

    Article  CAS  Google Scholar 

  • Pereira SIA, Castro PML (2014) Phosphate-solubilizing rhizobacteria enhance Zea mays growth in agricultural P-deficient soils. Ecol Eng 73:526–535

    Article  Google Scholar 

  • Pereira SIA, Barbosa L, Castro PML (2015) Rhizobacteria isolated from a metal-polluted area enhance plant growth in Zn and Cd contaminated sites. Int J Environ Sci Technol 12:2127–2142

    Article  CAS  Google Scholar 

  • Pires C (2010) Bacteria in heavy metal contaminated soil: diversity, tolerance and use in remediation systems. PhD thesis. Cranfield University, UK

  • Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842

    Article  CAS  Google Scholar 

  • Robinson BH, Bañuelos G, Conesa HM, Evangelou MWH, Schulin R (2009) The phytomanagement of trace elements in soil. Crit Rev Plant Sci 28:240–266

    Article  CAS  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 2011:1–30

    Google Scholar 

  • Sheoran V, Sheoran AS, Poonia P (2010) Soil reclamation of abandoned mine land by revegetation: a review. Int J Soil Sediment Water 3(2):1–21

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 2nd edn. Academic Press, London

    Google Scholar 

  • Solís-Domíngues FA, Valentín-Vargas A, Chorover J, Maier RM (2011) Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci Total Environ 409(6):1009–1016

    Article  Google Scholar 

  • Thewys T, Witters N, Van Slycken S, Ruttens A, Meers E, Tack FMG, Vangronsveld J (2010) Economic viability of phytoremediation of a cadmium contaminated agricultural area using energy maize. Part I: effect on the farmer’s income. Int J Phytoremediation 12:650–662

    Article  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  Google Scholar 

  • Wallinga I, Vark W, Houba VJG, Lee JJ (1989) Plant analysis procedures. Department of Soil Science and Plant Nutrition, Wageningen Agricultural University, Wageningen

    Google Scholar 

  • Whips JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    Article  Google Scholar 

  • Wuana RA, Okieimen FE (2010) Phytoremediation potential of maize (Zea mays L). A review. Afr J Gen Agric 6(4):275–287

    Google Scholar 

  • Zhang HH, Tang M, Chen H, Zheng CL, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46:306–311

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by Fundação para a Ciência e a Tecnologia and Fundo Social Europeu (III Quadro Comunitário de apoio), research grants of Helena Moreira (SFRH/BPD/105152/2014), Sofia I.A. Pereira (SFRH/BPD/65134/2009), Ana P.G.C. Marques (EXPL/AGR-PRO/0521/2013), and by National Funds through FCT—Fundação para a Ciência e Tecnologia under the project PEst-OE/EQB/LA0016/2013.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paula M. L. Castro.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moreira, H., Pereira, S.I.A., Marques, A.P.G.C. et al. Mine land valorization through energy maize production enhanced by the application of plant growth-promoting rhizobacteria and arbuscular mycorrhizal fungi. Environ Sci Pollut Res 23, 6940–6950 (2016). https://doi.org/10.1007/s11356-015-5914-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5914-4

Keywords

Navigation