Plant species-specificity and effects of bioinoculants and fertilization on plant performance for nickel phytomining

  • Zahra Ghasemi
  • Seyed Majid Ghaderian
  • Beatriz Rodríguez-Garrido
  • Ángeles Prieto-Fernández
  • Petra Susan Kidd
Regular Article

Abstract

Aims

To investigate the effects of fertilization and bacterial inoculation on the growth, health and Ni phytoextraction capacity of three Ni-hyperaccumulators, Odontarrhena bracteata, O. inflata and O. serpyllifolia.

Methods

Plants were grown for three months in serpentine soil fertilized with inorganic NPK or amended with cow manure and inoculated with five rhizobacterial strains (previously isolated from O. serpyllifolia). Shoot and root dry weight (DW) yields, Ni accumulation and removal, nutritive status and stress indicators were determined.

Results

Plants grown in manure-amended soil showed significantly higher DW yields, improved nutritive status and higher total Ni phytoextracted. Some bacterial inoculants enhanced Ni removal due to the stimulation in growth and/or increase in shoot Ni concentration but this depended on the plant species, soil type and inoculant. Pseudoarthrobacter oxydans strain SBA82 enhanced shoot DW yield of all three Odontarrhena spp. in at least one soil type. Paenarthrobacter sp. strain LA44 and Stenotrophomonas sp. strain MA98 promoted growth of O. serpyllifolia and O. bracteata. Inoculated plants showing growth promotion presented lower activities of antioxidative enzymes, and concentrations of malondialdehyde (MDA) and H2O2, indicating a protective effect of these inoculants on the plants.

Conclusion

Rhizobacterial inoculants applied in combination with manure can improve plant growth and health, and Ni phytoextraction, in some hyperaccumulating Odontarrhena spp.

Keywords

Plant growth promoting rhizobacteria (PGPR) Ultramafic soil Alyssum hyperaccumulators Antioxidant stress enzymes 

Notes

Acknowledgements

ZG would like to acknowledge a scholarship from the Ministry of Science, Research and Technology of Iran (MSRT), Graduate School of University of Isfahan and Plant Antioxidants Center of Excellence (PACE) of University of Isfahan. This research was funded by the FACCE Surplus project Agronickel (ID71) and Ministerio de Economía, Industria y Competitividad (PCIN-2017-028). Finally, the authors thank Marián de Jesús González and Lucia Debernardo Espiñeira for technical assistance.

References

  1. Abou-Shanab R et al (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224CrossRefGoogle Scholar
  2. Abou-Shanab R, Angle J, Chaney R (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889CrossRefGoogle Scholar
  3. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefPubMedGoogle Scholar
  4. Alvarez-Lopez V, Prieto-Fernández Á, Becerra-Castro C, Monterroso C, Kidd PS (2016a) Rhizobacterial communities associated with the flora of three serpentine outcrops of the Iberian Peninsula. Plant Soil 403:233–252CrossRefGoogle Scholar
  5. Alvarez-Lopez V, Prieto-Fernández Á, Cabello-Conejo M, Kidd P (2016b) Organic amendments for improving biomass production and metal yield of Ni-hyperaccumulating plants. Sci Total Environ 548:370–379CrossRefPubMedGoogle Scholar
  6. Alvarez-López V, Prieto-Fernández Á, Roiloa S, Rodríguez-Garrido B, Herzig R, Puschenreiter M, Kidd PS (2017) Evaluating phytoextraction efficiency of two high-biomass crops after soil amendment and inoculation with rhizobacterial strains. Environ Sci Pollut Res 24:7591–7606CrossRefGoogle Scholar
  7. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–5CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bani A, Echevarria G, Sulçe S, Morel JL (2015) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediat 17:117–127CrossRefGoogle Scholar
  9. Beaudoin-Eagan LD, Thorpe TA (1985) Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures. Plant Physiol 78:438–441CrossRefPubMedPubMedCentralGoogle Scholar
  10. Becerra-Castro C, Kidd P, Kuffner M, Prieto-Fernández A, Hann S, Monterroso C, Sessitsch A, Wenzel W, Puschenreiter M (2013) Bacterially induced weathering of ultramafic rock and its implications for phytoextraction. Appl Environ Microbiol 79:5094–5103CrossRefPubMedPubMedCentralGoogle Scholar
  11. Benizri E, Kidd PS (2018) The role of the rhizosphere and microbes associated with hyperaccumulator plants in metal accumulation. In: Van der Ent A, Echevarria G, Baker A, Morel JL (eds) Agromining: Farming for Metals. Extracting Unconventional Resources Using Plants. Springer, Berlin, pp 157–188Google Scholar
  12. Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol 156:205–215CrossRefGoogle Scholar
  13. 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 72:248–254CrossRefPubMedGoogle Scholar
  14. Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  15. Broadhurst CL, Chaney RL (2016) Growth and Metal Accumulation of an Alyssum murale Nickel Hyperaccumulator Ecotype Co-cropped with Alyssum montanum and perennial ryegrass in Serpentine Soil. Front Plant Sci 7:451CrossRefPubMedPubMedCentralGoogle Scholar
  16. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, PortlandGoogle Scholar
  17. Busse HJ (2016) Review of the taxonomy of the genus Arthrobacter, emendation of the genus Arthrobacter sensu lato, proposal to reclassify selected species of the genus Arthrobacter in the novel genera Glutamicibacter gen. nov., Paeniglutamicibacter gen. nov., Pseudoglutamicibacter gen. nov., Paenarthrobacter gen. nov. and Pseudarthrobacter gen. nov., and emended description of Arthrobacter roseus. Int J Syst Evol Microbiol 66:9–37CrossRefPubMedGoogle Scholar
  18. Cabello-Conejo M, Centofanti T, Kidd P, Prieto-Fernández Á, Chaney R (2013) Evaluation of plant growth regulators to increase nickel phytoextraction by Alyssum species. Int J Phytoremediat 15:365–375CrossRefGoogle Scholar
  19. Cabello-Conejo M, Becerra-Castro C, Prieto-Fernández A, Monterroso C, Saavedra-Ferro A, Mench M, Kidd P (2014a) Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant Soil 379:35CrossRefGoogle Scholar
  20. Cabello-Conejo M, Prieto-Fernández Á, Kidd P (2014b) Exogenous treatments with phytohormones can improve growth and nickel yield of hyperaccumulating plants. Sci Total Environ 494:1–8CrossRefPubMedGoogle Scholar
  21. Chaney RL, Angle JS, Baker AJM, Li Y-M (1998) Method for phytomining of nickel, cobalt and other metals from soil. US Patent 5,711,784, 27 Jan 1998Google Scholar
  22. Chaney RL, Fellet G, Torres R, Centofanti T, Green CE, Marchiol L (2009) Using Chelator-buffered Nutrient Solutions to Limit Ni Phytoavailability to the Ni-Hyperaccumulator Alyssum murale. Northeast Nat 16:215–222CrossRefGoogle Scholar
  23. Chaney RL, Reeves RD et al (2014) Phytoremediation and phytomining: using plants to remediate contaminated or mineralized environments. In: Rajakaruna R, Boyd RS, Harris T (eds) Plant ecology and evolution in harsh environments. Nova Sience Publishers, New York, pp 365–391Google Scholar
  24. Chaney RL, Baklanov IA (2017) Chapter Five-Phytoremediation and Phytomining: Status and Promise. Adv Bot Res 83:189–221CrossRefGoogle Scholar
  25. Chiang H-C, Lo J-C, Yeh K-C (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798CrossRefPubMedGoogle Scholar
  26. Cuypers A et al (2010) Cadmium stress: an oxidative challenge. Bio Metals 23:927–940Google Scholar
  27. Dewir Y, Chakrabarty D, Ali M, Hahn E, Paek K (2006) Lipid peroxidation and antioxidant enzyme activities of Euphorbia millii hyperhydric shoots. Environ Exp Bot 58:93–99CrossRefGoogle Scholar
  28. Everhart JL, McNear D, Peltier E, Van der Lelie D, Chaney RL, Sparks DL (2006) Assessing nickel bioavailability in smelter-contaminated soils. Sci Total Environ 367:732–744CrossRefPubMedGoogle Scholar
  29. Fabiano CC, Tezotto T, Favarin JL, Polacco JC, Mazzafera P (2015) Essentiality of nickel in plants: a role in plant stresses. Front Plant Sci 6:754.  https://doi.org/10.3389/fpls.2015.00754 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191CrossRefPubMedPubMedCentralGoogle Scholar
  31. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254CrossRefGoogle Scholar
  32. Fravel D (2005) Commercialization and implementation of biocontrol 1. Annu Rev Phytopathol 43:337–359Google Scholar
  33. Ghasemi R, Ghaderian SM (2009) Responses of two populations of an Iranian nickel-hyperaccumulating serpentine plant, Alyssum inflatum Nyar., to substrate Ca/Mg quotient and nickel. Environ Exp Bot 67:260–268CrossRefGoogle Scholar
  34. Ghasemi R, Ghaderian SM, Krämer U (2009) Interference of nickel with copper and iron homeostasis contributes to metal toxicity symptoms in the nickel hyperaccumulator plant Alyssum inflatum. New Phytol 184:566–580CrossRefPubMedGoogle Scholar
  35. Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefPubMedPubMedCentralGoogle Scholar
  36. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68CrossRefPubMedGoogle Scholar
  37. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  38. Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11CrossRefPubMedGoogle Scholar
  39. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  40. Janmohammadi M, Bihamta M, Ghasemzadeh F (2013) Influence of rhizobacteria inoculation and lead stress on the physiological and biochemical attributes of wheat genotypes. Cercet Agron Mold 46:49–67Google Scholar
  41. Kidd P et al (2009) Trace element behaviour at the root–soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259CrossRefGoogle Scholar
  42. Kidd PS, Álvarez-López V, Becerra-Castro C, Cabello-Conejo M, Prieto-Fernández Á (2017) Chapter Three-Potential Role of Plant-Associated Bacteria in Plant Metal Uptake and Implications in Phytotechnologies. Adv Bot Res 83:87–126CrossRefGoogle Scholar
  43. Li Y-M, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115CrossRefGoogle Scholar
  44. Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Amer J 42:421–428Google Scholar
  45. Ma Y, Rajkumar M, Freitas H (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75:719–725CrossRefPubMedGoogle Scholar
  46. Mergeay M, Nies D, Schlegel H, Gerits J, Charles P, Van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334PubMedPubMedCentralGoogle Scholar
  47. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefPubMedGoogle Scholar
  48. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  49. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  50. Nkrumah PN, Chaney RL, Morel JL (2018) Agronomy of ‘Metal Crops’ Used in Agromining. In: Van der Ent, A, Echevarria G, Baker A, Morel JL (eds) Agromining: Farming for Metals. Extracting Unconventional Resources Using Plants. Springer, Berlin, pp 19–38 Google Scholar
  51. Nkrumah PN, Baker AJ, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A (2016) Current status and challenges in developing nickel phytomining: an agronomic perspective. Plant Soil 406:55–69CrossRefGoogle Scholar
  52. Pollard AJ, Reeves RD, Baker AJ (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217:8–17CrossRefPubMedGoogle Scholar
  53. Robinson B, Chiarucci A, Brooks R, Petit D, Kirkman J-H, Gregg P, De Dominicis V (1997) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86CrossRefGoogle Scholar
  54. Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52CrossRefGoogle Scholar
  56. Singh N, Srivastava S, Rathaur S, Singh N (2016) Assessing the bioremediation potential of arsenic tolerant bacterial strains in rice rhizosphere interface. J Environ Sci 48:112–119CrossRefGoogle Scholar
  57. Singleton V, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  58. Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413CrossRefPubMedGoogle Scholar
  59. Thijs S, Langill T, Vangronsveld J (2017) Chapter Two- The Bacterial and Fungal Microbiota of Hyperaccumulator Plants: Small Organisms, Large Influence. Adv Bot Res 83:43–86CrossRefGoogle Scholar
  60. van der Ent A, Baker A, Van Balgooy M, Tjoa A (2013) Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): mining, nickel hyperaccumulators and opportunities for phytomining. J Geochem Explor 128:72–79CrossRefGoogle Scholar
  61. Vangronsveld J et al (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794CrossRefGoogle Scholar
  62. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66CrossRefGoogle Scholar
  63. Verma S, Dubey R (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Zahra Ghasemi
    • 1
  • Seyed Majid Ghaderian
    • 1
  • Beatriz Rodríguez-Garrido
    • 2
  • Ángeles Prieto-Fernández
    • 2
  • Petra Susan Kidd
    • 2
  1. 1.Department of Biology, Faculty of SciencesUniversity of IsfahanIsfahanIran
  2. 2.Instituto de Investigaciones Agrobiológicas de Galicia (IIAG), Consejo Superior de Investigaciones Científicas (CSIC)Santiago de CompostelaSpain

Personalised recommendations