Skip to main content

Advertisement

SpringerLink
Log in

Is annual or perennial harvesting more efficient in Ni phytoextraction?

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

The use of perennial metal hyperaccumulators in phytoextraction provides an excellent gateway toward the removal of heavy metals from polluted sites, and the opportunity for the phytomining of valuable metals. In order to further advance our understanding of the effect of cropping systems on metal phytoextraction, it is important to investigate the effect of harvesting time. This study focuses on the variation in biomass production, Ni concentration and Ni mass across the different phenological stages, populations and organs of Alyssum lesbiacum, in order to evaluate when Ni phytoextraction is at a maximum.

Methods

We sampled 60 single-phenological stage plots in three A. lesbiacum populations and we determined biomass production and Ni concentration at the plant organ level.

Results

Based on spontaneous A. lesbiacum vegetation, we were able to record remarkably high values of Ni phytoextraction. Biomass production and Ni concentration were found to be maximal on the third and fourth year of the A. lesbiacum life cycle respectively, while maximum phytoextraction capacity was reached in the third year.

Conclusions

Our results: (1) demonstrate the significant variation in Ni phytoextraction across different phenological stages, populations and organs of A. lesbiacum, (2) imply that its phytoextraction potential is mostly influenced by biomass production and (3) suggest that perennial harvests could be an interesting alternative to consider in the future.

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

Access this article

Log in via an institution

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

  • Adamidis GC, Aloupi M, Kazakou E, Dimitrakopulos PG (2014a) Intra-specific variation in Ni tolerance, accumulation and translocation patterns in the Ni-hyperaccumulator Alyssum lesbiacum. Chemosphere 95:496–502

    Article  CAS  PubMed  Google Scholar 

  • Adamidis GC, Dimitrakopoulos PG, Manolis A, Papageorgiou AC (2014b) Genetic diversity and population structure of the serpentine endemic Ni hyperaccumulator Alyssum lesbiacum. Plant Syst Evol 300:2051–2060

    Article  Google Scholar 

  • Adamidis GC, Kazakou E, Baker AJM, Reeves RD, Dimitrakopoulos PG (2014c) The effect of harsh abiotic conditions on the diversity of serpentine plant communities on lesbos, an eastern Mediterranean island. Plant Ecol Divers 7:433–444

    Article  Google Scholar 

  • Adamidis GC, Kazakou E, Fyllas NM, Dimitrakopoulos PG (2014d) Species adaptive strategies and leaf economic relationships across serpentine and non-serpentine habitats on lesbos, eastern Mediterranean. PLoS One 9:e96034. doi:10.1371/journal.pone.0096034

    Article  PubMed  PubMed Central  Google Scholar 

  • Adamidis GC, Kazakou E, Aloupi M, Dimitrakopoulos PG (2016) Is it worth hyperaccumulating Ni on non-serpentine soils? Decomposition dynamics of mixed-species litters containing hyperaccumulated Ni across serpentine and non-serpentine environments. Ann Bot 117(7):1241–1248

    Article  PubMed  PubMed Central  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Alkorta I, Hernández-Allica J, Becerril J, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci Biotechnol 3:71–90

    Article  CAS  Google Scholar 

  • Bani A, Echevarria G, Sulçe S, Morel J, Mullai A (2007) In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil 293:79–89

    Article  CAS  Google Scholar 

  • Bani A, Echevarria G, Sulçe S, Morel JL (2015a) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediat 17:117–127

    Article  CAS  Google Scholar 

  • Bani A, Echevarria G, Zhang X, Benizri E, Laubie B, Morel JL et al (2015b) The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Aust J Bot 63:72–77. doi:10.1071/bt14285

    CAS  Google Scholar 

  • Bednářová Z, Kalina J, Hájek O, Sáňka M, Komprdová K (2016) Spatial distribution and risk assessment of metals in agricultural soils. Geoderma 284:113–121

    Article  Google Scholar 

  • Belouchrani AS, Mameri N, Abdi N, Grib H, Lounici H, Drouiche N (2016) Phytoremediation of soil contaminated with Zn using canola(Brassica napus L). Ecol Eng 95:43–49

    Article  Google Scholar 

  • Berti WWR, Cunningham SD (2000) Phytostabilization of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals – using plants to clean up the environment. John Wiley & Sons, Inc, New York, pp 71–88

    Google Scholar 

  • Bian Z, Miao X, Lei S, Chen S-E, Wang W, Struthers S (2012) The challenges of reusing mining and mineral-processing wastes. Science 337(6095):702–703

    Article  CAS  PubMed  Google Scholar 

  • Broadhurst CL, Chaney RL, Angle JS, Erbe EF, Maugel TK (2004) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265:225–242

    Article  CAS  Google Scholar 

  • Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akmans Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). P Roy Soc Lond B 203:387–403

    Article  CAS  Google Scholar 

  • Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining Trends Plant Sci 1: 359–362

  • Chaney RL (1983) Plant uptake of inorganic waste constituents. In: Parr JFEA (ed) Land treatment of hazardous wastes. Noyes Data Corp, Park Ridge, pp 50–76

    Google Scholar 

  • Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284

    Article  CAS  PubMed  Google Scholar 

  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1433

    Article  CAS  PubMed  Google Scholar 

  • Chardot V, Massoura ST, Echevarria G, Reeves RD, Morel JL (2005) Phytoextraction potential of the nickel hyperaccumulators Leptoplax emarginata and Bornmuellera tymphaea. Int J Phytoremediat 7:323–335

    Article  CAS  Google Scholar 

  • Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390

    Article  CAS  PubMed  Google Scholar 

  • Cluis C (2004) Junk-greedy greens: phytoremediation as a new option for soil decontamination. Bio Teach J 2:61–67

    Google Scholar 

  • Coinchelin D, Bartoli F, Robin C, Echevarria G (2012) Ecophysiology of nickel phytoaccumulation: a simplified biophysical approach. J Exp Bot 63:5815–5827

    Article  CAS  PubMed  Google Scholar 

  • Deng T, Tang Y, van der Ent A, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil 404:35–45

    Article  CAS  Google Scholar 

  • Durand A, Piutti S, Rue M, Morel JL, Echevarria G, Benizri E (2016) Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria. Plant Soil 399(1–2):179–192

    Article  CAS  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Chaney RL (2015) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780

    Article  PubMed  Google Scholar 

  • Greipsson S (2011) Phytoremediation Nat Educ Knowl 3(10), 7

  • Kachenko AG, Singh B (2006) Heavy metals contamination in vegetables grown in urban and metal smelter contaminated sites in Australia. Water Air Soil Pollut 169(3):101–123

    Article  CAS  Google Scholar 

  • Kazakou E, Adamidis GC, Baker AJM, Reeves RD, Godino M, Dimitrakopoulos PG (2010) Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332:369–385

    Article  CAS  Google Scholar 

  • Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534

    Article  PubMed  Google Scholar 

  • Li YM, Chaney RL, Brewer E, Roseberg RJ, Angle JS, Baker AJM, Reeves RD, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115

    Article  CAS  Google Scholar 

  • Li JT, Liao B, Lan CY, Ye ZH, Baker AJM, Shu WS (2010) Cadmium tolerance and accumulation in cultivars of a high-biomass tropical tree (Averrhoa carambola) and its potential for phytoextraction. J Environ Qual 39:1262–1268

    Article  CAS  PubMed  Google Scholar 

  • Macek T, Kotrba P, Svatos A, Novakova M, Demnerova K, Mackova M (2008) Novel roles for genetically modified plants in environmental protection. Trends Biotechnol 26:146–152

    Article  CAS  PubMed  Google Scholar 

  • Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li R, Zhang Z (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicol Environ Saf 126:111–121

    Article  CAS  PubMed  Google Scholar 

  • Milic D, Lukovic J, Ninkov J, Zeremski-Skoric T, Zoric L, Vasin J, Milic S (2012) Heavy metal content in halophytic plants from inland and maritime saline areas. Cent Eur J Biol 7:307–317

    CAS  Google Scholar 

  • Moon JW, Moon HS, Woon NC, Hahn JS, Won JS (2000) Evaluation of heavy metal contamination and implication of multiple sources from Hunchun basin, northeastern China. Environ Geol 39(9):1039–1052

    Article  CAS  Google Scholar 

  • Nkrumah PN, Baker AJM, 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(1–2):55–69

    Article  CAS  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rafati M, Khorasani N, Moattar F, Shirvany A, Moraghebi F, Hosseinzadeh S (2011) Phytoremediation potential of Populus alba and Morus alba for cadmium, chromuim and nickel absorption from polluted soil. Int J Environ Res 5:961–970

    CAS  Google Scholar 

  • Reeves RD, Baker AJM, Kelepertsis A (1997) The distribution and biogeochemistry of some serpentine plants of Greece. In: Jaffre T, Reeves RD, Becquer T (eds) Ecologie des milieux sur roches ultramafiques et sur sols metalliferes. ORSTOM, Noumea, pp 205–207

    Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxicmetals. Wiley, New York, pp 193–229

  • Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997a) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126

    Article  CAS  Google Scholar 

  • Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, De Dominicis V (1997b) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86

    Article  CAS  Google Scholar 

  • Robinson BH, Brooks RR, Clothier BE (1999) Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot-London 84:689–694

    Article  CAS  Google Scholar 

  • Robinson BH, Anderson CWN, Dickinson NM (2015) Phytoextraction: where’s the action? J Geochem Explor 151:34–40

    Article  CAS  Google Scholar 

  • Singer AC, Bell T, Heywood CA, Smith JAC, Thompson IP (2007) Phytoremediation of mixed-contaminated soil using the hyperaccumulator plant Alyssum lesbiacum: evidence of histidine as a measure of phytoextractable nickel. Environ Pollut 147:74–82

    Article  CAS  PubMed  Google Scholar 

  • Strid A, Tan K (2002) Flora Hellenica, vol 2. A.R.G. Gantner Verlag KG, Ruggell

  • Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (1964-1980) Flora Europaea. Cambridge University Press, Cambridge

  • US Environmental Protection Agency (2007) Method 3051A, microwave assisted acid digestion of sediments, Sludges, soils, and oils, revision 1. Test Methods for Evaluating Solid Waste, USEPA Washington DC

    Google Scholar 

  • Zhang X, Houzelot V, Bani A, Morel JL, Echevarria G, Simonnot M-O (2014) Selection and combustion of nickel-hyperaccumulators for the phytomining process. Int J Phytoremed 16:1058–1072

    Article  CAS  Google Scholar 

  • Zhang X, Zhong T, Liu L, Ouyang X (2015) Impact of soil heavy metal pollution on food safety in China. PLoS One 10(8):e0135182

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Professor Triantaphyllos Akriotis for editorial assistance, and the Editor van der Ent and three anonymous reviewers for their constructive comments on an earlier version of the manuscript.

Author information

Author notes

  1. Petros Mastoras and Maria-Ioanna Papadaki equally contributed to this work.

Authors and Affiliations

  1. Biodiversity Conservation Laboratory, Department of Environment, University of the Aegean, Lesbos, 81100, Mytilene, Greece

    George C. Adamidis, Petros Mastoras, Maria-Ioanna Papadaki & Panayiotis G. Dimitrakopoulos

  2. Water and Air Quality Laboratory, Department of Environment, University of the Aegean, Lesbos, 81100, Mytilene, Greece

    Maria Aloupi

Authors
  1. George C. Adamidis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Aloupi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Petros Mastoras
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria-Ioanna Papadaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Panayiotis G. Dimitrakopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to George C. Adamidis.

Additional information

Responsible Editor: Antony Van der Ent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adamidis, G.C., Aloupi, M., Mastoras, P. et al. Is annual or perennial harvesting more efficient in Ni phytoextraction?. Plant Soil 418, 205–218 (2017). https://doi.org/10.1007/s11104-017-3287-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3287-9

Keywords

Search

Navigation