Skip to main content
SpringerLink
Log in

Differential effects of nickel dosages on in vitro and in vivo seed germination and expression of a high affinity nickel-transport family protein (AT2G16800) in trembling aspen (Populus tremuloides)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstracts

It has been demonstrated that a number of metals including mercury (Hg), zinc (Zn), cadmium (Cd), cobalt (Co), lead (Pb), copper (Cu), and nickel (Ni) decrease seed germination rates and plant growth. The threshold levels of metal toxicity on seed germination, plant development, and gene regulation have not been studied in detail. The main objective of this study was to assess in vitro and in vivo the effects of different doses of nickel on Trembling aspen (Populus tremuloides) seed germination and regulation of the high affinity nickel transporter family protein (AT2G16800) gene. The in vitro assays showed that Nickel completely inhibited seed germination even at the lowest concentration of 0.401 mg Ni per mL (in media) tested. However, when the same concentration of nickel (150 mg Ni per 1 kg of dry soil) was added to soil samples, during the vivo assays, almost all of the seeds germinated. Significant inhibition of seed germination was observed when soil samples were treated with at least 400 mg/kg of Ni. No damages were observed on growing seedlings treated with 150, 400, and 800 mg/kg of Ni. Only the highest dose of 1, 600 mg/kg resulted in visible leaf and stem damages and reduced growth on 75% of seedlings. A significant repression of the AT2G16800 gene was observed for the 400, 800, and 1600 mg/kg of nickel treatments compared to the water control with the lowest level of expression observed in samples treated with 800 mg/kg of Ni. Results of this study suggest that P. tremuloides populations will likely be sustainable for long term in sites that are highly contaminated with Ni including mining regions since the bioavailable amount of this metal is usually below 400 mg/kg in Canada.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Ahmad MS, Hussain M, Saddiq R, Alvi AK (2007) Mungbean: a nickel indicator, accumulator or excluder? Bull Environ Contam Toxicol 78:319–24

    Article  CAS  Google Scholar 

  • Asgeir R, Almå S, Mulder J, Bakken LR (2005) Trace metal exposure of soil bacteria depends on their position in the soil matrix. Environ Sci Technol 39(16):5927–5932. https://doi.org/10.1021/es048113w

    Article  CAS  Google Scholar 

  • Ayaz FA, Kadioglu A (1997) Effects of metals (Zn, Cd, Cu, Hg) on the soluble protein bands of germinating Lens esculenta L. seeds. Tr J Bot 21:85–88

    Google Scholar 

  • Baccouch S, Chaoui A, El Ferjani E (2001) Nickel toxicity induces oxidative damage in Zea mays roots. J Plant Nutr 21:577–588

    Article  Google Scholar 

  • Bishnoi NR, Sheoran IS, Singh R (1993) Influence of cadmium and nickel on photosynthesis and water relations in wheat leaves of different insertion level. Photosynthetica 28:473–479

    CAS  Google Scholar 

  • Booker FL (2004) Influence of ozone on ribonuclease activity in wheat (Triticum aestivum) leaves. Physiol Plant 120:249–255

    Article  CAS  Google Scholar 

  • Boominathan R, Doran PM (2002) Ni-induced oxidative stress in roots of the Ni hyperaccumulator Alyssum bertolonii. New Phytol 156:205–215

    Article  CAS  Google Scholar 

  • Chibuike GU, Obiora SC (2014) Heavy Metal Polluted Soils: Effect on Plants and Bioremediation Methods. Appl Environ Soil Sci https://doi.org/10.1155/2014/752708

  • Dharmawardhana P, Brunner AM, Strauss SH (2010) Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genomics. https://doi.org/10.1186/1471-2164-11-150

  • Deng X, He J, He N (2013) Comparative study on Ni2+-affinity transport of nickel/cobalt permeases (NiCoTs) and the potential of recombinant Escherichia coli for Ni2+ bioaccumulation. Bioresour Technol 130:69–74

    Article  CAS  Google Scholar 

  • Diaz-Ravina M, Baath E (2001) Response of soil bacterial communities pre-exposed to different metals and reinoculated in an unpolluted soil. Soil Biol Biochem 33:241–248

    Article  CAS  Google Scholar 

  • Edalatifard L, Hammad SA, Sanavy M, Askari H (2014) The optimum condition under light and media for seed germination of Withania coagulans. Int J Farm Alli Sci 3(7):722–728

    Google Scholar 

  • Espen L, Pirovano L, Cocucci SM (1997) Effects of Ni2+ during the early phases of radish (Raphanus sativas) seed germination. Environ Exp Bot 38(2):187–197

    Article  CAS  Google Scholar 

  • Fargasova A (1994) Effect of Pb, Cd, Hg, As and Cr on germination and root growth of Sinapsis alba seeds. Bull Environ Contam Toxicol 52:452–456

    Article  CAS  Google Scholar 

  • Foster AJ, Pelletier G, Tanguay P, Séguin A (2015) Transcriptome analysis of poplar during leaf spot infection with Sphaerulina spp. PLOS ONE 10(9):0138162. https://doi.org/10.1371/journal.pone.0138162

    Article  CAS  Google Scholar 

  • Gabbrielli R, Pandolfini T, Espen L, Palandri MR (1999) Growth, peroxidase activity and cytological modifications in Pisum sativum seedlings exposed to Ni2+ toxicity. J Plant Physiol 155:639–645

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowka M (2008) Differential biochemical response of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul 54:179–188

    Article  CAS  Google Scholar 

  • Gomes-Filho E, Lima CFRM, Eneas-Filho J, Gondim LA, Prisco JT (1999) Purification and properties of a ribonuclease from cowpea cotyledons. Biol Plant 42:525–532

    Article  CAS  Google Scholar 

  • Hamrick JL, Linhart YB, Mitton JB (1979) Relationships between life history characteristics and electrophoretically detectable genetic variation in plants. Annu Rev Ecol Syst 10:173–200

    Article  Google Scholar 

  • Kalubi KN, Mehes-Smith M, Omri A (2016) Comparative analysis of metal translocation in red maple (Acer rubrum) and trembling aspen (Populus tremuloides) populations from stressed ecosystems contaminated with metals. Chem Ecol 32(4):312–323

    Article  CAS  Google Scholar 

  • Kalubi KN, Michael P, Omri A (2018) Analysis of gene expression in red maple (Acer rubrum) and trembling aspen (Populus tremuloides) populations from a mining region. Genes Genomics. https://doi.org/10.1007/s13258-018-0670-8

  • Kim RJ, Yoon JK, Kim TS, Yang J, Owens G, Kim KR (2015) Bioavailability of heavy metals in soils: definitions and practical implementation- a critical review. Environ Geochem Health 37(6):1041–1061

    Article  CAS  Google Scholar 

  • Kinniburgh DG, Milne CJ, Benedetti MF, Pinheiro JP, Filius J, Koopal LK, Van Riemsdijk WH (1996) Metal ion binding by humic acid: application of the Nica-Donnan Model. Environ Sci Technol 30:1687–1698

    Article  CAS  Google Scholar 

  • Kirchgessner M, Schnegg A (1979) Activty of proteases leucine arylamidase and alpha-amylase in pancreatic tissue during nickel deficiency. Nutr Metab 23(1):62–4

    Article  CAS  Google Scholar 

  • Kirkey FM, Matthews J, Ryser P (2012) Metal resistance in populations of red maple (Acer rubrum L.) and white birch (Betula papyrifera Marsh.) from a metal-contaminated region and neighbouring non-contaminated regions. Environ Pollut 164:53–58

    Article  CAS  Google Scholar 

  • Koné M, Koné T, Silué N, Soumahoro AB, Kouakou T (2015) In Vitro Seeds Germination and Seedling Growth of Bambara Groundnut (Vigna subterranea (L.) Verdc. (Fabaceae)). Sci World J. https://doi.org/10.1155/2015/595073

  • Leon V, Rabier J, Notonier R, Barthelemy R, Moreau X, Bouraima-Medjebi S, Viano J, Pineau R (2005) Effects of three nickel salts on germinating seeds of Grevillea exul var. rubiginosa, an endemic serpentine proteaceae. Ann Bot 95:609–618

    Article  CAS  Google Scholar 

  • Lin YC, Kao CH (2006) Effect of excess nickel on starch mobilization in germination rice grains. J Plant Nutr 29:1405–1412

    Article  CAS  Google Scholar 

  • Maheshwari R, Dubey R (2008) Inhibition of ribonuclease and proteases activities in germinating rice seeds exposed to nickel. Acta Physiol Plant 30(6):863–872

    Article  CAS  Google Scholar 

  • Maheshwari R, Dubey RS (2007) Nickel toxicity inhibits ribonuclease and protease activities in rice seeds exposed to nickel. Acta Physiol Plant 30(6):863–872

    Article  CAS  Google Scholar 

  • Mishra A, Choudhuri MA (1998) Amelioration of lead and mercury effects on germination and rice seedling growth by antioxidants. Biol Planta 41:469–473

    Article  CAS  Google Scholar 

  • Munzuroglu O, Geckil H (2002) Effects of metals on seed germination, root elongation, and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Arch Environ Contam Toxicol 43:203–213

    Article  CAS  Google Scholar 

  • Nkongolo KK, Narendrula-Kotha R, Kalubi K, Rainville S, Michael P (2017) High level of nickel tolerance and metal exclusion identified in silver maple (Acer saccharinum). Chem Ecol 33(9):795–806. https://doi.org/10.1080/02757540.2017.1376664

    Article  CAS  Google Scholar 

  • Palma JM, Sandalio LM, Corpas FJ, Romero-Puertas MC, McCarthy I, del Rio LA (2002) Plant protease, protein degradation, and oxidative stress: Role of peroxisomes. Plant Physiol Biochem 40:521–530

    Article  CAS  Google Scholar 

  • Pena LB, Tomaro ML, Gallego SM (2006) Effect of different metals on protease activity in sunflower cotyledons. Electron J Biotechnol 9:258–262

    Article  CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–36

    CAS  Google Scholar 

  • Qiu Q, Ma T, Hu Q, Liu B, Wu Y, Zhou H, Wang Q, Wang J, Liu J (2011) Genome-scale transcriptome analysis of the desert poplar Populus euphratica. Tree Physiol 31:452–461

    Article  Google Scholar 

  • Radwanski D, Gallagher F, Vanderklein DW, Schafer KVR (2017) Photosynthesis and aboveground carbon allocation of two co-occurring poplar species in an urban brownfield. Environ Pollut 223:497–506

    Article  CAS  Google Scholar 

  • Rao KVM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeon pea (Cajnus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP binding cassette transporters. J Bacteriol 188:317–327

    Article  CAS  Google Scholar 

  • Sfaxi-Bousbih A, Chaoui A, El Ferjani E (2010) Cadmium impairs mineral and carbohydrate mobilization during the germination of bean seeds. Ecotoxicol Environ Saf 73(6):1123–1129

    Article  CAS  Google Scholar 

  • Shim SI, Moon JC, Jang CS, Raymer P, Kim W (2008) Effect of potassium nitrate priming on seed germination of Seashore Paspalum. Hortscience 43(7):2259–2262

    Article  Google Scholar 

  • Taiz L, Zeiger E (2006) Plant Physiology, 4nd ed. Sinauer Associates, Inc, Sunderland, Massachusetts, p 103–122

    Google Scholar 

  • Theriault G, Nkongolo KK, Michael P (2015) Transcriptome analysis of nickel-resistant and susceptible Betula papyrifera genotypes. In: Proceedings of the annual meeting of American society of agronomy, crop sciences society of America, and soil sciences society of America held in Minneapolis, 16-19 November 2015

  • Theriault G, Michael P, Nkongolo KK (2016a) Comprehensive Transcriptome Analysis of Response to Nickel Stress in White Birch (Betula papyrifera). PLoS ONE 11(4):e0153762. https://doi.org/10.1371/journal.pone.0153762

    Article  CAS  Google Scholar 

  • Theriault G, Michael P, Nkongolo KK (2016b) Decrypting the regulation and mechanism of nickel resistance in white birch (Betula papyrifera) using cross-species metal-resistance genes. Genes Genom 38:341–350

    Article  CAS  Google Scholar 

  • Valko M, Morris H, Cronin MTD (2005) Metals: toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  CAS  Google Scholar 

  • Van den Ende W, Michiels A, Le Roy K, Van Laere A (2002) Cloning of a vacuolar invertase from Belgian endive leaves (Cichorium intybus). Physiol Plant 115:504–512

    Article  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q (2001) Activities of starch hydrolytic enzymes and sucrosephosphate synthase in the stems of rice subjected to water stress during grain filling. J Exp Bot 52:2169–2179

    Article  CAS  Google Scholar 

  • Yamauchi D (2003) Regulation of gene expression of a cysteine proteinase, EP-C1, by a VIVIPAROUS1-like factor from common bean. Plant Cell Physiol 44:649–652

    Article  CAS  Google Scholar 

  • Zhang H, Lian C, Shen Z (2009) Proteomic identification of small, copper-responsive proteins in germinating embryos of Oryza sativa. Ann Bot 103(6):923–930

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Natural Sciences and Engineering Council of Canada (NSERC). Thanks to Dr. Gabriel Theriault and Mrs. Charnelle Djeukam for technical assistance.

Author information

Authors and Affiliations

  1. Department of Biology, Laurentian University, Sudbury, Ontario, P3E 2C6, Canada

    Karolina M. Czajka & Kabwe Nkongolo

  2. Biomolecular Sciences Program, Laurentian University, Sudbury, Ontario, P3E 2C6, Canada

    Paul Michael & Kabwe Nkongolo

Authors
  1. Karolina M. Czajka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Michael
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kabwe Nkongolo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kabwe Nkongolo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human subjects or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Czajka, K.M., Michael, P. & Nkongolo, K. Differential effects of nickel dosages on in vitro and in vivo seed germination and expression of a high affinity nickel-transport family protein (AT2G16800) in trembling aspen (Populus tremuloides). Ecotoxicology 28, 92–102 (2019). https://doi.org/10.1007/s10646-018-2003-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-2003-8

Keywords

Search

Navigation