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Kinetics of metal toxicity in plant roots and its effects on root morphology

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Abstract

Aims

Elevated levels of metals reduce plant growth, including contaminated, acid, and saline soils, but much remains unknown regarding their mechanisms of toxicity. In this regard, it is important to understand the kinetics of changes in root elongation rate (RER) and root morphology.

Methods

Seedlings of soybean (Glycine max) were grown in solutions containing toxic levels of one of seven metals that differed markedly in their properties (Ag, Al, Ca, Cu, Hg, Na, and Sr), with mannitol and ‘mixed salts’ treatments also included.

Results

Despite their widely differing properties, all treatments caused similar symptoms, with roots swelling radially within the elongation zone, possibly associated with ethylene or auxin. In addition, Ag, Al, Cu, and Hg caused a rupturing of the outer root tissues likely associated with inhibition of wall loosening. Finally, using kinematic analyses to examine the effects of Hg in 5 min intervals, it was found that RER decreased by 50% after only 40 min, primarily associated with a decrease in the rate at which individual cells were elongating.

Conclusions

The information provided here will assist in understanding the mechanisms by which toxic levels of metals reduce root elongation.

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Abbreviations

LEZ:

Length of the elongation zone

MEER:

Maximum elemental elongation rate

RER:

Root elongation rate

References

  • Alarcon MV, Lloret PG, Salguero J (2013) Auxin-ethylene interaction in transversal and longitudinal growth in maize primary root. Botany 91:680–685

    Article  CAS  Google Scholar 

  • Barceló J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92

    Article  Google Scholar 

  • Baskin TI (2013) Patterns of root growth acclimation: constant processes, changing boundaries. Wiley Interdiscip Rev Dev Biol 2:65–73

    Article  CAS  PubMed  Google Scholar 

  • Basu P, Pal A, Lynch JP, Brown KM (2007) A novel image-analysis technique for kinematic study of growth and curvature. Plant Physiol 145:305–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blamey FPC, Nishizawa NK, Yoshimura E (2004) Timing, magnitude, and location of initial soluble aluminium injuries to mungbean roots. Soil Sci Plant Nutr 50:67–76

    Article  CAS  Google Scholar 

  • Blamey FPC, Kopittke PM, Wehr JB, Kinraide TB, Menzies NW (2010) Rhizotoxic effects of silver in cowpea seedlings. Environ Toxicol Chem 29:2072–2078

    CAS  PubMed  Google Scholar 

  • Blancaflor EB, Jones DL, Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol 118:159–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, Inzé D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640

    Article  CAS  PubMed  Google Scholar 

  • Cramer GR, Epstein E, Läuchli A (1988) Kinetics of root elongation of maize in response to short-term exposure to NaCl and elevated calcium concentration. J Exp Bot 39:1513–1522

    Article  CAS  Google Scholar 

  • Eswaran H, Reich P, Beinroth F (1997) Global distribution of soils with acidity. In: Plant-soil interactions at low pH. Ed. A C Moniz. Brazilian Soil Science Society, Sao Paulo, pp 159–164

    Google Scholar 

  • Ghassemi F, Jakeman A J, Nix H A (1995) Salinisation of land and water resources: human causes, extent, management and case studies. Canberra, Australia: the Australian National University, Wallingford, Oxon, UK: CAB international. CAB International, Wallingford pp. 544

  • Jones DL, Kochian LV (1995) Aluminum inhibition of the inositol 1,4,5-trisphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity? Plant Cell 7:1913–1922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29:1309–1318

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB (1988) Proton extrusion by wheat roots exhibiting severe aluminum toxicity symptoms. Plant Physiol 88:418–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinraide TB (2009) Improved scales for metal ion softness and toxicity. Environ Toxicol Chem 28:525–533

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB, Yermiyahu U (2007) A scale of metal ion binding strengths correlating with ionic charge, Pauling electronegativity, toxicity, and other physiological effects. J Inorg Biochem 101:1201–1213

    Article  CAS  PubMed  Google Scholar 

  • Kopittke PM, Blamey FPC, Menzies NW (2008) Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root cortical cells of cowpea. Plant Soil 303:217–227

    Article  CAS  Google Scholar 

  • Kopittke PM, McKenna BA, Blamey FPC, Wehr JB, Menzies NW (2009) Metal-induced cell rupture in elongating roots is associated with metal ion binding strengths. Plant Soil 322:303–315

    Article  CAS  Google Scholar 

  • Kopittke PM, Blamey FPC, Kinraide TB, Wang P, Reichman SM, Menzies NW (2011) Separating multiple, short-term deleterious effects of saline solutions to the growth of cowpea seedlings. New Phytol 189:1110–1121

    Article  CAS  PubMed  Google Scholar 

  • Kopittke PM, Menzies NW, Wang P, McKenna BA, Wehr JB, Lombi E, Kinraide TB, Blamey FPC (2014) The rhizotoxicity of metal cations is related to their strength of binding to hard ligands. Environ Toxicol Chem 33:268–277

    Article  CAS  PubMed  Google Scholar 

  • Kopittke PM, Moore KL, Lombi E, Gianoncelli A, Ferguson BJ, Blamey FPC, Menzies NW, Nicholson TM, McKenna BA, Wang P, Gresshoff PM, Kourousias G, Webb RI, Green K, Tollenaere A (2015) Identification of the primary lesion of toxic aluminum (Al) in plant roots. Plant Physiol 167:1402–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Yang JL, He LS, Li YY, Zheng SJ (2008) Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biol Plantarum 52:87–92

    Article  CAS  Google Scholar 

  • Llugany M, Poschenrieder C, Barceló J (1995) Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity. Physiol Plant 93:265–271

    Article  CAS  Google Scholar 

  • Massot N, Nicander B, Barcelo J, Poschenrieder C, Tillberg E (2002) A rapid increase in cytokinin levels and enhanced ethylene evolution precede Al3+-induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.) Plant Growth Regul 37:105–112

    Article  CAS  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto H, Motoda H (2012) Aluminum toxicity recovery processes in root apices. Possible association with oxidative stress. Plant Sci 185–186:1–8

    Article  PubMed  Google Scholar 

  • Munns R, Termaat A (1986) Whole-plant responses to salinity. Aust J Plant Physiol 13:143–160

    Article  Google Scholar 

  • NLWRA (2002) Australians and natural resource management, http://www.nlwra.gov.au/. National Land and Water Resources Audit, Canberra

  • Osawa H, Endo I, Hara Y, Matsushima Y, Tange T (2011) Transient proliferation of proanthocyanidin-accumulating cells on the epidermal apex contributes to highly aluminum-resistant root elongation in camphor tree. Plant Physiol 155:433–446

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Parker DR (1995) Root growth analysis: an underutilised approach to understanding aluminium rhizotoxicity. Plant Soil 171:151–157

    Article  CAS  Google Scholar 

  • Pierik R, Verkerke W, Voesenek RACJ, Blom KWPM, Visser EJW (1999) Thick root syndrome in cucumber (Cucumis sativus L.): a description of the phenomenon and an investigation of the role of ethylene. Ann Bot 84:755–762

    Article  CAS  Google Scholar 

  • Sasaki M, Yamamoto Y, Matsumoto H (1996) Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiolgia Plantar 96:193–198

    Article  CAS  Google Scholar 

  • Sasaki M, Yamamoto Y, Ma JF, Matsumoto H (1997) Early events induced by aluminum stress in elongating cells of wheat root. Soil Sci Plant Nutr 43:1009–1014

    Article  CAS  Google Scholar 

  • Sheldon AR, Menzies NW (2005) The effect of copper toxicity on the growth and root morphology of Rhodes grass (Chloris gayana Knuth.) in resin buffered solution culture. Plant Soil 278:341–349

    Article  CAS  Google Scholar 

  • Valentovičová K, Mistrík I, Zelinová V, Tamás L (2012) How cobalt facilitates cadmium- and ethylene precursor-induced growth inhibition and radial cell expansion in barley root tips. Cent Eur J Biol 7:551–558

    Google Scholar 

  • Veitch FP (1904) Comparison of methods for the estimation of soil acidity. J Am Chem Soc 26:637–662

    Article  Google Scholar 

  • Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2010) Under pressure, cell walls set the pace. Trends Plant Sci 15:363–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zelinova V, Haluskova L, Huttova J, Illes P, Mistrik I, Valentovicova K, Tamas L (2011) Short-term aluminium-induced changes in barley root tips. Protoplasma 248:523–530

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Dr. Kopittke is the recipient of an Australian Research Council (ARC) Future Fellowship (FT120100277).

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Correspondence to Peng Wang.

Additional information

Responsible Editor: Juan Barcelo.

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Supplementary Video S1

A time-lapse video compiled from the kinematic analysis (Experiment 3) showing the growth of soybean roots in a solution containing 1 μM Hg, with a radial swelling forming. The video represents the period from 447 to 745 min after initially exposing the root to Hg. (AVI 10987 kb)

Supplementary Video S2

A time-lapse video compiled showing the growth of soybean roots in a solution containing 1 μM NPA, with a radial swelling forming. The video represents the period from 564 to 764 min after initially exposing the root to NPA. (AVI 8393 kb)

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Kopittke, P.M., Wang, P. Kinetics of metal toxicity in plant roots and its effects on root morphology. Plant Soil 419, 269–279 (2017). https://doi.org/10.1007/s11104-017-3342-6

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