Skip to main content
Log in

Low Cd concentration-activated morphogenic defence responses are inhibited by high Cd concentration-induced toxic superoxide generation in barley root tip

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Exposure of roots to low Cd concentration induced morphogenic responses including the inhibition of root growth and the radial swelling of root tip. High Cd concentrations within a few minutes caused a robust induction of superoxide generation leading to the cell death and root growth arrest. This toxic superoxide generation blocked the development of low Cd concentration-activated morphogenic responses. While the morphogenic responses of roots to low Cd concentration are induced very rapidly and probably due to the interaction of Cd with the apoplast of root tissue, high Cd concentration-induced superoxide production required the entry of Cd into the symplast. Auxin signaling is involved in the activation of Cd-induced morphogenic defence responses but not in the Cd-induced toxic superoxide generation. These results suggest that oxidative stress is not a primary cause for the Cd-induced morphogenic responses such as growth reduction and radial cell expansion in barley root tips.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

NBT:

Nitro-blue tetrazolium chloride

PCIB:

p-Chlorophenoxyisobutyric acid

ROS:

Reactive oxygen species

SIMR:

Stress-induced morphogenic response

References

  • Ali S, Bai P, Zeng F, Cai S, Shamsi IH, Qiu B, Wu F, Zhang G (2011) The ecotoxicological and interactive effects of chromium and aluminium on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance. Environ Exp Bot 70:185–191

    Article  CAS  Google Scholar 

  • Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser M-T, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bočová B, Mistrík I, Pavlovkin J, Tamás L (2012) Cadmium disrupts apoplastic ascorbate redox status in barley root tips. Acta Physiol Plant 34:2297–2302

    Article  CAS  Google Scholar 

  • Bohnert HJ, Sheveleva E (1998) Plant stress adaptations—making metabolism move. Curr Opin Plant Biol 1:267–274

    Article  PubMed  CAS  Google Scholar 

  • Cabot C, Gallego B, Martos S, Barceló J, Poschenrieder C (2013) Signal cross talk in Arabidopsis exposed to cadmium, silicon, and Botrytis cinerea. Planta 237:337–349

    Article  PubMed  CAS  Google Scholar 

  • Cutler JM, Rains DW (1974) Characterization of cadmium uptake by plant tissue. Plant Physiol 54:67–71

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56:1213–1220

    Article  PubMed  CAS  Google Scholar 

  • Fujimaki S, Suzui N, Ishioka NS, Kawachi N, Ito S, Chino M, Nakamura S (2010) Tracing cadmium from culture to spikelet: noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol 152:1796–1806

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fusconi A, Gallo C, Camusso W (2007) Effects of cadmium on root apical meristems of Pisum sativum L.: cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution. Mutat Res 632:9–19

    Article  PubMed  CAS  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 

  • Garnier L, Simon-Plas F, Thuleau P, Agnel J-P, Blein J-P, Ranjeva R, Montillet J-L (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29:1956–1969

    Article  PubMed  CAS  Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Func Plant Biol 32:481–494

    Article  CAS  Google Scholar 

  • Inouhe M, Ninomiya S, Tohoyama H, Joho M, Murayama T (1994) Different characteristics of roots in the cadmium-tolerance and Cd-binding complex formation between mono- and dicotyledonous plants. J Plant Res 107:201–207

    Article  CAS  Google Scholar 

  • Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856

    Article  PubMed  CAS  Google Scholar 

  • Kawano T, Kawano N, Muto S, Lapeyrie F (2002) Retardation and inhibition of the cation-induced superoxide generation in BY-2 tobacco cell suspension culture by Zn2+ and Mn2+. Physiol Plant 114:395–404

    Article  PubMed  CAS  Google Scholar 

  • Kevrešan S, Kiršek S, Kandrač J, Petrović N, Kelemen DJ (2003) Dynamics of cadmium distribution in the intercellular space and inside cells in soybean roots, stems and leaves. Biol Plant 46:85–88

    Article  Google Scholar 

  • Kovács E, Nyitrai P, Czövek P, Óvári M, Keresztes Á (2009) Investigation into the mechanism of stimulation by low-concentration stressors in barley seedlings. J Plant Physiol 166:72–79

    Article  PubMed  CAS  Google Scholar 

  • Lenzen S (2008) The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetes 51:216–226

    CAS  Google Scholar 

  • Liptáková Ľ, Bočová B, Huttová J, Mistrík I, Tamás L (2012) Superoxide production induced by short-term exposure of barley roots to cadmium, auxin, alloxan and sodium dodecyl sulfate. Plant Cell Rep 31:2189–2197

    Article  PubMed  CAS  Google Scholar 

  • Maltais K, Houde M (2002) A new biochemical marker for aluminium tolerance in plants. Physiol Plant 115:81–86

    Article  PubMed  CAS  Google Scholar 

  • Navascués J, Pérez-Rontomé C, Sánchez DH, Staudinger C, Wienkoop S, Rellán-Álvarez R, Becana M (2012) Oxidative stress is a consequence, not a cause, of aluminum toxicity in the forage legume Lotus corniculatus. New Phytol 193:625–636

    Article  PubMed  CAS  Google Scholar 

  • Ortega-Villasante C, Hernández LE, Rellán-Álvarez R, Del Campo FF, Carpena-Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176:96–107

    Article  PubMed  CAS  Google Scholar 

  • Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environ Geochem Health 32:1–12

    Article  PubMed  CAS  Google Scholar 

  • Panou-Filotheou H, Bosabalidis AM (2004) Root structural aspects associated with copper toxicity in oregano (Origanum vulgare subsp. hirtum). Plant Sci 166:1497–1504

    Article  CAS  Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Jansen MAK (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169

    Article  PubMed  Google Scholar 

  • Rangel AF, Rao IM, Horst WJ (2007) Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminium resistance. J Exp Bot 58:3895–3904

    Article  PubMed  CAS  Google Scholar 

  • Rascio N, Vecchia FD, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv.Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62:267–278

    Article  CAS  Google Scholar 

  • Rucińska R, Walpak S, Gwóźdź EA (1999) Free radical formation and activity of antioxidant enzymes in lupin roots exposed to lead. Plant Physiol Biochem 37:187–194

    Article  Google Scholar 

  • Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Sharma SS, Dietz K-J (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    Article  PubMed  CAS  Google Scholar 

  • Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol 116:155–163

    Article  CAS  PubMed Central  Google Scholar 

  • Tamás L, Mistrík I, Huttová J, Halušková Ľ, Valentovičová K, Zelinová V (2010) Role of reactive oxygen species-generating enzymes and hydrogen peroxide during cadmium, mercury and osmotic stresses in barley root tip. Planta 231:221–231

    Article  PubMed  CAS  Google Scholar 

  • Tamás L, Bočová B, Huttová J, Liptáková Ľ, Mistrík I, Valentovičová K, Zelinová V (2012) Impact of the auxin signaling inhibitor p-chlorophenoxyisobutyric acid on short-term Cd-induced hydrogen peroxide production and growth response in barley root tip. J Plant Physiol 169:1375–1381

    Article  PubMed  CAS  Google Scholar 

  • Tognetti VB, Mühlenbock P, Van Breusegem F (2012) Stress homeostasis—the redox and auxin perspective. Plant Cell Environ 35:321–333

    Article  PubMed  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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

We wish to thank Margita Vašková for excellent technical assistance. This work was supported by the Grant Agency VEGA, Project No. 2/0019/13.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ladislav Tamás.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tamás, L., Mistrík, I. & Alemayehu, A. Low Cd concentration-activated morphogenic defence responses are inhibited by high Cd concentration-induced toxic superoxide generation in barley root tip. Planta 239, 1003–1013 (2014). https://doi.org/10.1007/s00425-014-2030-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2030-5

Keywords

Navigation