Skip to main content
SpringerLink
Log in

Intra-specific variability in the response of maize to arsenic exposure

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The response of maize (Zea mays L.) to inorganic arsenic exposure was studied, at the seedling stage under hydroponic conditions, preliminarily in sixteen lines (fourteen hybrids and two inbred lines) and then, more deeply, in six of these lines, selected by showing contrasting differences in their sensitivity to the metalloid. The results indicated that (i) maize is rather tolerant to arsenic toxicity, (ii) arsenite is more phytotoxic than arsenate, (iii) roots are less sensitive than shoots to the metalloid, (iv) a great accumulation of non-protein thiols (probably phytochelatins), without substantial effect on the glutathione content, is produced in roots but not in shoots of arsenic-exposed plants and (v) maize is able to accumulate high levels of arsenic in roots with very low translocation to shoots. The study, thus, suggests that maize, for its very low rate of acropetal transport of arsenic from roots to shoots, may be a safe crop in relation to the risk of entry of metalloid in the food chain and, for being an important bioenergy crop capable of expressing high levels of arsenic tolerance and accumulation in roots, may represent an interesting opportunity for the exploitation of agricultural useless arsenic contaminated lands.

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

Similar content being viewed by others

Abbreviations

As(V):

Arsenate

As(III):

Arsenite

DTNB:

5,5′-Dithiobis(2-nitrobenzoic acid)

DW:

Dry weight

EC50 :

Effective concentration that inhibits plant growth by 50 %

FW:

Fresh weight

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

iAs:

Inorganic arsenic

NPTs:

Non-protein thiols

ONPTs:

Other non-protein thiols different to GSH

PCs:

Phytochelatins

RAI:

Root absorption index

RTI STI and WPTI:

Root, shoot and whole-plant tolerance index, respectively

References

  • Abedin MJ, Meharg AA (2002) Relative toxicity of arsenite and arsenate on germination and early seedling growth of rice (Oryza sativa L.). Plant Soil 243:57–66

    Article  CAS  Google Scholar 

  • Abedin MJ, Cotter-Howells J, Meharg AA (2002) Arsenic uptake and accumulation in rice (Oryza sativa L.) irrigated with contaminated water. Plant Soil 240:311–319

    Article  CAS  Google Scholar 

  • Ahsan N, Lee DG, Alam IA, Kim PJ, Lee JJ, Ahn YO, Kwak SS, Lee IJ, Bahk JD, Kang KY, Renaut J, Komatsu S, Lee BH (2008) Comparative proteomic study of arsenic-induced differentially expressed proteins in rice roots reveals glutathione plays a central role during As stress. Proteomics 8:3561–3576

    Article  CAS  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–554

    Article  CAS  Google Scholar 

  • Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257

    CAS  Google Scholar 

  • Carbonell-Barrachina AA, Aarabi MA, DeLaune RD, Gambrell RP, Patrick WH Jr (1998) The influence of arsenic chemical form and concentration on Spartina patens and Spartina alterniflora growth and tissue arsenic concentration. Plant Soil 198:33–43

    Article  CAS  Google Scholar 

  • Ci XK, Liu HL, Hao YB, Zhang JW, Liu P, Dong ST (2012) Arsenic distribution, species, and its effect on maize growth treated with arsenate. J Integr Agric 11:416–423

    Article  CAS  Google Scholar 

  • Cullen WR, Reimer KJ (1989) Arsenic speciation in the environment. Chem Rev 89:713–764

    Article  CAS  Google Scholar 

  • De Vos CHR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853–858

    Article  Google Scholar 

  • Dhankher OP (2005) Arsenic metabolism in plants: an inside story. New Phytol 168:503–505

    Article  CAS  Google Scholar 

  • Drlicková G, Vaculík M, Matejkovic P, Lux A (2013) Bioavailability and toxicity of arsenic in maize (Zea mays L.) grown in contaminated soils. Bull Environ Contam Toxicol 91:235–239

    Article  Google Scholar 

  • Gong JM, Lee DA, Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatin and cadmium. Proc Natl Acad Sci U S A 100:10118–10123

    Article  CAS  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  CAS  Google Scholar 

  • Gulz PA, Gupta SK, Schulin R (2005) Arsenic accumulation of common plants from contaminated soils. Plant Soil 272:337–347

    Article  CAS  Google Scholar 

  • Kocsy G, von Ballmoos P, Suter M, Rüegsegger A, Galli U, Szalai G, Galiba G, Brunold C (2000) Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211:528–536

    Article  CAS  Google Scholar 

  • Kocsy G, von Ballmoos P, Rüegsegger A, Szalai G, Galiba G, Brunold C (2001) Increasing the glutathione content in a chilling-sensitive maize genotype using safeners increased protection against chilling-induced injury. Plant Physiol 127:1147–1156

    Article  CAS  Google Scholar 

  • Liu ZH, Li WH, Qi HY, Song GL, Ding D, Fu ZY, Liu JB, Tang JH (2012) Arsenic accumulation and distribution in the tissues of inbred lines in maize (Zea mays L.). Genet Res Crop Evol 59:1705–1711

    Article  CAS  Google Scholar 

  • Lubin JH, Beane Freeman LE, Cantor KP (2007) Inorganic arsenic in drinking water: an evolving public health concern. J Natl Cancer Inst 99:906–907

    Article  CAS  Google Scholar 

  • Marin AR, Masscheleyn PH, Patrick WH Jr (1992) The influence of chemical form and concentration of arsenic on rice growth and tissue arsenic concentration. Plant Soil 139:175–183

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids, and radionuclides. Adv Agron 75:1–56

    Article  CAS  Google Scholar 

  • Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Reduction and coordination of arsenic in Indian mustard. Plant Physiol 122:1171–1177

    Article  CAS  Google Scholar 

  • Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol 114:695–704

    CAS  Google Scholar 

  • Porter EK, Peterson PJ (1977) Arsenic tolerance in grasses growing on mine waste. Environ Pollut 14:255–265

    Article  CAS  Google Scholar 

  • Raab A, Feldmann J, Meharg AA (2005) Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annus): formation of arsenic-phytochelatin complexes during exposure to high arsenic concentrations. New Phytol 168:551–558

    Article  CAS  Google Scholar 

  • Rahman MA, Hsegawa H, Rahman MM, Islam MN, Miah MAM, Tasmen A (2007) Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere 67:1072–1079

    Article  CAS  Google Scholar 

  • Requejo R, Tena M (2005) Proteome analysis of maize roots reveals that oxidative stress is a main contributing factor to plant arsenic toxicity. Phytochemistry 66:1519–1528

    Article  CAS  Google Scholar 

  • Requejo R, Tena M (2012) Influence of glutathione chemical effectors in the response of maize to arsenic exposure. J Plant Physiol 169:649–653

    Article  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  CAS  Google Scholar 

  • Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392

    Article  CAS  Google Scholar 

  • Schmöger MEV, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–801

    Article  Google Scholar 

  • Schröder P, Herzig R, Bojinov B, Ruttens A, Nehnevajova E, Stamatiadis S, Memon A, Vassilev A, Caviezel M, Vangronsveld J (2008) Bioenergy to save the world – Producing novel energy plants for growth on abandoned land. Environ Sci Pollut Res 15:196–204

    Article  Google Scholar 

  • Schulz H, Härtling S, Tanneberg H (2008) The identification and quantification of arsenic-induced phytochelatins – comparison between plants with varying As sensitivities. Plant Soil 303:275–287

    Article  CAS  Google Scholar 

  • Smith E, Naidu R, Alston AM (1998) Arsenic in the soil environment: a review. Adv Agron 64:149–195

    Article  CAS  Google Scholar 

  • Sneller FEC, Van Heerwaarden LM, Kraaijeveld-Smit FJL, Ten Bookum WM, Koevoets PLM, Schat H, Verkleij JAC (1999) Toxicity of arsenate in Silene vulgaris, accumulation and degradation of arsenate-induced phytochelatins. New Phytol 144:223–232

    Article  CAS  Google Scholar 

  • Stoeva N, Berova M, Zlatev Z (2003) Physiological response of maize to arsenic contamination. Biol Plant 47:449–452

    Article  CAS  Google Scholar 

  • Vázquez S, Esteban E, Goldsbrough P (2005) Arsenate-induced phytochelatins in white lupin: influence of phosphate status. Physiol Plant 124:42–50

    Google Scholar 

  • Wang J, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. Plant Physiol 130:1552–1561

    Article  CAS  Google Scholar 

  • Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ, Feldman J, Meharg AA (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859

    Article  CAS  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research has been supported by the Spanish Science and Technology Ministry (Project REN2003-03843/TECNO) and Andalusia (Spain) Regional Government (PAI Group AGR 164). The authors thank Alberto Ojembarrena (Pioneer Hi-Bred Spain) and Cindy Leveque (Pioneer Génétique France), and Prof Peter Stamp and Dr Jörg Leipner (Institute for Plant Sciences, ETH Zürich) for providing seeds of the maize hybrids and inbred lines, respectively.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, ETSIAM, University of Córdoba, Edif. Severo Ochoa, Campus de Rabanales, 14071, Córdoba, Spain

    Raquel Requejo & Manuel Tena

Authors
  1. Raquel Requejo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel Tena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel Tena.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Requejo, R., Tena, M. Intra-specific variability in the response of maize to arsenic exposure. Environ Sci Pollut Res 21, 10574–10582 (2014). https://doi.org/10.1007/s11356-014-3097-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3097-z

Keywords

Search

Navigation