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Arsenic Toxicity in Crop Plants: Approaches for Stress Resistance

  • Alok Krishna SinhaEmail author
  • Dhammaprakash Pandahri Wankhede
  • Meetu Gupta
Chapter

Abstract

Heavy metals have been consistent source of environmental pollution. Among all the heavy metals, arsenic (As), a non-essential element for plants, is one of the major pollutants affecting human life. Arsenic exists in three major forms, arsenate (AsV), arsenite (ASIII) and as methylated species. These forms are taken up by different mechanism and mobilized inside the plants. The causes of arsenic toxicity are mainly due to interference in ATP synthesis and alteration in protein structure and catalytic properties. Plants detoxify arsenic largely by complexation with phytochelatins and/or vacuolar sequestration. Existence of genetic variation in different germplasm of crop cultivars with respect to arsenic accumulation offers hope for classical breeding strategies to develop arsenic-tolerant crop cultivars. In this chapter, along with how arsenic is being taken up and metabolized inside the plants, we also discuss the different ways of detoxification of this major heavy metal pollutant.

Keywords

Arsenic toxicity Crop productivity Genetic engineering Plant breeding Stress resistance 

References

  1. Abbas MHH, Meharg AA (2008) Arsenate, arsenite and dimethyl arsenic acid (DMA) uptake and tolerance in maize (Zea mays L). Plant and Soil 304:277–289CrossRefGoogle Scholar
  2. Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128PubMedCrossRefGoogle Scholar
  3. Ahsan N, Lee DG, Alam I et al. (2008) Comparative proteomic study of arsenic-induced differentially expressed proteins in rice roots reveals glutathione plays a central role during As stress. Proteomics 8:3561–3576PubMedCrossRefGoogle Scholar
  4. Asher CJ, Reay PF (1979) Arsenic uptake by barley seedlings. Aust J Plant Physiol 6:459–466CrossRefGoogle Scholar
  5. Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: Arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271PubMedCrossRefGoogle Scholar
  6. Bhattacharjee H, Rosen BP (2007) Arsenic metabolism in prokaryotic and eukaryotic microbes. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals. Springer-Verlag, Berlin, Germany, pp 371–406CrossRefGoogle Scholar
  7. Bienert GP, Thorsen M, Schüssler MD et al. (2008) A subgroup of plant aquaporins facilitate the bidirectional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biology 6:26PubMedCrossRefGoogle Scholar
  8. Bleeker PM, Hakvoort HWJ, Bliek M et al. (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J 45:917–929PubMedCrossRefGoogle Scholar
  9. Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173:11–26PubMedCrossRefGoogle Scholar
  10. Catarecha P, Segura MD, Franco-Zorrilla JM et al. (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133PubMedCrossRefGoogle Scholar
  11. Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: Recent advances and new possibilities. Environ Sci Technol 39:9377–9390PubMedCrossRefGoogle Scholar
  12. Dasgupta T, Hossain SA, Meharg AA, Price AH (2004) An arsenate tolerance gene on chromosome 6 of rice. New Phytologist 163:45–49CrossRefGoogle Scholar
  13. Delnomdedieu M, Basti MM, Otvos JD, Thomas DJ (1994) Reduction and binding of arsenate and dimethylarsinate by glutathione–a magnetic resonance study. Chem Biol Interact 90:139–155PubMedCrossRefGoogle Scholar
  14. Dhankher OP, Li YJ, Rosen BP et al. (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145PubMedCrossRefGoogle Scholar
  15. Dhankher OP, Rosen BP, McKinney EC, Meagher RB (2006) Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase (ACR2). Proc Natl Acad Sci USA 103;5413–5418PubMedCrossRefGoogle Scholar
  16. Duan GL, Zhou Y, Tong YP et al. (2007) A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 174:311–321PubMedCrossRefGoogle Scholar
  17. Ellis DR, Gumaelius L, Indriolo E et al. (2006) A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol 141:1544–1554PubMedCrossRefGoogle Scholar
  18. Francesconi KA, Kuehnelt D (2002) Arsenic compounds in the environment. In: Frankenberger JWT (ed) Environmental chemistry of arsenic. Marcel Dekker, New York, NY, USA, pp 51–94Google Scholar
  19. Ghosh M, Shen J, Rosen BP (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96:5001–5006PubMedCrossRefGoogle Scholar
  20. Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential responses of arsenic stress in two varieties of Brassica juncea. Chemosphere 74:1201–1208Google Scholar
  21. González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) PHOSPHATETRANSPORTERTRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500–3512Google Scholar
  22. Ha SB, Smith AP, Howden R et al. (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1163Google Scholar
  23. Hartly-Whitakar J, Ainsworth G, Meharg AA (2001) Copper- and arsenate-induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ 24:713–722CrossRefGoogle Scholar
  24. Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133:1–16PubMedCrossRefGoogle Scholar
  25. Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582:1625–1628Google Scholar
  26. Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants. 3rd Edn. CRC Press, Boca Raton, FLGoogle Scholar
  27. Landrieu I, da Costa M, De Veylder L et al. (2004) A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:13380–13385Google Scholar
  28. Landrieu I, Hassan S, Sauty M et al. (2004) Characterization of the Arabidopsis thaliana Arath;CDC25 dual-specificity tyrosine phosphatase. Biochem Biophys Res Commun 322:734–739Google Scholar
  29. Li Y, Dankher OP, Carreira L et al. (2006) The shoot-specific expression of gamma-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiol 141:288–298PubMedCrossRefGoogle Scholar
  30. Li Y, Dhankher O, Carreira L et al. (2005) Engineered overexpression of g-glutamylcysteine synthetase in plants confers high level arsenic and mercury tolerance. Environ Toxicol Chem 24:1376–1386PubMedCrossRefGoogle Scholar
  31. Li YJ, Dhankher OP, Carreira L et al. (2004) Overexpression of phytochelatin synthase in Arabidopsis leads to enhanced arsenic tolerance and cadmium hypersensitivity. Plant Cell Physiol 45:1787–1797Google Scholar
  32. Liu WJ, Zhu YG, Hu Y et al. (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L). Environ Sci Technol 40:5730–5736PubMedCrossRefGoogle Scholar
  33. Liu ZJ, Boles E, Rosen BP (2004) Arsenic trioxide uptake by hexose permeases in Saccharomyces cerevisiae. J Biol Chem 279:17312–17318PubMedCrossRefGoogle Scholar
  34. Lombi E, Zhao FJ, Fuhrmann M et al. (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol 156:195–203CrossRefGoogle Scholar
  35. Ma JF, Yamaji N, Mitani N et al. (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935PubMedCrossRefGoogle Scholar
  36. Ma LQ, Komar KM, Tu C et al. (2001) A fern that hyperaccumulates arsenic. Nature 409:579–579PubMedCrossRefGoogle Scholar
  37. Meharg AA, Naylor J, Macnair MR (1994) Phosphorus nutrition of arsenate tolerant and nontolerant phenotypes of velvet grass. J Environ Qual 23:234–238CrossRefGoogle Scholar
  38. Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytologist 154:29–43CrossRefGoogle Scholar
  39. Mei XQ, Ye ZH, Wong MH (2009) The relationship of root porosity and radial oxygen loss on arsenic tolerance and uptake in rice grains and straw. Environ Pollut 157:2550–2557PubMedCrossRefGoogle Scholar
  40. Mendoza-Cózatl DG, Butko E, Springer F et al. (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259Google Scholar
  41. Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562PubMedCrossRefGoogle Scholar
  42. Mihucz VG, Tatar E, Virag I et al. (2005) Arsenic speciation in xylem sap of cucumber (Cucumis sativus L.). Anal Bioanal Chem 383:461–466PubMedCrossRefGoogle Scholar
  43. Mylona PV, Polidoros AN, Scandalios JG (1998) Modulation of antioxidant responses by arsenic in maize. Free Radic Biol Med 25:576–585PubMedCrossRefGoogle Scholar
  44. Nissen P, Benson AA (1982) Arsenic metabolism in fresh-water and terrestrial plants. Physiol Plant 54:446–450CrossRefGoogle Scholar
  45. Norton GJ, Lou-Hing DE, Meharg AA, Price AH (2008a) Rice-arsenate interactions in hydroponics: Whole genome transcriptional analysis. J Exp Bot 59:2267–2276CrossRefGoogle Scholar
  46. Norton GJ, Nigar M, Williams PN et al. (2008b) Rice-arsenate interactions in hydroponics: A three-gene model for tolerance. J Exp Bot 59:2277–2284CrossRefGoogle Scholar
  47. Norton GJ, Islam MR, Deacon CM et al. (2009) Identification of low inorganic and total grain arsenic rice cultivars from Bangladesh. Environ Sci Technol 43:6070–6075PubMedCrossRefGoogle Scholar
  48. Nriagu JO (2002) In: Frankenberger JWT (ed) Arsenic poisoning through the ages. Environmental chemistry of arsenic. Marcel Dekker, New York, NY, USA pp 1–26Google Scholar
  49. Picault, N. Cazalé AC, Beyly A et al. (2006) Chloroplast targeting of phytochelatin synthase in Arabidopsis: Effects on heavy metal tolerance and accumulation. Biochimie 88:1743–1750Google Scholar
  50. Pickering IJ, Gumaelius L, Harris HH et al. (2006) Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol 40:5010–5014PubMedCrossRefGoogle Scholar
  51. Qin J, Rosen BP, Zhang Y et al. (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci USA 103:2075–2080PubMedCrossRefGoogle Scholar
  52. Qin J, Lehr CR, Yuan CG et al. (2009) Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci USA 106:5213–5217PubMedCrossRefGoogle Scholar
  53. Quaghebeur M, Rengel Z (2003) The distribution of arsenate and arsenite in shoots and roots of Holcus lanatus is influenced by arsenic tolerance and arsenate and phosphate supply. Plant Physiol 132:1600–1609PubMedCrossRefGoogle Scholar
  54. Raab A, Williams PN, Meharg A, Feldmann J (2007a) Uptake and translocation of inorganic and methylated arsenic species by plants. Environ Chem 4:197–203CrossRefGoogle Scholar
  55. Raab A, Wright SH, Jaspars M et al. (2007b) Pentavalent arsenic can bind to biomolecules. Angew Chemie Int Ed 46:2594–2597CrossRefGoogle Scholar
  56. Rao KP, Vani G, Kumar K et al. (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82PubMedCrossRefGoogle Scholar
  57. Rathinasabapathi B, Wu S, Sundaram S et al. (2006) Arsenic resistance in Pteris vittata L.: Identification of a cytosolic triosephosphate isomerase based on cDNA expression cloning in Escherichia coli. Plant Mol Biol 62:845–857Google Scholar
  58. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37PubMedCrossRefGoogle Scholar
  59. Requejo R, Tena M (2005) Proteome analysis of maize roots reveals that oxidative stress is a main contributing factor to plant arsenic toxicity. Phytochem 66:1519–1528CrossRefGoogle Scholar
  60. Schat H, Llugany M, Vooijs R et al. (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392PubMedCrossRefGoogle Scholar
  61. Schmöger MEV, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122:793–801CrossRefGoogle Scholar
  62. Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642PubMedCrossRefGoogle Scholar
  63. Sneller FEC, Van Heerwaarden LM, Kraaijeveld-Smit FJL et al. (1999) Toxicity of arsenate in Silene vulgaris, accumulation and degradation of arsenate-induced phytochelatins. New Phytol 144:223–232CrossRefGoogle Scholar
  64. Su YH, McGrath SP, Zhao FJ (2010) Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant and Soil 328:27–34CrossRefGoogle Scholar
  65. Tripathi RD, Srivastava S, Mishra S et al. (2007) Arsenic hazards: Strategies for tolerance and remediation by plants. Trends Biotechnol 25:158–165PubMedCrossRefGoogle Scholar
  66. Tu C, Ma LQ (2002) Effects of arsenic concentrations and forms on arsenic uptake by the hyperaccumulator ladder brake. J Environ Qual 31:641–647PubMedCrossRefGoogle Scholar
  67. Ullrich-Eberius CI, Sanz A, Novacky AJ (1989) Evaluation of arsenate- and vanadate-associated changes of electrical membrane potential and phosphate transport in Lemna gibba-G1. J Exp Bot 40:119–128CrossRefGoogle Scholar
  68. Vögeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Implication of a transport function for cadmium-binding peptides. Plant Physiol 92:1086–1093PubMedCrossRefGoogle Scholar
  69. Williams PN, Villada A, Deacon C et al. (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859PubMedCrossRefGoogle Scholar
  70. Wu JH, Zhang R, Lilley RM (2002) Methylation of arsenic in vitro by cell extracts from bent grass (Agrostis tenuis): Effect of acute exposure of plants to arsenate. Funct Plant Biol 29:73–80CrossRefGoogle Scholar
  71. Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599PubMedCrossRefGoogle Scholar
  72. Zhang J, Zhu YG, Zeng DL et al. (2008) Mapping quantitative trait loci associated with arsenic accumulation in rice (Oryza sativa). New Phytol 177:350–355PubMedGoogle Scholar
  73. Zhao R, Zhao M, Wang H, Taneike Y, Zhang X (2006) Arsenic speciation in moso bamboo shoot—a terrestrial plant that contains organoarsenic species. Sci Total Environ 371:293–303Google Scholar
  74. Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794PubMedCrossRefGoogle Scholar
  75. Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: Mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559PubMedCrossRefGoogle Scholar
  76. Zhu YG, Williams PN, Meharg AA (2008) Exposure to inorganic arsenic from rice: A global health issue? Environ Pollut 154:169–171PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Alok Krishna Sinha
    • 3
    Email author
  • Dhammaprakash Pandahri Wankhede
    • 1
  • Meetu Gupta
    • 2
  1. 1.National Institute of Plant Genome ResearchDepartment of Biotechnology, Government of IndiaNew DelhiIndia
  2. 2.Department of BiotechnologyNew DelhiIndia
  3. 3.National Institute of Plant Genome ResearchNew DelhiIndia

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