Abstract
This review explains the transport, mobility, resistance and detoxification of toxic metalloid arsenic (As) in plants. Arsenic is ubiquitously present in Earth’s crust; however, numerous human interventions such as rapid industrialization use of As-based pesticides, insecticides and discharge of industrial wastes in water bodies leads to cumulative increase in As in the environment and has become a global challenge. Arsenic exists in different organic and inorganic forms, but inorganic forms such as pentavalent arsenate (AsV) and trivalent arsenite (AsIII) are more toxic and actively taken up by plants. Its toxicity is marked by generation of reactive oxygen species (ROS) that are capable of degrading various biomolecules of the cellular systems. To keep the ROS under the limit, plants have an array of enzymatic antioxidants such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR) and glutathione-S-transferase (GST); and non-enzymatic antioxidant like ascorbate, proline, and cysteine. Contrary to this, As-hyper-accumulator plants survive under high concentration of As through the strenuous action of Asv reduction into AsIII followed by the vacuolar compartmentalization of complex or inorganic As. Hence, this review focuses on the potential sources of As in the environment, its speciation and toxicity, and tolerance strategies in plants.
Similar content being viewed by others
References
Abbas MHH, Meharg AA (2008) Arsenate, arsenite and dimethyl arsenic acid (DMA) uptake and tolerance in maize (Zea mays L.). Plant Soil 304:277–289
Abercrombie J, Halfhill M, Ranjan P, Rao M, Saxton A, Yuan J, Stewart CN (2008) Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol 8:87
Adriano DC (2001) Trace elements in the terrestrial environment, vol 47. Springer, New York, pp 217–286
Ahmad P, Alam P, Balawi TH, Atalayan F, Ahanger AM, Ashraf M (2020a) Sodium nitropruside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. Chemistry 244:125480
Ahmad P, Alyemeni MN, Al-Huquail AA, Alqahtahi MA, Wijaya L, Asharaf M, Kaya C, Bajguz A (2020b) Zinc oxide nanoparticle application alleviates arsenite toxicity in Soybean plants by restricting the uptake of As and modulating key biochemical attributes, antioxidant enzymes ascorbate-glutathione cycle and glyoxalase system. Plants 9:825
Ahsan N, Lee DG, Alam I, Kim PJ, Lee JJ 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 8:3561–3576
Alsahli AA, Bhat JA, Alyemeni M, Asharaf M, Ahmad P (2020) Hydrogen sulide (H2S) mitigates arsenic induced toxicity in pea (Pisum sativum L.) plants by regulating osmoregulation, antioxidant defense system, ascorbate- glutathione cycle and glyoxalase system. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10254-6
Bhattacharya P, Jacks G, Ahmed KM, Routh J, Khan AA (2002) Arsenic in groundwater of the Bengal delta plain aquifers in Bangladesh. Bull Environ Contam Toxicol 69:538–545
Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 6:26
Bissen M, Frimmel FH (2003) Arsenic a review part I: Occurrence, toxicity, speciation, and mobility. Acta Hydrochim Hydrobiol 31:9–18
Bleeker PM, Hakvoort HWJ, Bliek M, Souer E, Schat H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcuslanatus. Plant J 45:917–929
Cao X, Ma LQ, Tub C (2004) Antioxidative responses to arsenic in the arsenic-hyperaccumulator chinese brake fern (Pteris vittata L.). Environ Pollut 128:317–325
Carey AM, Norton GJ, Deacon C, Scheckel KG, Lombi E, Punshon T et al (2011) Phloem transport of arsenic species from flag leaf to grain during grain filling. New Phytol 192:87–98
Catarecha P, Segura MD, Franco-Zorrilla JM, Garcia-Ponce B, Lanza M et al (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133
Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
Cozzolino V, Pigna M, Di Meo V, Caporale AG, Violante A (2010) Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth of Lactuca sativa L. and arsenic and phosphorus availability in an arsenic polluted soil under nonsterile conditions. Appl Soil Ecol 45:262–268
Dembitsky VM, Levitsky DO (2004) Arsenolipids. Prog Lipid Res 43:403–448
Dhankher OP, Li YJ, Rosen BP, Shi J, Salt D et al (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamyl cysteine synthetase expression. Nat Biotechnol 20:1140–1145
Dhankher OP, Rosen BP, McKinney EC, Meagher RB (2006) Hyperaccumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase (ACR2). PNAS USA 103:5413–5418
DiTusa SF, Fontenot EB, Wallace RW, Silvers MA, Steele TN, Elnagar AH, Dearman KM, Smith AP (2016) A member of the Phosphate transporter 1 (Pht1) family from the arsenic-hyperaccumulating fern Pteris vittata is a high-affinity arsenate transporter. New Phytol 209:762–772
Dixit G, Singh AP, Kumar A, Mishra S, Dwivedi S, Kumar S, Trivedi PK, Pandey V, Tripathi RD (2016) Reduced arsenic accumulation in rice (Oryza sativa L.) shoot involves sulfur mediated improved thiol metabolism, antioxidant system and altered arsenic transporters. Plant Physiol Biochem 99:86–96
Drewniak L, Sklodowska A (2013) Arsenic-transforming microbes and their role in biomining processes. Environ Sci Pollut Res 20:7728–7739
Duan GL, Zhou Y, Tong YP, Mukhopadhyay R, Rosen BP, Zhu YG (2007) A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 174:311–321
Ernst WH, Krauss GJ, Verkleij JA, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143
Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321
Gasic K, Korban SS (2007) Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance. Plant Mol Biol 64:361–369
González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) Phosphate transporter traffic facilitator is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500–3512
Guo J, Dai X, Xu W, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026
Hartley-Whitaker J, Ainsworth G, Meharg AA (2001) Copper and arsenate-induced oxidative stress in Holcuslanatus L. clones with differential sensitivity. Plant Cell Environ 24:713–722
Hasan MM, Hasan MM, da Silva JA, Li X (2016) Regulation of phosphorus uptake and utilization: transitioning from current knowledge to practical strategies. Cell Mol Biol Lett 21:7
Imamul-Huq SM, Joardar JC, Parvin S (2005) Marigold (Tagetespatula) and ornamental arum (Syngonia sp.) as phytoremediators for arsenic in pot soil. Bangla J Bot 34:65–70
Imamul-Huq SM, Parvin K, Rahman S, Joardar JC (2009) Response of cowpea (Vigna sinensis L.) to arsenic. Can J Pure Appl Sci 3:879–902
Indriolo E, Na G, Ellis D, Salt DE, Banks JA (2010) A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22:2045–2057
Kaya C, Ashraf M, Alyemeni MN, Corpas FJ, Ahmad P (2020) Salicylic acid-induced nitric oxide enhances arsenic toxicity tolerance in maize plants by up regulating the ascorbate-glutathione cycle and glyoxalase system. J Hazard Mater 399:123020
Kumari A, Pandey N, Pandey-Rai S (2017) Protection of Artemisia annua roots and leaves againstoxidative stress induced by arsenic. Biol Planta 61:367–377
Li Y, Dhankher OP, Carreira L, Balish RS, Meagher RB (2005) Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial gamma-glutamyl cysteine synthetase. Environ Toxicol Chem 24:1376–1386
Li RY, Ago Y, Liu WJ, Mitani N, Feldmann J, McGrath SP, Ma JF, Zhao FJ (2009) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150:2071–2080
Liu WJ, Zhu YG, Smith FA, Smith SE (2004) Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture. New Phytol 162:481–488
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. PNAS USA 105:9931–9935
Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235
Matysik J, Alia Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Meharg AA (2004) Arsenic in rice understanding a new disaster for South-East Asia. Trends Plant Sci 9:415–417
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytol 154:29–43
Meharg AA, Rahman MM (2003) Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ Sci Technol 37:229–234
Milivojevic DB, Nikolic BR, Drinic G (2006) Effects of arsenic on phosphorous content in different organs and chlorophyll fluorescence in primary leaves of soybean. Biol Plant 1:149–151
Mishra S, Dubey RS (2006) Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. J Plant Physiol 163:927–936
Mishra PK, Sinha AK (2012) Rice diversity in Bankura district of West Bengal (India). Biosci Discov 3:284–287
Mishra VK, Upadhyay AR, Pathak V, Tripathi B (2008) Phytoremediation of mercury and arsenic from tropical opencast coalmine effluent through naturally occurring aquatic macrophytes. Water Air Soil Pollut 192:303–314
Mitani N, Yamaji N, Ma JF (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflugers Arch 456:679–686
Miteva E (2002) Accumulation and effect of arsenic on tomatoes. Comm Soil Sci Plant Anal 33:1917–1926
Mitra A, Chatterjee S, Moogouei R, Gupta DK (2017) Arsenic accumulation in rice and probable mitigation approaches: a review. Agronomy 7:67
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481
Mosa KA, Kumar K, Chhikara S, McDermott J, Liu Z, Musante C, White JC, Dhankher OP (2012) Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21:1265–1277
Ng JC (2005) Environmental contamination of arsenic and its toxicological impact on humans. Environ Chem 2:146–160
Patel A, Tiwari S, Prasad SM (2018) Toxicity assessment of arsenate and arsenite on growth, chlorophyll a fluorescence and antioxidant machinery in Nostoc muscorum. Ecotoxicol Environ Saf 167:369–379
Patel A, Tiwari S, Prasad SM (2020) Effect of time interval on arsenic toxicity to paddy field cyanobacteria as evident by nitrogen metabolism, biochemica constituent, and exopolysaccharide content. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02289-3
Pickering IJ, Gumaelius L, Harris HH, Prince RC, Hirsch G, Banks A, Salt DE, George GN (2006) Localizing the biochemical transformations of arsenate in a hyper accumulating fern. Environ Sci Technol 40:5010–5014
Pigna M, Cozzolina V, Violante A, Meharg AA (2008) Influence of phosphate on the arsenic uptake by wheat (Triticum durum L.) irrigated with arsenic solutions at three different concentrations. Water Air Soil Pollut 197:371–380
Rahman MA, Hasegawa H, Rahman MM, Islam MN, Miah MAM, Tasmin A (2007) Arsenic accumulation in rice (Oryza sativa L.) varieties of Bangladesh: a glass house study. Water Air Soil Pollut 185:53–61
Rahman MA, Hasegawa H, Rahman MM, Miah MAM, Tasim A (2008) Straight head disease of rice (Oryza sativa L.) induced by arsenic toxicity. Environ Exp Bot 62:54–59
Rahman MA, Rahman MM, Kadohashi K, Maki T, Hasegawa H (2011) Effect of external iron and arsenic species on chelant-enhanced iron bioavailability and arsenic uptake in rice (Oryza sativa L.). Chemosphere 84:439–445
Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37
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
Shaibur MR, Kawai S (2009) Effect of arsenic on visible symptom and arsenic concentration in hydroponic Japanese mustard spinach. Environ Exp Bot 67:65–70
Sharma VK, Sohn M (2009) Aquatic arsenic: toxicity, speciation, transformations, and remediation. Environ Int 35:743–759
Sharma AK, Tjell JC, Sloth JJ, Holm PE (2014) Review of arsenic contamination, exposure through water and food and low cost mitigation options for rural areas. Appl Geochem 41:11–33
Shi S, Wang T, Chen Z, Tang Z, Wu Z, Salt DE, Chao DY, Zhao F (2016) OsHAC1; 1 and OsHAC1; 2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol 172:1708–1719
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 39:629–642
Singh N, Ma LQ, Srivastava M, Rathinasabapathi B (2006) Metabolic adaptations to arsenic induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci 170:274–282
Singh M, Kumar J, Singh S, Singh VP, Prasad SM et al (2015a) Adaptation strategies of plants against heavy metal toxicity: a short review. Biochem Pharmacol 4:161
Singh R, Singh S, Parihar P, Singh VP, Prasad SM (2015b) Arsenic contamination, consequences and remediation techniques: a review. Ecotoxicol Environ Saf 112:247–270
Singh VP, Singh S, Kumar J, Prasad SM (2015c) Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged Luffa seedlings. Protoplasma 252:1217–1229
Singh VP, Singh S, Kumar J, Prasad SM (2015d) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181:20–29
Singh PK, Indoliya Y, Chauhan AS, Singh SP, Singh AP, Dwivedi S, Tripathi RD, Chakrabarty D (2017) Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci Rep 7:3592. https://doi.org/10.1038/s41598-017-03923-2
Singh R, Parihar P, Prasad P (2018) Simultaneous exposure of sulphr and calcium hinder As toxicity: up-regulation of growth, mineral nutrients uptake and antioxidant system. Ecotoxicol Environ Saf 161:318–331
Singh R, Parihar P, Prasad SM (2020) Interplay of calcium and nitric oxide in improvement of growth and arsenic-induced toxicity in mustard seedlings. Sci Rep 10:1–12
Sinha S, Sinam G, Mishra RK, Mallick S (2010) Metal accumulation, growth, antioxidants and oil yield of Brassica juncea L. exposed to differentmetals. Ecotoxicol Environ Saf 73:1352–1361
Song WY, Park J, Mendoza-Cozatl DG et al (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. PNAS USA 107:21187–21192
Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyper-accumulator and sensitive fern species to arsenic. J Exp Bot 56:1335–1342
Srivastava S, Shrivastava M, Suprasanna P, D’Souza SF (2011) Phytofiltration of arsenic from simulated contaminated water using Hydrilla verticillata in field conditions. Ecol Eng 37:1937–1941
Srivastava S, Upadhyay MK, Tripathi RD, Dhankher OP (2016) Arsenic transport, metabolism and toxicity in plants. Int J Plant Environ 2:1–12
Stoeva N, Bineva TZ (2003) Oxidative changes and photosynthesis in Oat plants grown in As-contaminated soil. Bulg J Plant Physiol 29:87–95
Stoeva N, Berova M, Vassilev A, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol Planta 49:293
Su YH, McGrath SP, Zhu YG, Zhao FJ (2008) Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol 180:434–441
Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011:939161
Tiwari M, Sharma D, Dwivedi S, Singh M, Tripathi RD, Trivedi PK (2014) Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ 37:140–152
Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372
Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068
Wang JR, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate and arsenic speciation. Plant Physiol 130:1552–1561
WHO (2001) Arsenic and arsenic compounds. Inter-organization programme for the sound management of chemicals. Environmental Health Criteria, Geneva, p 224
Wu Z, Ren H, McGrath SP, Wu P, Zhao F (2011) Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 157:498–508
Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:392–399
Zhao FJ, Ago Y, Mitani N, Li RY, Su YH, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186:392–399
Acknowledgements
The author ‘Rohit Kumar Mishra’ is grateful to the University Grants Commission, New Delhi, for providing financial assistance as PDF under Dr. DS Kothari UGC Fellowship Scheme-F 4-2/2006 (BSR)/13-113/2013 (BSR), Sanjesh Tiwari is thankful to UGC-CSIR-SRF and Anuradha Patel is thankful to UGC-NFO-SRF.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mishra, R.K., Tiwari, S., Patel, A. et al. Arsenic contamination, speciation, toxicity and defense strategies in plants. Braz. J. Bot 44, 1–10 (2021). https://doi.org/10.1007/s40415-020-00694-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-020-00694-5