Abstract
Arsenic is a metalloid which is toxic to living organisms. Natural occurrence of arsenic and human activities have led to widespread contamination in many areas of the world, exposing a large section of the human population to potential arsenic poisoning. Arsenic intake can occur through consumption of contaminated crops and it is therefore important to understand the mechanisms of transport, metabolism and tolerance that plants display in response to arsenic. Plants are mainly exposed to the inorganic forms of arsenic, arsenate and arsenite. Recently, significant progress has been made in the identification and characterisation of proteins responsible for movement of arsenite into and within plants. Aquaporins of the NIP (nodulin26-like intrinsic protein) subfamily were shown to transport arsenite in planta and in heterologous systems. In this review, we will evaluate the implications of these new findings and assess how this may help in developing safer and more tolerant crops.
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References
Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568
Brewstar MD (1994) Removing arsenic from contaminated water. Water Environ Technol 4:54–57
Chatterjee A (1994) Ground water arsenic contamination in residential area and surroundings of P.N.Mitra Lane, Behala, Calcutta, due to industrial effluent discharge. PhD thesis, Jadavpur University, Calcutta, India
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and non resistant plant species. New Phytol 154:429–432
Yarnell A (1983) Salvarsan. http://pubs.acs.org/cen/coverstory/83/8325/8325 salvarsan.html. Accessed Mar 2006
Van den Enden E (1999) Arsenic poisoning. http://www.itg.be/evde/ Teksten/sylabus/49_Arsenicism.doc Accessed Apr 2006
National Academy of Sciences (1977) Arsenic: medical and biological effects of environmental pollutants. National Academy Press, USA
Orme S, Kegley S (2006) PAN Pesticides Database. http://ww.pesticideinfo.org Accessed May 2006
Ishiguro S (1992) Industries using arsenic and arsenic compounds. Appl Organomet Chem 6:323–331
IARC (1987) Arsenic and arsenic compounds (Group 1). In: IARC monographs on the evaluation of the carcinogenic risks to humans. Supplement 7, date accessed: 6 Feb 2003. Available from http://193.51.164.11/htdocs/monographs/ suppl7/arsenic.html>
Naidu R, Smith E, Wens G, Bhattacharya P, Nadebaum P (2006) Managing arsenic in the environment from soil to human. CSIRO Publishing, pp 327–350
National Research Council (2001) Arsenic in drinking water update. National Academy Press, USA
IPCS (2001) Environmental health criteria on arsenic and arsenic compounds. Environmental Health Criteria Series, No. 224. Arsenic and arsenic compounds, second, WHO, Geneva, p 521
Gochfeld M (1997) Factors influencing susceptibility to metals. Environ Health Perspect 105(4):817–833
Young A (2000) Arsenic. http://www.protfolio.mvm.ac.uk/studentweb/session2/ group12/arsenic.html
Chou W, Jie C, Kenedy A, Jones RJ, Trush MA, Dang CV (2004) Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukaemia cells. Proc Natl Acad Press USA 101:4578–4583
Mead MN (2005) Arsenic: in search of an antidote to a global poison. Environ Health Perspect 113:A379–A386
Tamaki S, Frankenberger WT (1992) Environmental biochemistry of arsenic. Rev Environ Contam Toxicol 124:79–110
Carbonell-Barrachina AA, Aarabi MA, De Laune RD, Gambrell RP, Patrick WHJ (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
Carbonell-Barrachina AA, Burlo F, Lopez E, Martinez-Sanchez F (1999) Arsenic toxicity and accumulation in radish as affected by arsenic chemical speciation. J Environ Sci Health Part B–Pestic Food Contam Agric Wastes 34:661–679
Petrick JS, Ayala-Fierro F, Cullen WR, Carter DE, Aposhian HV (2000) Monomethylarsonous acid (MMAIII) is more toxic than arsenite in Chang human hepatocytes. Toxicol Appl Pharmacol 163:203–207
Ontario Ministry of the Environment (2001) Arsenic in the environment. http://www.ene.gov.on.ca/cons/3792e.htm Accessed Feb 2006
Nordstrom DK (2002) Public health-Worldwide occurrences of arsenic in ground water. Science 296:2143–2145
Fazal MA, Kawachi T, Ichio E (2001) Validity of the latest research findings on causes of groundwater arsenic contamination in Bangladesh. Water Int 26:380–389
Chowdhury UK, Biswas BK, Chowdhury TR, Samanta G, Mandal BK, Basu GC, Chanda CR, Lodh D, Saha KC, Mukherjee SK, Roy S, Kabir S, Quamruzzaman Q, Chakraborti D (2000) Groundwater arsenic contamination in Bangladesh and West Bengal, India. Environ Health Perspect 108:393–397
O’Neill P (1995) Arsenic. In: Alloway BJ (ed) Heavy metals in soils. Blackie, London, pp 105–121
Williams PN, Price AH, Raab A, Hossain SA, Feldmann J, Meharg AA (2005) Variation in arsenic speciation and concentration in paddy rice related to dietary exposure. Environ Sci Technol 39:5531–5540
Xu XY, McGrath SP, Meharg A, Zhao FJ (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ Sci Technol 42:5574–5579
Zavala YJ, Duxbury JM (2008) Arsenic in rice: I. Estimating normal levels of total arsenic in rice grain. Environ Sci Technol 42:3856–3860
Tripathi R, Srivastava S, Mishra S, Singh N, Tuli R, Gupta D, Maathuis FJM (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotech 25(4):158–165
Rosenberg H, Gerdes G, Chegwidden K (1977) Two systems for the uptake of phosphate in Escherichia coli. J Bacteriol 131(2):505–511
Willsky G, Malamy M (1980) Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. J Bacteriol 144(1):356–365
Willsky G, Malamy M (1980) Effect of arsenate on inorganic phosphate transport in Escherichia coli. J Bacteriol 144(1):366–374
Bhattacharjee H, Rosen BP (2007) Arsenic metabolism in prokaryotic and eukaryotic microbes in: molecular microbiology of heavy metals. Springer, Heidelberg
Lin YF, Walmsley A, Rosen B (2006) An arsenic metallochaperone for an arsenic detoxification pump. Proc Natl Acad Sci USA 103(42):15617–15622
Rosen B (2002) Biochemistry of arsenic detoxification. FEBS Lett 529:86–92
Yang H, Cheng J, Finan T, Rosen B, Bhattacharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187(20):6991–6997
Qin J, Rosen B, Zhang Y, Wang G, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci USA 103(7):2075–2080
Wysocki R, Chéry C, Wawrzycka D, Hulle VM, Cornelis R, Thevelein J, Tamás M (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol Microbiol 40(6):1391–1401
Liu Z, Boles E, Rosen B (2004) Arsenic trioxide uptake by hexose permeases in Saccharomyces cerevisiae. J Biol Chem 279(17):17312–17318
Liu Z, Sanchez M, Jiang X, Boles Landfear S, Rosen B (2006) Mammalian glucose permease GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem Biophys Res Commun 351(2):424–430
Ghosh M, Shen J, Rosen BP (1999) Pathways of AsIII detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96:5001–5006
Liu Z, Shen JM, Carbrey J, Mukhopadhyay R, Agre P, Rosen B (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci USA 99(9):6053–6058
Liu Z, Styblo M, Rosen B (2006) Methylarsonous acid transport by aquaglyceroporins. Environ Health Perspect 114(4):527–531
Liu Z, Carbrey J, Agre P, Rosen B (2004) Arsenic trioxide uptake by human and rat aquaglyceroporins. Biochem Biophys Res Commun 316(4):1178–1185
Liu J, Chen H, Miller D, Saavedra J, Keefer L, Johnson D, Klaassen C, Waalkes P (2001) Overexpression of Glutathione S-Transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol Pharmacol 60:302–309
Kojima C, Qu W, Waalkes M, Himeno S, Sakurai T (2006) Chronic exposure to methylated arsenicals stimulates arsenic excretion pathways and induces arsenic tolerance in rat liver cells. Toxicol Sci 91(1):70–81
Liu J, Liu Y, Powell DA, Waalkesa MP, Klaassen CD (2002) Multidrug-resistance mdr1a/1b double knockout mice are more sensitive than wild type mice to acute arsenic toxicity, with higher arsenic accumulation in tissues. Toxicol 170(1–2):55–62
Leslie ME, Haimeur A, Waalkes M (2004) Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). J Biol Chem 279(31):32700–32708
Shin H, Shin HS, Gary RD, Maria JH (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
Raab A, Williams PN, Meharg AA, Feldmann J (2007) Uptake and translocation of inorganic and methylated arsenic species by plants. Environ Chem 4:197–203
Wang J, 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
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 103:5413–5418
Bleeker PM, Hakvoort HW, Bliek M, Souer E, Schat H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J 45:917–929
Ellis DR, Gumaelius L, Indriolo E, Pickering IJ, Banks JA, Salt DE (2006) A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol 141(4):1544–1554
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(2):311–321
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol doi: 10.1111/j.1469-8137.2008.02716.x
Raab A, Feldmann J, Meharg AA (2004) The Nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134(3):1113–1122
Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast, Schizosaccharomyces pombe. Plant Cell 11:1153–1164
Zhao FJ, Wang JR, Barker JHA, Schat H, Bleeker PM, McGrath SP (2003) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol 159:403–410
Pickering IJ, Gumaelius L, Harris HH, Prince RC, Hirsch G, Banks JA, Salt DE, George GN (2006) Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol 40:5010–5014
Caille N, Zhao FJ, McGrath SP (2005) Comparison of root absorption, translocation and tolerance of arsenic in the hyperaccumulator Pteris vittata and the non hyperaccumulator Pteris tremula. New Phytol 165:755–761
Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582:1625–1628
Ma JF, Yamaji N, Mitani N, Xiao XY, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105(29):9931–9935
Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Reduction and co-ordination of arsenic in Indian mustard. Plant Physiol 122:1171–1177
Salt DE, Rauser WE (1995) MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol 107:1293–1301
Meharg AA, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44
Wallace IS, Choi WG, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochem Biophys Acta-Biomem 1758:1165–1175
Takano J, Wada M, Ludewig U, Schaaf G, Von WN, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509
Tanaka M, Wallace IS, Takano J, Roberts DM, Fujiwara F (2008) NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 20:2860–2875
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691
Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bidirectional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 6:26
Kamiya T, Tanaka M, Mitani N, Ma FJ, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284(4):2114–2120
Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599
Rosen BP (2002) Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol A 133:689–693
Wysocki R, Bobrowicz P, Ulaszewski S (1997) The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem 272:30061–30066
Salt D, Banks JA, Indriolo E (2007) Expression of putative arsenite effluxers in Pteris vittata. Proc Bot Soc Am USA Number: P05023 Abstract ID: 2093
Pickering IJ, Gumaelius L, Harris HH, Prince RC, Hirsch G, Banks JA, Salt DE, George GN (2006) Localizing the biochemical transformations of arsenate in a hyper accumulating fern. Environ Sci Technol 40:5010–5014
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Ali, W., Isayenkov, S.V., Zhao, FJ. et al. Arsenite transport in plants. Cell. Mol. Life Sci. 66, 2329–2339 (2009). https://doi.org/10.1007/s00018-009-0021-7
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DOI: https://doi.org/10.1007/s00018-009-0021-7