Plant and Soil

, Volume 327, Issue 1–2, pp 1–21 | Cite as

Arsenic uptake and toxicity in plants: integrating mycorrhizal influences

  • Sally E. Smith
  • Helle M. Christophersen
  • Suzanne Pope
  • F. Andrew Smith
Marschner Review

Abstract

Arsenic (As) contamination of soil and water is a global problem that impacts on many areas of biology. This review firstly covers aspects of soil chemistry and soil-plant interactions relevant to the ways plants take up As (particularly arsenate (As(V)) from aerobic soils, with especial attention to As-phosphorus (P) interactions. It then assesses the extent to which studies of plant As tolerance based on short-term uptake of As(V) from nutrient solutions can be extrapolated to longer-term growth in contaminated soil. Mycorrhizal symbioses are then highlighted, because they are formed by ~ 90% of higher plants, often with increased uptake of phosphate (Pi) compared with non-mycorrhizal (NM) counterparts. It is therefore likely that mycorrhizas influence As(V) uptake. Published work shows that arbuscular mycorrhizal (AM) plants (the most common mycorrhizal type) have higher P/As ratios than NM plants, and this would be expected to affect sensitivity to soil As. We discuss ways in which higher P/As selectivity might result from differential operation of P and As uptake pathways in AM compared with NM plants, taking into account new understanding of P uptake mechanisms. We also give suggestions for future research required to increase understanding of mechanisms of As(V) uptake, and its interactions with plant P.

Keywords

Arsenic Phosphate Mechanisms of plant tolerance Mycorrhizas Soil toxicity 

References

  1. Abedin MJ, Cotter-Howells J, Meharg AA (2002a) Arsenic uptake and accumulation in rice (Oryza sativa L.) irrigated with contaminated water. Plant Soil 240:311–319CrossRefGoogle Scholar
  2. Abedin MJ, Feldman J, Meharg AA (2002b) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128PubMedCrossRefGoogle Scholar
  3. Ahmed FRS, Killham K, Alexander I (2006) Influences of arbuscular mycorrhizal fungus Glomus mosseae on growth and nutrition of lentil irrigated with arsenic contaminated water. Plant Soil 258:33–41CrossRefGoogle Scholar
  4. Al Agely A, Sylvia DM, Ma LQ (2005) Mycorrhizae increase arsenic uptake by the hyperaccumulator Chinese brake fern (Pteris vittata L.). J Environ Qual 34:2181–2186PubMedCrossRefGoogle Scholar
  5. Anastasia F, Kender W (1973) Influence of soil arsenic on the growth of lowbush blueberry. J Environ Qual 2:335–337Google Scholar
  6. Asher CJ, Reay PF (1979) Arsenic uptake by barley seedlings. Aust J Plant Physiol 6:459–466CrossRefGoogle Scholar
  7. Bieleski RL, Lauchli A (1992) Phosphate uptake, efflux and deficiency in the water fern, Azolla. Plant Cell Environ 15:665–673CrossRefGoogle Scholar
  8. Bucher M (2006) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26CrossRefGoogle Scholar
  9. Burleigh SH, Cavagnaro TR, Jakobsen I (2002) Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot 53:1593–1601PubMedCrossRefGoogle 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. Chen BD, Tang XY, Zhu YG et al (2005) Metal concentrations and mycorrhizal status of plants colonizing copper mine tailings: potential for revegetation. Sci China Ser C 48:156–164CrossRefGoogle Scholar
  12. Chen BD, Xiao X, Zhu YG et al (2007) The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Sci Total Environ 379:226–234PubMedCrossRefGoogle Scholar
  13. Christophersen HM, Smith SE, Pope S, Smith FA (2009) No evidence for competition between arsenate and phosphate for uptake from soil by medic or barley. Env Int 35:485–490CrossRefGoogle Scholar
  14. Christophersen HM, Smith FA, Smith SE (2009) Arbuscular mycorrhizal colonisation reduces arsenate uptake in barley via down-regulation of transporters in the direct epidermal phosphate uptake pathway. New Phytol in pressGoogle Scholar
  15. Clark GT, Dunlop J, Phung HT (2000) Phosphate absorption by Arabidopsis thaliana: interactions between phosphorus status and inhibition by arsenate. Aust J Plant Physiol 27:959–965Google Scholar
  16. Covey RP, Koch BL, Larsen HJ (1981) Influence of vesicular arbuscular mycorrhizae on the growth of apple and corn in low-phosphorous soil. Phytopathology 71:712–715CrossRefGoogle Scholar
  17. 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
  18. 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
  19. Esteban E, Carpena RO, Meharg AA (2003) High-affinity phosphate/arsenate transport in white lupin (Lupinus albus) is relatively insensitive to phosphate status. New Phytol 158:165–173CrossRefGoogle Scholar
  20. Ezawa T, Smith SE, Smith FA (2002) P metabolism and transport in AM fungi. Plant Soil 244:221–230CrossRefGoogle Scholar
  21. Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil-rhizosphere-plant system: fundamentals and potential application to phytoremediation. J Biotech 99:259–278CrossRefGoogle Scholar
  22. Geng CN, Zhu YG, Hu Y et al (2006) Arsenate causes differential acute toxicity in two P-deprived genotypes of rice seedlings (Oryza sativa L.). Plant Soil 279:297–306CrossRefGoogle Scholar
  23. Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698PubMedCrossRefGoogle Scholar
  24. Gonzaga MIS, Santos JAG, Ma LQ (2006) Arsenic phytoextraction and hyperaccumulation by fern species. Sci Ag (Peracicaba, Braz.) 63:90–101Google Scholar
  25. Gonzalez-Chavez C, Harris PJ, Dodd J et al (2002) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171CrossRefGoogle Scholar
  26. Grace EJ (2008) Functional characterisation of phosphorus uptake pathways in a non-responsive arbuscular mycorrhizal host. PhD Thesis, School of Earth and Environmental Sciences. The University of Adelaide, Adelaide, AustraliaGoogle Scholar
  27. Grace EJ, Cotsaftis O, Smith FA et al (2009) Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonisation, fungal P uptake or effects on plant phosphate transporter expression. New Phytol 181:938–949CrossRefGoogle Scholar
  28. Gunes A, Pilbeam DJ, Inal A (2009) Effect of arsenic-phosphorus interaction on arsenic-induced oxidative stress in chickpea plants. Plant Soil 314:211–220CrossRefGoogle Scholar
  29. Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429PubMedCrossRefGoogle Scholar
  30. Hartley-Whitaker J, Ainsworth GC, Meharg AA (2001) Copper-and arsenate-induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ 24:713–722CrossRefGoogle Scholar
  31. Hartley-Whitaker J, Woods C, Meharg AA (2002) Is differential phytochelatin production related to decreased arsenate influx in arsenate tolerant Holcus lanatus? New Phytol 155:219–225CrossRefGoogle Scholar
  32. Huang CY, Barker SJ, Langridge P et al (2000) Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol 124:415–422PubMedCrossRefGoogle Scholar
  33. Hurd-Karrer AM (1939) Antagonism of certain elements essential to plants toward chemically related toxic elements. Plant Physiol 14:9–29PubMedCrossRefGoogle Scholar
  34. Ipsilantis I, Sylvia DM (2007) Interactions of assemblages of mycorrhizal fungi with two Florida wetland plants. Appl Soil Ecol 35:261–271CrossRefGoogle Scholar
  35. Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322PubMedCrossRefGoogle Scholar
  36. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  37. Karandashov V, Nagy R, Wegmüller S et al (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 101:6285–6290PubMedCrossRefGoogle Scholar
  38. Khan AG, Belik M (1995) Occurrence and ecological significance of mycorrhizal symbiosis in aquatic plants. In: Varma A, Hock B (eds) Mycorrhiza, Structure, Function. Molecular Biology and Biotechnology. Springer Verlag, Berlin Heidelberg, pp 627–666Google Scholar
  39. Knudson JA, Meikle T, DeLuca TH (2003) Role of mycorrhizal fungi and phosphorus in the arsenic tolerance of basin wildrye. J Environ Qual 32:2001–2006PubMedGoogle Scholar
  40. Lambert DH, Baker DE, Cole H Jr (1979) The role of mycorrhizae in the interactions of phosphorus with zinc, copper, and other elements. Soil Sci Soc Am J 43:976–980Google Scholar
  41. Lee DA, Chen A, Schroeder JI (2003) ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J 35:637–646PubMedCrossRefGoogle Scholar
  42. Leung HM, Ye ZH, Wong MH (2005) Interactions of mycorrhizal fungi with Pteris vitatta (As hyperaccumulator) in As-contaminated soils. Environ Poll 139:1–8CrossRefGoogle Scholar
  43. Li HY, Smith SE, Holloway RE et al (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536–543PubMedCrossRefGoogle Scholar
  44. Liu H, Trieu AT, Blaylock LA, Harrison MJ (1998) Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and response to colonization by arbuscular mycorrhizal (AM) fungi. Mol Plant Microbe Interact 11:14–22PubMedCrossRefGoogle Scholar
  45. Liu Y, Zhu YG, Chen BD et al (2005a) Influence of the arbuscular mycorrhizal fungus Glomus mosseae on uptake of arsenate by the As hyperaccumulator fern Pteris vittata L. Mycorrhiza 15:187–192PubMedCrossRefGoogle Scholar
  46. Liu Y, Zhu YG, Chen BD et al (2005b) Yield and arsenate uptake of arbuscular mycorrhizal tomato colonized by Glomus mosseae BEG167 in As spiked soil under glasshouse conditions. Environ Int 31:867–873PubMedCrossRefGoogle Scholar
  47. Logoteta B, Xu XY, Macnair MR et al (2009) Arsenite efflux is not enhanced in the arsenate-tolerant phenotype of Holcus lanatus. New Phytol. doi:10.1111/j.1469-8137.2009.02841.x PubMedGoogle Scholar
  48. 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
  49. Ma LQ, Komar KM, Tu C et al (2001) A fern that hyperaccumulates arsenic. Nature 409:579PubMedCrossRefGoogle Scholar
  50. Macnair MR, Cumbes Q (1987) Evidence that arsenic tolerance in Holcus lanatus is caused by an altered phosphate uptake system. New Phytol 107:387–394CrossRefGoogle Scholar
  51. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extraradical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant Microbe Interact 14:1140–1148PubMedCrossRefGoogle Scholar
  52. Mascher R, Lippmann B, Holzinger S et al (2002) Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Sci 163:961–969CrossRefGoogle Scholar
  53. McGrath SP, Zhao F-J (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotech 14:277–282PubMedCrossRefGoogle Scholar
  54. Meding SM, Zasoski RJ (2008) Hyphal mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland. Soil Biol Biochem 40:126–134CrossRefGoogle Scholar
  55. Meharg AA (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107:1253–1265PubMedCrossRefGoogle Scholar
  56. Meharg AA (2004) Arsenic in rice - understanding a new disaster for South-East Asia. Trends Plant Sci 9:415–417PubMedCrossRefGoogle Scholar
  57. Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69–112CrossRefGoogle Scholar
  58. Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154:29–43CrossRefGoogle Scholar
  59. Meharg AA, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44CrossRefGoogle Scholar
  60. Meharg AA, Macnair MR (1990) An altered phosphate uptake system in arsenate-tolerant Holcus lanatus. New Phytol 116:29–35CrossRefGoogle Scholar
  61. Meharg AA, Macnair MR (1992a) Genetic correlation between arsenate tolerance and the rate of influx of arsenate and phosphate in Holcus lanatus L. Heredity 69:336–341Google Scholar
  62. Meharg AA, Macnair MR (1992b) Polymorphism and physiology of arsenate tolerance in Holcus lanatus L. from an uncontaminated site. Plant Soil 146:219–225CrossRefGoogle Scholar
  63. Meharg AA, Macnair MR (1992c) Suppression of the high-affinity phosphate-uptake system - a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524CrossRefGoogle Scholar
  64. Meharg AA, Naylor J, Macnair MR (1994a) Phosphorus nutrition of arsenate-tolerant and nontolerant phenotypes of velvetgrass. J Environ Qual 23:234–238CrossRefGoogle Scholar
  65. Meharg AA, Bailey K, Breadmore K et al (1994b) Biomass allocation, phosphorus nutrition and vesicular-arbuscular mycorrhizal infection in clones of Yorkshire Fog, Holcus lanatus L. (Poaceae) that differ in their phosphate uptake kinetics and tolerance to arsenate. Plant Soil 160:11–20CrossRefGoogle Scholar
  66. Nagy F, Karandashov V, Chague W et al (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250PubMedCrossRefGoogle Scholar
  67. Paivoke AEA, Simola LK (2001) Arsenate toxicity to Pisum sativum: mineral nutrients, chlorophyll content and phytase activity. Ecotox Environ Safe 49:111–121CrossRefGoogle Scholar
  68. Paszkowski U, Kroken S, Roux C et al (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329PubMedCrossRefGoogle Scholar
  69. Pickering IJ, George MJ, Smith RD et al (2000) Reduction and coordination of arsenic in Indian Mustard. Plant Physiol 122:1171–1177PubMedCrossRefGoogle Scholar
  70. Pigna M, Cozzolino V, Violante A et al (2009) Influence of phosphate on the arsenic uptake by wheat (Triticum durum L.) irrigated with arsenic solutions at three different concentrations. Water Air Soil Pollut 197:371–380CrossRefGoogle Scholar
  71. Pope S (2006) Increased phosphate supply and mycorrhizal colonisation increase growth and P status of Medicago truncatula in arsenic-contaminated soil but do not reduced As uptake. In: B Env Sci (Honours) Thesis, Soil and Land Systems, School of Earth and Environmental Sciences. The University of Adelaide, Adelaide, AustraliaGoogle Scholar
  72. Pope S, Smith SE, Christophersen HM et al (2007) Arsenic uptake by Medicago truncatula: P supply and arbuscular mycorrhizal (AM) colonization do not reduce specific uptake from soil. In: Zhu YG, Lepp N, Naidu R (eds) Biogeochemistry of Trace Elements: Environmental Protection. Remediation and Human Health. Tsinghua University Press, Beijing, pp 863–864Google Scholar
  73. Poulsen KH, Nagy R, Gao LL et al (2005) Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytol 168:445–453PubMedCrossRefGoogle Scholar
  74. 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
  75. Quaghebeur M, Rengel Z (2005) Arsenic speciation governs arsenic uptake and transport in terrestrial plants. Microchim Acta 151:141–152CrossRefGoogle Scholar
  76. Raab A, Ferreira K, Meharg AA et al (2007) Can arsenic-phytochelatin complex formation be used as an indicator for toxicity in Helianthus annuus? J Exp Bot 58:1333–1338PubMedCrossRefGoogle Scholar
  77. Rausch C, Daram P, Brunner S et al (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466PubMedCrossRefGoogle Scholar
  78. Sharples JM, Chambers SM, Meharg AA et al (2000) Genetic diversity of root-associated fungal endophytes from Calluna vulgaris at contrasting field sites. New Phytol 148:153–162CrossRefGoogle Scholar
  79. Sharples JM, Meharg AA, Chambers SM et al (1999) Arsenate sensitivity in ericoid and ectomycorrhizal fungi. Environ Toxicol Chem 18:1848–1855CrossRefGoogle Scholar
  80. Sharples JM, Meharg AA, Chambers SM et al (2001) Arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. New Phytol 151:265–270CrossRefGoogle Scholar
  81. Shin H, Shin HS, Dewbre GR et al (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
  82. Singh N, Ma LQ, Srivastava MM et al (2006) Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L and Pteris ensiformis L. Plant Sci 170:274–282CrossRefGoogle Scholar
  83. Smith E, Naidu R, Alston AM (1998) Arsenic in the soil environment: a review. Adv Agron 64:149–195CrossRefGoogle Scholar
  84. Smith E, Smith J, Naidu R (2006) Distribution and nature of arsenic along former railway corridors of South Australia. Sci Tot Environ 363:175–182CrossRefGoogle Scholar
  85. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol doi:10.1111/j.1469-8137.2008.02753.x
  86. Smith FW, Mudge SR, Rae AL et al (2003a) Phosphate transport in plants. Plant Soil 248:71–83CrossRefGoogle Scholar
  87. Smith SE, Dickson S, Smith FA (2001) Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Aust J Plant Physiol 28:683–694Google Scholar
  88. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic Press, New York, London, Burlington, San DiegoGoogle Scholar
  89. Smith SE, Smith FA, Jakobsen I (2003b) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20PubMedCrossRefGoogle Scholar
  90. Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524CrossRefGoogle Scholar
  91. Su YH, McGrath SP, Zhu YG et al (2008) Highly efficient xylem transport of arsenite in the arsenic hyperaccumulator Pteris vittata. New Phytol 180:434–441PubMedCrossRefGoogle Scholar
  92. Trappe JM, Stahly EA, Benson NR et al (1973) Mycorrhizal deficiency of apple trees in high arsenic soils. Hortscience 8:52–53Google Scholar
  93. Tripathi RD, Srivastava S, Mishra S et al (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotech 25:158–165CrossRefGoogle Scholar
  94. Trotta A, Falaschi P, Cornara L et al (2006) Arbuscular mycorrhizae increase the arsenic translocation factor in the As hyperaccumulating fern Pteris vitatta L. Chemosphere 65:74–81PubMedCrossRefGoogle Scholar
  95. Tuan LQ, Huong TTT, Hong PTA et al (2008) Arsenic (V) induces a fluidization of algal cell and liposome membranes. Toxicol In Vitro 22:1632–1638CrossRefGoogle Scholar
  96. 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 L. J Exp Bot 40:119–128CrossRefGoogle Scholar
  97. Ultra VU, Tanaka S, Sakurai K et al (2007a) Arbuscular mycorrhizal fungus (Glomus aggregatum) influences biotransformation of arsenic in the rhizosphere of sunflower (Helianthus annuus L.). Soil Sci Plant Nutr 53:499–508CrossRefGoogle Scholar
  98. Ultra VU, Tanaka S, Sakurai K et al (2007b) Effects of arbuscular mycorrhiza and phosphorus application on arsenic toxicity in sunflower (Helianthus annuus L.) and on the transformation of arsenic in the rhizosphere. Plant Soil 290:29–24CrossRefGoogle Scholar
  99. Vetterlein D, Szegedi K, Ackerman J et al (2007) Competitive mobilization of phosphate and arsenate associated with goethite by root activity. J Environ Qual 36:1811–1820PubMedCrossRefGoogle Scholar
  100. Wang JR, Zhao FJ, Meharg AA et al (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561PubMedCrossRefGoogle Scholar
  101. Wells BR, Glilmour JT (1977) Sterility in rice cultivars as influenced by MSMA rate and water management. Agron J 69:451–454CrossRefGoogle Scholar
  102. Westheimer FH (1987) Why nature chose phosphates. Science 235:1173–1178PubMedCrossRefGoogle Scholar
  103. Woolson EA, Axley JH, Kearney PC (1973) The chemistry and phytotoxicity of arsenic in soils. II effects of time and phosphorus. Soil Sci Soc Am. Proc 37:254–259Google Scholar
  104. Wright W, Fitter A, Meharg A (2000) Reproductive biomass in Holcus lanatus clones that differ in their phosphate uptake kinetics and mycorrhizal colonization. New Phytol 146:493–501CrossRefGoogle Scholar
  105. Xia YS, Chen BD, Christie P et al (2007) Arsenic uptake by arbuscular mycorrhizal maize (Zea mays L.) grown in an arsenic-contaminated soil with added phosphorus. J Environ Sci 19:1245–1251CrossRefGoogle Scholar
  106. Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176:590–599PubMedCrossRefGoogle Scholar
  107. Zhao FJ, Ma JF, Meharg AA et al (2008) Arsenic uptake and metabolism in plants. New Phytol 181:777–794CrossRefGoogle Scholar
  108. Zhao FJ, Wang JR, Barker JHA et al (2003) The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol 159:403–410CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Sally E. Smith
    • 1
  • Helle M. Christophersen
    • 1
  • Suzanne Pope
    • 1
  • F. Andrew Smith
    • 1
  1. 1.Soil and Land Systems, School of Earth and Environmental Sciences, Waite CampusThe University of AdelaideAdelaideAustralia

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