Plant and Soil

, Volume 371, Issue 1–2, pp 199–217 | Cite as

Effects of simultaneous arsenic and iron toxicities on rice (Oryza sativa L.) development, yield-related parameters and As and Fe accumulation in relation to As speciation in the grains

  • Delphine Vromman
  • Stanley LuttsEmail author
  • Isabelle Lefèvre
  • Laurent Somer
  • Olivier De Vreese
  • Zdenka Šlejkovec
  • Muriel Quinet
Regular Article


Background and aim

In numerous areas, rice cultivated under flooded conditions is exposed simultaneously to iron excess and arsenic contamination. The impact of these combined stresses on yield-related parameters and As distribution and speciation in various plant parts remains poorly documented.


Rice (cv I Kong Pao) was exposed to iron excess (125 mg L−1 Fe2SO4), arsenic (50 and 100 μM Na2HAsO4.7H2O) or a combination of those stressing agents in hydroponic culture until harvest. Plant growth, yield-related parameters, non protein thiols concentration and mineral nutrition were studied in roots and shoots. Arsenic speciation was determined by high-performance liquid chromatography-hydride generation-atomic fluorescence spectrometry.

Key Results

Iron excess increased As retention by the roots in relation to the development of the root iron plaque but decreased As accumulation in the shoot. Arsenic concentration was lower in the grains than in the shoots. Iron stress reduced As accumulation in the husk but not in the dehusked grains. Iron excess decreased the proportion of extractable As(III) and As(V) in the grain while it increased the proportion of extractable As(III) in the shoot. Combined stresses (Fe+As) affected plant nutrition and significantly reduced the plant yield by limiting the number of grains per plant and the grain filling.


Fe excess had an antagonist impact on shoot As concentration but an additive negative impact on several yield-related parameters. Iron stress influences both As distribution and As speciation in rice.


Iron plaque Iron stress Arsenic Oryza sativa Rice Rice grain arsenic 



The authors are grateful to the Fonds National de la Recherche Scientifique (FNRS—FRFC; Convention 2.4599.12) for financial support. The authors would like to thank anonymous referees for their valuable help in improving the quality of the manuscript.


  1. Asch F, Becker M, Kpongor DS (2005) A quick and efficient screen for resistance to iron toxicity in lowland rice. J Plant Nutr and Soil Sci 168:764–773CrossRefGoogle Scholar
  2. Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122PubMedGoogle Scholar
  3. Bhattacharya P, Samal AC, Majumbar J, Santra SC (2010) Accumulation of arsenic and its distribution in rice plant (Oryza sativa L.) in Gangetic West Bengal, India. Paddy Water Environ 8:63–70CrossRefGoogle Scholar
  4. Becker M, Asch F (2005) Iron toxicity in rice-conditions and management concepts. J Plant Nutr Soil Sci 168:558–573CrossRefGoogle Scholar
  5. Brammer H, Ravenscroft P (2009) Arsenic in groundwater: a threat to sustainable agriculture in South and South-east Asia. Environ Int 35:647–654PubMedCrossRefGoogle Scholar
  6. Carbonell AA, Aarabi MA, DeLaune RD, Gambrell RP, Patrick WH Jr (1998) Arsenic in wetland vegetation: availability, phytotoxicity, uptake and effects on plant growth and nutrition. Sci Total Environ 217:189–199CrossRefGoogle Scholar
  7. Carey A-M, Scheckel KG, Lombi E, Newville M, Choi Y, Norton GJ, Charnock JM, Feldmann J, Price AH, Meharg A (2010) Grain unloading of arsenic species in rice. Plant Physiol 152:309–319PubMedCrossRefGoogle Scholar
  8. Carey A-M, Lombi E, Donner E, de Jonge MD, Punshon T, Jackson BP, Guerinot ML, Price AH, Meharg AA (2012) A review of recent devopments in the speciation and location of arsenic and selenium in rice grain. Anal Bioanal Chem 402:3275–3286PubMedCrossRefGoogle Scholar
  9. Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D, Kumar S, Rai A, Pandey A, Nigam D, Tripathi RD, Tuli R (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74:688–702PubMedCrossRefGoogle Scholar
  10. Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97PubMedCrossRefGoogle Scholar
  11. Dameron CT, Reese RN, Mehra RK, Kortan AR (1989) Biosynthesis of cadmium-sulfide quantum semiconductor crystallites. Nature 338:596–597CrossRefGoogle Scholar
  12. de Dorlodot S, Lutts S, Bertin P (2005) Effects of ferrous iron toxicity on the growth and mineral composition of an interspecific rice. J Plant Nutr 28:1–20CrossRefGoogle Scholar
  13. Delfosse T, Delmelle P, Givron C, Delvaux B (2005) Inorganic sulphate extraction from SO2-impacted Andosols. Europ J Soil Sci 56:127–133CrossRefGoogle Scholar
  14. Deng D, Wu S-C, Wu Y, Deng H, Wong M-H (2010) Effects of root anatomy and Fe plaque on arsenic uptake by rice seedlings grown in solution culture. Environ Poll 158:2589–2595CrossRefGoogle Scholar
  15. De Vos CHR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubatus. Plant Physiol 98:853–858PubMedCrossRefGoogle Scholar
  16. Fageria NK, Santosa AB, Barbosa Filhoa MP, Guimarãesa CM (2008) Iron toxicity in lowland rice. J Plant Nutr 31:1676–1697CrossRefGoogle Scholar
  17. Feng R, Wei C, Tu S, Tang S, Wu F (2011) Simultaneous hyperaccumulation of arsenic and antimony in Cretan brake fern: evidence of plant uptake and subcellular distributions. Mikrochem J 97:38–43CrossRefGoogle Scholar
  18. Garnier J-M, Travassac F, Lenoble V, Rose J, Zheng Y, Hossain MS, Chowdhury SH, Biswas AK, Ahmed KM, Cheng Z, van Geen A (2010) Temporal variations in arsenic uptake by rice plants in Bangladesh; the role of iron plaque in paddy fields irrigated with groundwater. Sci Total Environ 408:4185–4193PubMedCrossRefGoogle Scholar
  19. Ghanem ME, van Elteren J, Albacete A, Quinet M, Martinéz-Andújar C, Kinet JM, Perez-Alfocea F, Lutts S (2009) Impact of salinity on early reproductive physiology of tomato (Solanum lycopersicum) in relation to a heterogeneous distribution of toxic ions in flowers organs. Funct Plant Biol 36:125–136CrossRefGoogle Scholar
  20. Hansel CM, La Force MJ, Fendorf S, Sutton S (2002) Spatial and temporal association of as and fe species on aquatic plant roots. Environ Sci Technol 36:1988–1994PubMedCrossRefGoogle Scholar
  21. Hartley-Whitaker J, Ainsworth G, Vooijs R, Ten Bookum W, Schat H, Meharg AA (2001) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiol 126:299–306PubMedCrossRefGoogle Scholar
  22. Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551PubMedGoogle Scholar
  23. Hossain M, Islam MR, Jahiruddin M, Abedin A, Islam S, Meharg AA (2007) Effects of arsenic-contaminated irrigation water on growth, yield, and nutrient concentration in rice. Commun Soil Sci Plant Anal 39:302–313CrossRefGoogle Scholar
  24. Hossain M, Jahiruddin M, Loeppert R, Panaullah G, Islam M, Duxbury J (2009) The effects of iron plaque and phosphorus on yield and arsenic accumulation in rice. Plant Soil 317:167–176CrossRefGoogle Scholar
  25. Hu Y, Li J, Zhu Y, Huang Y, Hu H, Christie P (2005) Sequestration of As by iron plaque on the roots of three rice (Oryza sativa L.) cultivars in a low-P soil with or without P fertilizer. Environ Geochem Health 27:169–176PubMedCrossRefGoogle Scholar
  26. Jeong J, Connolly EL (2009) Iron uptake mechanisms in plants: functions of the FRO family of ferric reductases. Plant Sci 176:709–714CrossRefGoogle Scholar
  27. Jeong J, Guerinot ML (2008) Biofortified and bioavailable: the gold standard for plant-base diets. Proc Nat Acad Sci USA 105:1777–1778PubMedCrossRefGoogle Scholar
  28. Kerkeb L, Connolly EL (2006) Iron transport and metabolism in plants. Genet Eng 27:119–139CrossRefGoogle Scholar
  29. Krämer U, Talke I, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272PubMedCrossRefGoogle Scholar
  30. Lee CH, Hsieh YC, Lin TH, Lee DY (2013) Iron plaque formation and its effect on arsenic uptake by different genotypes of rice. Plant Soil 363:231–241CrossRefGoogle Scholar
  31. Liu W, Zhu YG, Smith FA, Smith SE (2004) Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oyza sativa L.) grown in solution culture? J Exp Bot 55:1707–1713PubMedCrossRefGoogle Scholar
  32. Liu WJ, Zhu YG, Hu Y, Williams PN, Gault AG, Meharg AA, Charnock JN, Smith FA (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. Lombi E, Scheckel KG, Pallon J, Carey AM, Zhu YG, Meharg AA (2009) Speciation and distribution of arsenic and localization of nutrients in rice grains. New Phytol 184:193–201PubMedCrossRefGoogle Scholar
  34. Lomax C, Liu WJ, Wu L, Xue K, Xiong J, Zhou J, McGrath SP, Meharg AA, Miller AJ, Zhao FJ (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–672PubMedCrossRefGoogle Scholar
  35. 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. Proc Nat Acad Sci USA 105:9931–9935PubMedCrossRefGoogle Scholar
  36. Majerus V, Bertin P, Lutts S (2007) Effects of iron toxicity on osmotic potential, osmolytes and polyamines concentrations in the African rice (Oryza glaberrima Steud.). Plant Sci 173:96–105CrossRefGoogle Scholar
  37. Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154:29–43CrossRefGoogle Scholar
  38. Mir KA, Rutter A, Koch I, Smith P, Reimer KJ, Poland JS (2007) Extraction and speciation of arsenic in plants grown on arsenic contaminated soils. Talanta 72:1507–1518PubMedCrossRefGoogle Scholar
  39. Moore KL, Schröder M, Wu ZC, Martin BGH, Hawes CR, McGrath SP, Hawkesford MJ, Ma JF, Zhao FJ, Grovenor CRM (2011) High-resolution secondary ion mass spectrometry reveals the contrasting subcellular distribution of arsenic and silicon in roce roots. Plant Physiol 156:913–924PubMedCrossRefGoogle Scholar
  40. Pal R, Rai JPN (2010) Phytochelatins: peptides involved in heavy metal detoxification. Appl Biochem Biotechnol 160:945–963PubMedCrossRefGoogle Scholar
  41. Panaullah G, Alam T, Hossain M, Loeppert R, Lauren J, Meisner C, Ahmed ZU, Duxbury JM (2009) Arsenic toxicity to rice (Oryza sativa L.) in Bangladesh. Plant Soil 317:31–39CrossRefGoogle Scholar
  42. Quinet M, Vromman D, Clippe A, Bertin P, Lequeux H, Dufey I, Lutts S, Lefèvre I (2012) Combined transcriptomic and physiological approaches reveal strong differences between short and long term response of rice (Oryza sativa) to iron toxicity. Plant Cell Environ 35:1837–1859PubMedCrossRefGoogle Scholar
  43. Rahman MA, Hasegawa H (2011) High levels of inorganic arsenic in rice in areas where arsenic-contamined water is used for irrigation and cooking. Sci Total Environ 409:4645–4655PubMedCrossRefGoogle Scholar
  44. 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 84:439–445PubMedCrossRefGoogle Scholar
  45. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181PubMedCrossRefGoogle Scholar
  46. Reese RN, White CA, Wing DR (1992) Cadmium-sulfide crystallites in Cd-gamma-ECnG peptide complexes from tomato. Plant Physiol 98:225–229PubMedCrossRefGoogle Scholar
  47. Sahrawat KL (2004) Iron toxicity in wetland rice and the role of other nutrients. J Plant Nutr 27:1471–1504CrossRefGoogle Scholar
  48. Seyfferth AL, Webbs SM, Andrews JC, Fendorf S (2011) Defining the distribution of arsenic species and plant nutrients in rice (Oryza sativa L.) from the root to the grain. Geochem Cosmochim Acta 75:6655–6671CrossRefGoogle Scholar
  49. Shaibur MR, Kitajima N, Sugawara R, Kondo T, Huq SMI, Kawai S (2006) Physiological and mineralogical properties of arsenic-induced chlorosis in rice seedlings grown hydroponically. Soil Sci Plant Nutr 52:691–700CrossRefGoogle Scholar
  50. Šlejkovec Z, Van Elteren JT (1999) Determination of arsenic compounds in reference materials by HPLC-UV-HGAFS. Talanta 49:619–627PubMedCrossRefGoogle Scholar
  51. Takahashi Y, Minamikawa R, Hattori KH, Kurishima K, Kihou N, Yuita K (2004) Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol 38:1038–1044PubMedCrossRefGoogle Scholar
  52. Thongbai P, Goodman BA (2000) Free radical generation and post-anoxic injury in rice grown in an iron-toxic soil. J Plant Nutr 23:1887–1900CrossRefGoogle Scholar
  53. Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJM (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotech 25:158–165CrossRefGoogle Scholar
  54. Voegelin A, Weber F-A, Kretzschmar R (2007) Distribution and speciation of arsenic around roots in a contaminated riparian floodplain soil: Micro-XRF element mapping and EXAFS spectroscopy. Geochim Cosmochim Acta 71:5804–5820CrossRefGoogle Scholar
  55. Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ, Feldmann J, Meharg AA (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859PubMedCrossRefGoogle Scholar
  56. Wu Z, McGrath SP, Wu P, Zhao F-J (2011) Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 157:498–508PubMedCrossRefGoogle Scholar
  57. Xu XY, McGrath SP, Meharg AA, Zhao FJ (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ Sci Technol 42:5574–5579PubMedCrossRefGoogle Scholar
  58. Yamaguchi N, Nakamura T, Dong D, Takahashi Y, Amachi S, Makino T (2011) Arsenic release from flooded paddy soils is influenced by speciation, Eh, pH, and iron dissolution. Chemosphere 83:925–932PubMedCrossRefGoogle Scholar
  59. Yoshida S, Forno D, Cock J, Gomez K (1976) Laboratory manual for physiological studies of rice. IRRI, PhilippinesGoogle Scholar
  60. Zhao F-J, Ma J, Meharg A, McGrath S (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794PubMedCrossRefGoogle Scholar
  61. Zhao F-J, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Ann Rev Plant Biol 61:535–559CrossRefGoogle Scholar
  62. Zhao F-J, Stroud JL, Khan MA, McGrath SP (2012) Arsenic translocation in rice investigated using radioactive 73As tracer. Plant Soil 350:413–420CrossRefGoogle Scholar
  63. Zhu YG, Williams PN, Meharg AA (2008) Exposure to inorganic arsenic from rice: a global health issue? Environ Poll 154:169–171CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Delphine Vromman
    • 1
  • Stanley Lutts
    • 1
    Email author
  • Isabelle Lefèvre
    • 1
  • Laurent Somer
    • 1
  • Olivier De Vreese
    • 1
  • Zdenka Šlejkovec
    • 2
  • Muriel Quinet
    • 1
  1. 1.Groupe de Recherche en Physiologie végétale (GRPV)Earth and Life Institute – Agronomy (ELI-A), Université catholique de LouvainLouvain-la-NeuveBelgium
  2. 2.Department of Environmental SciencesJožef Stefan InstituteLjubljanaSlovenia

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