Environmental Science and Pollution Research

, Volume 22, Issue 9, pp 6570–6577 | Cite as

Influence of Rhizophagus irregularis inoculation and phosphorus application on growth and arsenic accumulation in maize (Zea mays L.) cultivated on an arsenic-contaminated soil

  • I. CattaniEmail author
  • G. M. Beone
  • C. Gonnelli
Research Article


Southern Tuscany (Italy) is characterized by extensive arsenic (As) anomalies, with concentrations of up to 2000 mg kg soil−1. Samples from the location of Scarlino, containing about 200 mg kg−1 of As, were used to study the influence of the inoculation of an arbuscular mycorrhizal (AM) fungus (Rhizophagus irregularis, previously known as Glomus intraradices) and of phosphorus (P) application, separately and in combination, on As speciation in the rhizosphere of Zea mays on plant growth and As accumulation. Also, P distribution in plant parts was investigated. Each treatment produced a moderate rise of As(III) in the rhizosphere, increased As(III) and lowered As(V) concentration in shoots. P treatment, alone or in combination with AM, augmented the plant biomass. The treatments did not affect total As concentration in the shoots (with all the values <1 mg kg−1 dry weight), while in the roots it was lowered by P treatment alone. Such decrease was probably a consequence of the competition between P and As(V) for the same transport systems, interestingly nullified by the combination with AM treatment. P concentration was higher with AM only in both shoots and roots. Therefore, the obtained results can be extremely encouraging for maize cultivation on a marginal land, like the one studied.


Arsenic Maize Arbuscular mycorrhiza Phosphorus Rhizobox Arsenic speciation 



The authors wish to thank Roberto M. De Santis, Vincenza Cozzolino, Massimo Pigna and Antonio Violante (Dipartimento di Scienza del Suolo, della Pianta, dell’Ambiente e delle Produzioni Animali- Università degli Studi di Napoli Federico II, Portici (NA), Italy) for their support in this work.


  1. Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128CrossRefGoogle Scholar
  2. Adriano DC (2001) Trace elements in terrestrial environment; biogeochemistry, bioavailability and risks of metals. Springer, New YorkGoogle Scholar
  3. Arnetoli M, Vooijs R, Ten Bookum W, Galardi F, Gonnelli C, Gabbrielli R, Schat H, Verkleij JAC (2008) Arsenate tolerance in Silene paradoxa does not rely on phytochelatin-dependent sequestration. Environ Poll 152:585–591CrossRefGoogle Scholar
  4. Bai J, Lin X, Yin R, Zhang H, Junhua W, Xueming C, Yongming L (2008) The influence of arbuscular mycorrhizal fungi on As and P uptake by maize (Zea mays L.) from As-contaminated soils. Appl Soil Ecol 38:137–145CrossRefGoogle Scholar
  5. Bhattacharya P, Samal AC, Majumdar J, Santra SC (2010) Arsenic contamination in rice, wheat, pulses and vegetables: a study in an arsenic affected area of West Bengal. India Water Air Soil Poll 213:3–13CrossRefGoogle Scholar
  6. Carbonell-Barachina AA, Arabi MA, De Laune RD, Gembrell RP, Patrick WH Jr (1998) The influence of arsenic chemical forms and concentrations on Spartina patens and Spartina alternifolia growth and tissue arsenic concentration. Plant Soil 198:33–43CrossRefGoogle Scholar
  7. Cattani I, Fragoulis G, Boccelli R, Capri E (2006) Copper bioavailability in the Zea mays rhizosphere of two Italian soils. Chemosphere 64:1972–1979CrossRefGoogle Scholar
  8. Cattani I, Capri E, Boccelli R, Del Re AAM (2009) Assessment of arsenic availability to roots in contaminated Tuscany soils by a diffusion gradient in thin films (DGT) method and uptake by Pteris vittata and Agrostis capillaris. Eur J Soil Sci 60:539–548CrossRefGoogle Scholar
  9. Cavagnaro T, Smith F, Smith S, Jakobsen I (2005) Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant Cell Environ 28:642–650CrossRefGoogle Scholar
  10. Chatain V, Bayard R, Sanchez F, Moszkowicz P, Gourdon R (2005) Effect of indigenous bacterial activity on arsenic mobilization under anaerobic conditions. Environ Int 31:221–226CrossRefGoogle Scholar
  11. Chen R, Smith BW, Winefordner JD, Tu MS, Kertulis G, Ma LQ (2004) Arsenic speciation in Chinese brake fern by ion pair high-performance liquid chromatography–inductively coupled plasma mass spectroscopy. Anal Chim Acta 504:199–207CrossRefGoogle Scholar
  12. Chen BD, Zhu YG, Smith FA (2006) Effects of arbuscular mycorrhizal inoculation on uranium and arsenic accumulation by Chinese brake fern (Pteris vittata L.) from an uranium mining-impacted soil. Chemosphere 62:1464–1473CrossRefGoogle Scholar
  13. Dahal BM, Fuerhacker M, Mentler A, Karki KB, Shrestha RR, Blum WE (2008) Arsenic contamination of soils and agricultural plants through irrigation water in Nepal. Environ Poll 155:157–163CrossRefGoogle Scholar
  14. 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
  15. 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
  16. Fitz WJ, Wenzel WW, Wieshammer G, Istenic B (2003) Microtome sectioning causes artifacts in rhizobox experiment. Plant Soil 256:455–462CrossRefGoogle Scholar
  17. Gaw SK, Kim ND, Northcoot GL, Wilkins AL, Robinson G (2008) Uptake of ΣDDT, arsenic, cadmium, copper and lead by lettuce and radish grown in contaminated horticultural soils. J Agric Food Chem 56:6584–6593CrossRefGoogle Scholar
  18. Gonzalez-Chavez C, Harris PJ, Dodd J, Meharg AA (2002) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171CrossRefGoogle Scholar
  19. Gulz PA, Gupta S, Schulin R (2005) Arsenic accumulation of common plants from contaminated soils. Plant Soil 272:337–347CrossRefGoogle Scholar
  20. Harrison AP, Cattani I, Turfa JM (2010) Metallurgy, environmental pollution and the decline of Etruscan civilisation. Environ Sci Pollut Res 17:165–180CrossRefGoogle Scholar
  21. Huang RQ, Gao SF, Wang WL, Staunton S, Wang G (2006) Soil arsenic availability and the transfer of soil arsenic to crops in suburban areas in Fujian Province, southeast China. Sci Tot Environ 368:531–541CrossRefGoogle Scholar
  22. Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133:1–16CrossRefGoogle Scholar
  23. Jackson BP, Miller WP (2000) Effectiveness of phosphate and hydroxide for desorption of arsenic and selenium species from iron oxides. Soil Sci Soc Am J 64:1616–1622CrossRefGoogle Scholar
  24. Kabata-Pendias A, Pendias H (2001) Trace elements in soils, 3rd edn. CRC, Boca Raton, 413 ppGoogle Scholar
  25. Lambkin DC, Alloway BJ (2003) Arsenate-induced phosphate release from soils and its effect on plant phosphorus. Water Air Soil Poll 144:41–56CrossRefGoogle Scholar
  26. Luster J, Göttlein A, Sarret G, Nowack B (2009) Sampling, defining, characterising and modeling the rhizosphere—the soil science toolbox. Plant Soil 321:457–482CrossRefGoogle Scholar
  27. Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235CrossRefGoogle Scholar
  28. Markley CT, Herbert BE (2009) Arsenic risk assessment: the importance of speciation in different hydrologic systems. Water Air Soil Poll 204:385–398CrossRefGoogle Scholar
  29. Mascaro I, Benvenuti M, Corsini F, Costagliola P, Lattanti P, Parrini P, Tanelli G (2001) Mine wastes at the polymetallic deposit of Fenice Capanne (Southern Tuscany, Italy). Mineralogy, geochemistry and environmental impact. Environ Geol 41:417–429CrossRefGoogle Scholar
  30. Mathimaran N, Ruh R, Vullioud P, Frossard E, Jansa J (2005) Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza 16:61–66CrossRefGoogle Scholar
  31. Meharg AA, Naylor J, Macnair MR (1994) Phosphorus nutrition of arsenate-tolerant and nontolerant phenotypes of velvetgrass. J Environ Qual 23:234–238CrossRefGoogle Scholar
  32. Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol 154:29–43CrossRefGoogle Scholar
  33. Norvell WA, Cary EE (1992) Potential errors caused by roots in analyses of rhizosphere soil. Plant Soil 143:223–231CrossRefGoogle Scholar
  34. Orlowska E, Godzik B, Turnau K (2012) Effect of different arbuscular mycorrhizal fungal isolates on growth and arsenic accumulation in Plantago lanceolata L. Environ Poll 168:121–130CrossRefGoogle Scholar
  35. Paik MK, Kim MJ, Kim WI, Yoo JH, Park BJ, Im GJ, Park JE, Hong MK (2010) Determination of arsenic in polished rice using a methanol–water digestion method. J Korean Soc Appl Biol Chem 53:634–638CrossRefGoogle Scholar
  36. Philips J, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  37. Pigna M, Cozzolino V, Violante A, Meharg AA (2009) Influence of phosphate on the arsenic uptake by wheat (Triticum durum L.) irrigated with arsenic solutions at three different concentrations. Water Air Soil Poll 197:371–380CrossRefGoogle Scholar
  38. Puckett EE, Serapiglia MJ, DeLeon AM, Long S, Minocha R, Smart LB (2012) Differential expression of genes encoding phosphate transporters contributes to arsenic tolerance and accumulation in shrub willow (Salix spp.). Environ Exp Bot 75:248–257CrossRefGoogle Scholar
  39. Rahman MM, Chen Z, Naidu R (2009) Extraction of arsenic species in soils using microwave-assisted extraction detected by ion chromatography coupled to inductively coupled plasma mass spectrometry. Environ Geochem Health 31:93–102CrossRefGoogle Scholar
  40. S.A.S. Institute, SAS/STAT user’s guide. Version 6, vols. 1 and 2, 4th ed., SAS Inst., Cary, NC, 1996Google Scholar
  41. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, LondonGoogle Scholar
  42. Ultra VU, Tanaka S, Sakurai K, Iwasaki K (2007) 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 290:29–41CrossRefGoogle Scholar
  43. Valberg PA, Beck BD, Bowers TS, Keating JL, Bergstrom PD, Boardman PD (1997) Issues in setting health-based cleanup levels for arsenic in soil. Reg Tox Pharm 26:219–229CrossRefGoogle Scholar
  44. Van den Broeck K, Vandecasteele C, Geuns JMC (1998) Speciation by liquid chromatography-inductively coupled plasma-mass spectrometry of arsenic in mung bean seedlings used as a bio-indicator for arsenic contamination. Anal Chim Acta 361:101–111CrossRefGoogle Scholar
  45. Wang Z-H, Zhang J-L, Christie P, Li X-L (2008) Influence of inoculation with Glomus mosseae or Acaulospora morrowiae on arsenic uptake and translocation by maize. Plant Soil 311:235–244CrossRefGoogle Scholar
  46. Wenzel WW, Wieshammer G, Fitz WJ, Pushenreiter M (2001) Novel rhizoboz design to assess rhizosphere characteristics at high spatial resolution. Plant Soil 237:37–45CrossRefGoogle Scholar
  47. Xia YS, Chen BD, Christie P, Smith FA, Wang YS, Li XL (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
  48. Yan JZ, Ying WY, XiaoLi R (2013) Arsenic uptake accumulation characteristics in varied crops. J South Agric 44:793–796Google Scholar
  49. Yu Y, Zhang S, Huang H, Luo L, Wien B (2009) Arsenic accumulation and speciation in maize as affected by inoculation with arbuscular mycorrhizal fungus Glomus mosseae. J Agric Food Chem 57:3695–3701CrossRefGoogle Scholar
  50. Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Istituto di Chimica Agraria ed AmbientaleUniversità Cattolica del Sacro CuorePiacenzaItaly
  2. 2.Dipartimento di BiologiaUniversità degli Studi di FirenzeFlorenceItaly

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