Skip to main content
SpringerLink
Log in

Effects of arbuscular mycorrhiza and phosphorus application on arsenic toxicity in sunflower (Helianthus annuus L.) and on the transformation of arsenic in the rhizosphere

  • Original paper
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Effects of arbuscular mycorrhiza (AM) and phosphorus (P) application on arsenic (As) toxicity were studied in a rhizobox system with As-contaminated soil collected from Shimane Prefecture, Japan. The treatments consisted of a combination of two levels of AM (Glomus aggregatum) inoculation (−AM and +AM) and two levels of P application (−P and +P at 30 mg P kg−1). Sunflower (Helianthus annuus L.) seedlings were cultured in rhizoboxes for 6 weeks. Rates of root AM infection in +AM treatments were about 40% regardless of P application. AM inoculation as well as P application reduced As toxicity symptoms, most clearly so in the +AM−P treatment. Plant growth was highest in the +AM + P treatment. Shoot As concentrations were slightly reduced by AM inoculation but enhanced by P application. Shoot P concentration in the +AM−P treatment was similar to that of +P treatments and was higher than in −AM−P. Analyses of rhizosphere soils at the end of the cultivation period indicated that P application increased water-soluble As (WS−As) in all compartments while AM inoculation increased WS−As in the central compartment only. Both the WS−arsenite [WS−As(III)] and the dominant form, arsenate [WS−As(V)], showed gradients toward the root surface. Dimethylarsine (DMAA) was detected in the +AM treatments only. To our knowledge, this is the first report of the occurrence of DMAA in the mycorrhizosphere. AM inoculation increased WS−P similarly as +P treatments did and promoted acid phosphatase activity in the soil. In conclusion, AM inoculation alleviated the effects of As toxicity by improving P nutrition without increasing As concentrations in the shoots. Moreover, AM appeared to be involved in the transformation of soil inorganic As into less toxic organic forms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abedin MJ, Cotter-Howells J, Meharg AA (2002) Arsenic uptake and accumulation in rice (Oryza sativa L.) irrigated with contaminated water. Plant Soil 240:311–319

    Article  CAS  Google Scholar 

  • Alef K, Nannipieri P, Trazar-Cepeda C (1995) Phosphatase activity. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp. 335–344

    Google Scholar 

  • Asher CJ, Reay PF (1979) Arsenic uptake by barley Hordeum vulgare cultivar zephyr seedlings. Aust J Plant Physiol 6:459–466

    Article  CAS  Google Scholar 

  • Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony and bismuth. Microbiol Mol Biol Rev 66:250–271

    Article  PubMed  CAS  Google Scholar 

  • Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorus in soils. Soil Sci 59:39–45

    Article  CAS  Google Scholar 

  • Brundrett M, Melville L, Peterson L (1994) Practical methods in mycorrhiza research. Mycologue Publications, Guelph, Canada 161 pp

    Google Scholar 

  • Caille N, Swanwick S, Zhao FJ, McGrath SP (2004) Arsenic hyperaccumulation by Pteris vittata from arsenic contaminated soils and the effect of liming and phosphate fertilization. Environ Pollut 132:113–120

    Article  PubMed  CAS  Google Scholar 

  • Cao X, Ma LQ, Shiralipoun A (2003) Effect of compost and phosphate amendments on arsenic mobility in soils and arsenic uptake by hyperaccumulator P. vittata L. Environ Pollut 126:157–167

    Article  CAS  Google Scholar 

  • 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 158:165–173

    Article  CAS  Google Scholar 

  • Fitz WJ, Wenzel WW (2002) Arsenic transformation in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. J Biotech 99:259–278

    Article  CAS  Google Scholar 

  • Frankenberger WT, Arshad M (2002) Volatilization of arsenic. In: Frankenberger WT (ed) Environmental chemistry of arsenic. Marcel Dekker Inc., New York, pp. 363–380

    Google Scholar 

  • Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–199

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Goldberg S (2002) Competitive adsorption of arsenate and arsenite on oxides and clay minerals. Soil Sci Soc Am J 66:413–421

    Article  CAS  Google Scholar 

  • Gonzalez-Chavez C, Harris PJ, Dodd J, Meharg AA (2002) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171

    Article  CAS  Google Scholar 

  • Gulz PA, Gupta S, Schulin R (2005) Arsenic accumulation of common plants from contaminated soils. Plant Soil 272:337–347

    Article  CAS  Google Scholar 

  • Holmgren GGS (1967) A rapid citrate–dithionite extractable iron procedure. Soil Sci Soc Am Proc 31:210–211

    Article  CAS  Google Scholar 

  • 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 64:1616–1622

    Article  CAS  Google Scholar 

  • Jiang QQ, Singh BR (1994) Effect of different forms and sources of arsenic crop yield and arsenic concentration. Water Air Soil Pollut 74:321–343

    CAS  Google Scholar 

  • Keon NE, Swartz CH, Brabander DJ, Harvey C, Hemond HF (2001) Validation of an arsenic sequential extraction method for evaluating mobility in sediments. Environ Sci Technol 35:2778–2784

    Article  PubMed  CAS  Google Scholar 

  • Knudson JA, Meikle T, DeLuca TH (2003) Role of mycorrhizal fungi and phosphorus in arsenic tolerance of basin wildrye. J Environ Qual 32:2001–2006

    PubMed  CAS  Google Scholar 

  • Kubicki JD (2005) Comparison of As (III) and As (V) complexation onto Al- and Fe-hydroxides. In: O’day PA, et al (eds) Advances in arsenic research: integration of experimental and observational studies and implication for mitigation. ASC symposium series 915, ACS, Washington, pp. 104–117

    Google Scholar 

  • Lambkin DC, Alloway BJ (2003) Arsenate-induced phosphate release from soils and its effect on plant phosphorus. Water Air Soil Pollut 144:41–56

    Article  CAS  Google Scholar 

  • Leung HM, Ye ZH, Wong MH (2005) Interactions of mycorrhizal fungi with Pteris vittata (As hyperaccumulator) in As-contaminated soils. Environ Pollut 139:1–8

    Article  PubMed  CAS  Google Scholar 

  • Li XL, George E, Marschner H (1991) Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in a calcareous soil. Plant Soil 136:41–48

    Article  Google Scholar 

  • Liu Y, Zhu YG, Chen BD, Christie P, Li LX (2005a) Yield and uptake of arbuscular mycorrhizal tomato colonized by Glomus mosseae BEG167 in As spiked soil under glasshouse conditions. Environ Int 31:867–873

    Article  CAS  Google Scholar 

  • Liu Y, Zhu YG, Chen BD, Christie P, Li LX (2005b) Influence of the arbuscular mycorrhizal fungus Glomus mosseae on uptake of arsenate by the As hyperaccumulator fern Pteris vittata. Mycorrhiza 15:187–192

    Article  CAS  Google Scholar 

  • Lombi E, Wenzel WW, Sletten RS (1999) Arsenic adsorption by soils and iron-oxide-coated sand: kinetics and reversibility. J Plant Nutr Soil Sci 162:451–456

    Article  CAS  Google Scholar 

  • Marin AR, Masscheleyn PH, Patrick WH Jr (1993) Soil redox-pH stability of arsenic species and its influence on arsenic uptake by rice. Plant Soil 152:235–253

    Article  Google Scholar 

  • Masscheleyn PH, Delaune RD, Patric WH Jr (1991) A hydride generation atomic absorption technique for arsenic speciation. J Environ Qual 20:96–100

    CAS  Google Scholar 

  • Meharg AA (2004) Arsenic in rice—understanding a new disaster for south-east Asia. Trends Plant Sci 9:415–417

    Article  PubMed  CAS  Google Scholar 

  • Meharg AA, Naylor J, Macnair MR (1994) Phosphorus nutrition of arsenate-tolerant and nontolerant phenotypes of velvet grass. J Environ Qual 23:234–238

    CAS  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Phung LT, Siver S (2002) Microbial arsenic: from geocycle to gene and enzymes. FEMS Microbiol Rev 26:311–325

    Article  PubMed  CAS  Google Scholar 

  • O’Reilly SE, Strawn DG, Sparks DL (2001) Residence␣time effects on arsenate adsorption/desorption␣mechanisms on goethite. Soil Sci Soc Am J 65: 67–77

    Article  CAS  Google Scholar 

  • Peryea FJ, Kammereck R (1997) Phosphate-enhanced movement of arsenic out of lead arsenic-contaminated topsoil and through uncontaminated subsoil. Water Air Soil Pollut 93:234–254

    Google Scholar 

  • Sakurai K, Tanaka N, Iwasaki K, Tanaka S (2001) Effects of arbuscular mycorrhizal application on the distribution of phosphorus and iron in the rhizosphere soils of sunflower (Helianthus annuus L.). In: Horst WJ et al (eds) Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research. Kluwer Academic Publishers, Dordrecht, pp. 620–621

    Google Scholar 

  • Schmidt AC, Mattusch J, Reisser W, Wennrich R (2004) Uptake and accumulation behavior of angiosperms irrigated with solution of different arsenic species. Chemosphere 56:305–313

    Article  PubMed  CAS  Google Scholar 

  • Schollenberger CJ, Simon RH (1945) Determination of exchange capacity and exchangeable bases in soils. Soil Sci 59:13–24

    Article  CAS  Google Scholar 

  • Sharples JM, Meharg AA, Chambers SM, Cairney JWG (2000) Mechanism of arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. Plant Physiol 124:1327–1334

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London, pp. 126–159

    Google Scholar 

  • Smith SE, Ryan PR, Smith FA (2005) The soil–pant interface: rhizosphere and mycorrhisphere. In: Li CJ et al. (eds) Plant nutrition for food security, human health and environmental protection. Tsinghua University Press, Beijing, China, pp. 456–457

    Google Scholar 

  • Tu S, Ma LQ (2003) Interactive effects of pH, arsenic and phosphorus on uptake of As and P and growth of the arsenic hyperaccumulator Pteris vittata L. under hydroponic conditions. Environ Exp Bot 50:243–251

    Article  CAS  Google Scholar 

  • Turpeinen R, Pantsar-Kallio M, Haggblom M, Kairesalo T (1999) Influence of microbes on the mobilization, toxicity and biomethylation of arsenic in soil. Sci Total Environ 236:173–180

    Article  PubMed  CAS  Google Scholar 

  • Vetterlein D, Szegedi K, Ackermann J, Mattusch J, Neue H-U, Tanneberg H, Jahn R (2005) The impact of rhizosphere processes on As speciation and mobility of arsenic—a case study with goethite. In: Li CJ et al (eds) Plant nutrition for food security, human health and environmental protection. Tsinghua University Press. Beijing, China, pp. 636–637

    Google Scholar 

  • Wenzel WW, Kirchbaumer N, Prohaska T, Stingeder G, Lombi E, Adriano DC (2001) Arsenic fractionation in soils using improved sequential extraction procedure. Anal Chim Acta 436:309–323

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by a Sasakawa Scientific Research Grant (No. 17–207) from The Japan Science Society to VUU and by a grant-in-aid for Scientific Research (B, No. 15380223) from MEXT of Japan to KI. The authors gratefully acknowledge Dr Shingo Matsumoto in Shimane University for his assistance in the sampling of As-contaminated soils.

Author information

Authors and Affiliations

  1. United Graduate School of Agricultural Sciences, Ehime University, Matsuyama , 790-8566, Japan

    V. U. Ultra Jr

  2. Graduate School of Kuroshio Science, Kochi University, Nankoku, Kochi, 783-8502, Japan

    S. Tanaka

  3. Faculty of Agriculture, Kochi University, Nankoku, Kochi, 783-8502, Japan

    K. Sakurai & K. Iwasaki

Authors
  1. V. U. Ultra Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Sakurai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Iwasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Iwasaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ultra, V.U., Tanaka, S., Sakurai, K. et al. 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, 29–41 (2007). https://doi.org/10.1007/s11104-006-9087-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-006-9087-2

Keywords

Search

Navigation