Abstract
The aim of the study was to assess how the extraradical mycelium (ERM) of arbuscular mycorrhizal (AM) fungi contributes to Cd immobilization in the rhizosphere. Substrates prepared by cultivation of AM and non-mycorrhizal tobacco (Nicotiana tabacum L.) in quartz sand in two experiments were amended with Cd in a range of concentrations and Cd immobilization was assessed as Cd toxicity using root growth tests. Split-root plants, inoculated at one part of the root system, and hyphal compartments colonized by ERM only were used to separate the effects of ERM from plant-mediated effects of mycorrhiza and from the effects of roots. AM decreased Cd toxicity in the substrates obtained by 12 weeks of cultivation (Experiment 1), while the effect was less clear after 8 weeks (Experiment 2). No indication was found for an involvement of plant-mediated effects; in contrast, the effect of ERM could be clearly demonstrated. Lower Cd toxicity in the substrates colonized by ERM was related to ERM-induced alkalinization, but not directly to ERM density. It is concluded that the ERM of AM fungi may enhance Cd immobilisation in soil not only due to its high Cd sorption capacity but also by its activity.
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References
Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. Springer-Verlag, New York
An YJ (2004) Soil ecotoxicity assessment using cadmium sensitive plants. Environ Pollut 127:21–26. doi:10.1016/S0269-7491(03)00263-X
Audet P, Charest C (2007) Dynamics of arbuscular mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environ Pollut 147:609–614. doi:10.1016/j.envpol.2006.10.006
Bago B, Azcón-Aguilar C (1997) Changes in the rhizospheric pH induced by arbuscular mycorrhiza formation in onion (Allium cepa L). Z Pflanz Bodenkunde 160:333–339. doi:10.1002/jpln.19971600231
Bago B, Vierheilig H, Piché Y, Azcón-Aguilar C (1996) Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol 133:273–280. doi:10.1111/j.1469-8137.1996.tb01894.x
Bethlenfalvay GJ, Andrade G, Azcón-Aguilar C (1997) Plant and soil responses to mycorrhizal fungi and rhizobacteria in nodulated or nitrate-fertilized peas (Pisum sativum L.). Biol Fertil Soils 24:164–168. doi:10.1007/s003740050225
Bi YL, Li XL, Christie P (2003) Influence of early stages of arbuscular mycorrhiza on uptake of zinc and phosphorus by red clover from a low-phosphorus soil amended with zinc and phosphorus. Chemosphere 50:831–837. doi:10.1016/S0045-6535(02)00227-8
Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117
Chen BD, Christie P, Li XL (2001) A modified glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza. Chemosphere 42:185–192. doi:10.1016/S0045-6535(00)00124-7
Christie P, Li X, Chen BD (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261:209–217. doi:10.1023/B:PLSO.0000035542.79345.1b
Cornu JY, Staunton S, Hinsinger P (2007) Copper concentration in plants and in the rhizosphere as influenced by the iron status of tomato (Lycopersicum esculentum L.). Plant Soil 292:63–70. doi:10.1007/311104-007-9202-Z
Giovannetti M, Mosse B (1980) An evaluation of techniques to measure vesicular-arbuscular infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x
Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122. doi:10.1007/s00425-006-0225-0
Gryndler M, Vejsadová H, Vančura V (1992) The effect of magnesium ions on the vesicular-arbuscular mycorrhizal infection of maize roots. New Phytol 122:455–460. doi:10.1111/j.1469-8137.1992.tb00073.x
Hinsinger P (2001) Bioavailability of trace elements as related to root-induced chemical changes in the rhizosphere. In: Gobran GR, Wenzel WW, Lombi E (eds) Trace Elements in the Rhizosphere. CRC, Boca Raton, pp 25–42
Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59. doi:10.1023/A:1022371130939
Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120:509–516. doi:10.1111/j.1469-8137.1993.tb03797.x
Janoušková M, Pavlíková D, Macek T, Vosátka M (2005) Arbuscular mycorrhiza decreases cadmium phytoextraction by transgenic tobacco with inserted metallothionein. Plant Soil 272:29–40. doi:10.1007/s11104-004-3847-7
Janoušková M, Pavlíková D, Vosátka M (2006) Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil. Chemosphere 65:1959–1965. doi:10.1016/j.chemosphere.2006.07.007
Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234. doi:10.1023/A:1026565701391
Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480. doi:10.1111/j.1469-8137.2004.01130.x
Kapoor R, Bhatnagar AK (2007) Attenuation of cadmium toxicity in mycorrhizal celery (Apium graveolens L.). World J Microbiol Biotechnol 23:1083–1089. doi:10.1007/s11274-006-9337-8
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505. doi:10.1016/S0953-7562(89)80195-9
Leyval C, Joner EJ (2001) Bioavailability of heavy metals in the mycorrhizosphere. In: Gobran GR, Wenzel WW, Lombi E (eds) Trace elements in the rhizosphere. CRC, Boca Raton, pp 165–185
Li XL, Christie P (2001) Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 42:201–207. doi:10.1016/S0045-6535(00)00126-0
Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 251:279–289. doi:10.1023/A:1023034825871
Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69–112
Michaud AM, Bravin MN, Galleguillos M, Hinsinger P (2007) Copper uptake and phytotoxicity as assessed in situ for durum wheat (Triticum turgidum durum L.) cultivated in Cu-contaminated, former vineyard soils. Plant Soil 298:99–111. doi:10.1007/s11104-007-9343-0
Redon PO, Béguiristain T, Leyval C (2008) Influence of Glomus intraradices on Cd partitioning in a pot experiment with Medicago truncatula in four contaminated soils. Soil Biol Biochem 40:2710–2712. doi:10.1016/j.soilbio.2008.07.018
Rivera-Becerril F, Calantzis C, Turnau K, Caussane JP, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185. doi:10.1093/jexbot/53.371.1177
Rufyikiri G, Thiry Y, Declerck S (2003) Contribution of hyphae and roots to uranium uptake and translocation by arbuscular mycorrhizal carrot roots under root-organ culture conditions. New Phytol 158:391–399. doi:10.1046/j.1469-8137.2003.00747.x
Rydlová J, Vosátka M (2003) Effect of Glomus intraradices isolated form Pb-contaminated soil on Pb uptake by Agrostis capillaris is changed by its cultivation in a metal-free substrate. Folia Geobot 38:155–165
Shen H, Christie P, Li X (2006) Uptake of zinc, cadmium and phosphorus by arbuscular mycorrhizal maize (Zea mays L.) from a low available phosphorus calcareous soil spiked with zinc and cadmium. Environ Geochem Health 28:111–119. doi:10.1007/s10653-005-9020-2
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, Oxford
Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170. doi:10.1007/s00572-002-0219-0
Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408. doi:10.1007/s11104-008-9686-1
Youssef RA, Chino M (1989) Root-induced changes in the rhizosphere of plants. I. pH chnages in relation to the bulk soil. Soil Sci Plant Nutr 35:461–468. doi:10.1002/jpln.19861490408
Acknowledgements
Financial support for this study was mainly provided by the Grant Agency of the Academy of Sciences of the Czech Republic (project No. KJB600050706) and by the institutional projects AV0Z60050516 (Grant Agency of the Academy of Sciences of the Czech Republic) and MSM 6046070901 (Ministry of Education, Youth and Sports of the Czech Republic). We are also grateful to M. Opičková for excellent technical assistance, T. Frantík for advice on statistical analyses and R. Sudová, J. Rydlová, D. Püschel for useful comments on earlier drafts of the manuscript.
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Janoušková, M., Pavlíková, D. Cadmium immobilization in the rhizosphere of arbuscular mycorrhizal plants by the fungal extraradical mycelium. Plant Soil 332, 511–520 (2010). https://doi.org/10.1007/s11104-010-0317-2
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DOI: https://doi.org/10.1007/s11104-010-0317-2