The effect of EDDS chelate and inoculation with the arbuscular mycorrhizal fungus Glomus intraradices on the efficacy of lead phytoextraction by two tobacco clones

Abstract Two pot experiments were conducted to investigate the effect of inoculation with the arbuscular mycorrhizal (AM) fungus Glomus intraradices on Pb uptake by two clones of Nicotiana tabacum plants. Non-transgenic tobacco plants, variety Wisconsin 38, were compared in terms of Pb uptake with transgenic plants of the same variety with inserted gene coding for polyhistidine anchor in fusion with yeast metallothionein. Bioavailability of Pb in experimentally contaminated soil was enhanced by the application of a biodegradable chelate ethylenediaminedissuccinate (EDDS). EDDS addition (2.5 and 5.0 mmol kg−1 substrate) increased Pb uptake from the substrate and enhanced Pb translocation from the roots to the shoots, with shoot Pb concentrations reaching up to 800 mg kg−1 at the higher chelate dose. Application of a single dose of 5 mmol kg−1 proved to be more efficient at increasing shoot Pb concentrations than two successive doses of 2.5 mmol kg−1, in spite of a marked negative effect on plant growth and phytotoxicity symptoms. Pb amendment (1.4 g kg−1 substrate) connected with either dose of EDDS decreased significantly plant biomass as well as reduced the development of AM fungi. AM inoculation promoted the growth of tobacco plants and partly alleviated the negative effect of Pb contamination, mainly in the case of root biomass. No consistent difference in Pb uptake was found between transgenic and non-transgenic tobacco plants. The effect of AM inoculation on Pb concentrations in plant biomass varied between experiments, with no effect observed in the first experiment and significantly higher root Pb concentrations and increased root–shoot ratio of Pb concentrations in the biomass of inoculated plants in the second experiment. Due to probable retention of Pb in fungal mycelium, the potential of AM for phytoremediation resides rather in Pb stabilisation than in phytoextraction.

[1]  N. Karagiannidis,et al.  The mycorrhizal fungus Glomus mosseae enhances growth, yield and chemical composition of a durum wheat variety in 10 different soils , 1998, Nutrient Cycling in Agroecosystems.

[2]  Manuela Giovannetti,et al.  AN EVALUATION OF TECHNIQUES FOR MEASURING VESICULAR ARBUSCULAR MYCORRHIZAL INFECTION IN ROOTS , 1980 .

[3]  C. Hamel,et al.  Measurement of development of endomycorrhizal mycelium using three different vital stains. , 1990, The New phytologist.

[4]  Domy C. Adriano,et al.  Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability, and Risks of Metals , 2001 .

[5]  Y. Wong,et al.  The isolation and characterization of Type 1 metallothionein (MT) cDNA from a heavy-metal-tolerant plant, Festuca rubra cv. Merlin , 2003 .

[6]  D. Barałkiewicz,et al.  Enhancing phytoremediative ability of Pisum sativum by EDTA application. , 2003, Phytochemistry.

[7]  D. Adriano.  Trace elements in terrestrial environments , 2001 .

[8]  Tomas Macek,et al.  Cadmium tolerance and accumulation in transgenic tobacco plants with a yeast metallothionein combined with a polyhistidine tail , 2004 .

[9]  D. J. Walker,et al.  A plant genetically modified that accumulates Pb is especially promising for phytoremediation. , 2003, Biochemical and biophysical research communications.

[10]  G. Bañuelos,et al.  Phytoremediation of Contaminated Soil and Water , 1999 .

[11]  B. Kos,et al.  Influence of a biodegradable ([S,S]-EDDS) and nondegradable (EDTA) chelate and hydrogel modified soil water sorption capacity on Pb phytoextraction and leaching , 2003, Plant and Soil.

[12]  Daniel Hammer,et al.  Root development and heavy metal phytoextraction efficiency: comparison of different plant species in the field , 2003, Plant and Soil.

[13]  C. Leyval,et al.  Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays L.) in pot culture with contaminated soil , 1995, Mycorrhiza.

[14]  R. E. Koske,et al.  A modified procedure for staining roots to detect VA mycorrhizas , 1989 .

[15]  Enzo Lombi,et al.  Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils , 2001, Plant and Soil.

[16]  D. Sylvia.  Activity of external hyphae of vesicular-arbuscular mycorrhizal fungi , 1988 .

[17]  M. Kaldorf,et al.  The Zinc Violet and its Colonization by Arbuscular Mycorrhizal Fungi , 1999 .

[18]  Xiao-dong Wang,et al.  Effects of interactions between cadmium and zinc on phytochelatin and glutathione production in wheat (Triticum aestivum L.) , 2005, Environmental toxicology.

[19]  G. Feng,et al.  Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc , 2004, Plant and Soil.

[20]  S. Greipsson,et al.  Effect of Arbuscular Mycorrhizal Fungi on Phytoextraction by Corn (Zea mays) of Lead-Contaminated Soil , 2004, International journal of phytoremediation.

[21]  R. A. Scott,et al.  Engineered Single-Chain, Antiparallel, Coiled CoilMimics the MerR Metal BindingSite , 2004, Journal of Bacteriology.

[22]  E. Pilon-Smits,et al.  Phytoremediation of Metals Using Transgenic Plants , 2002 .

[23]  N. Nikolaou,et al.  Influence of Arbuscular Mycorrhizae on Heavy Metal (Pb and Cd) Uptake, Growth, and Chemical Composition of Vitis vinifera L. (cv. Razaki) , 2000, American Journal of Enology and Viticulture.

[24]  S. D. Cunningham,et al.  Chelate-Assisted Pb Phytoextraction: Pb Availability, Uptake, and Translocation Constraints , 1999 .

[25]  I. Jakobsen,et al.  External hyphae of vesicular arbuscular mycorrhizal fungi associated with trifolium subterraneum l. 1. spread of hyphae and phosphorus inflow into roots , 1992 .

[26]  T. Macek,et al.  Arbuscular mycorrhiza decreases cadmium phytoextraction by transgenic tobacco with inserted metallothionein , 2005, Plant and Soil.

[27]  G. Díaz,et al.  Effect of native and introduced arbuscular mycorrhizal fungi on growth and nutrient uptake ofLygeum spartum andAnthyllis cytisoides , 1995, Biologia Plantarum.

[28]  J. Barea,et al.  Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. , 2003, Canadian journal of microbiology.

[29]  A. Bajguz.  Brassinosteroids and lead as stimulators of phytochelatins synthesis in Chlorella vulgaris , 2002 .

[30]  M. Gryndler,et al.  Effects of inoculation with Glomus intraradices on lead uptake by Zea mays L. and Agrostis capillaris L. , 2003 .

[31]  Kazuki Saito,et al.  Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase , 2004, Biotechnology Letters.

[32]  A. Kuhn,et al.  Selective Element Deposits in Maize Colonized by a Heavy Metal Tolerance Conferring Arbuscular Mycorrhizal Fungus , 1999 .

[33]  J. Rydlová,et al.  Effectiveness of indigenous and non-indigenous isolates of arbuscular mycorrhizal fungi in soils from degraded ecosystems and man-made habitats , 2000 .

[34]  R. Schulin,et al.  Zinc Extraction potential of two common crop plants, Nicotiana tabacum and Zea mays , 2002, Plant and Soil.

[35]  T. Macek,et al.  Influence of arbuscular mycorrhiza on the growth and cadmium uptake of tobacco with inserted metallothionein gene , 2005 .

[36]  J. Barea,et al.  Assessing the tolerance to heavy metals of arbuscular mycorrhizal fungi isolated from sewage sludge-contaminated soils , 1999 .

[37]  Qingren Wang,et al.  Enhanced uptake of soil Pb and Zn by Indian mustard and winter wheat following combined soil application of elemental sulphur and EDTA , 2004, Plant and Soil.

[38]  B. Kos,et al.  EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity , 2001, Plant and Soil.

[39]  B. Dehn,et al.  Influence of VA mycorrhizae on the uptake and distribution of heavy metals in plants , 1990 .

[40]  T. Macek,et al.  Phytoremediation—Biological Cleaning of a Polluted Environment , 2004, Reviews on environmental health.

[41]  J. Rydlová,et al.  Effect ofGlomus intraradices isolated from Pb-contaminated soil on Pb uptake byAgrostis capillaris is changed by its cultivation in a metal-free substrate , 2003, Folia Geobotanica.

[42]  Scott D. Cunningham,et al.  Phytoremediation of contaminated soils , 1995 .

[43]  Meetu Gupta,et al.  Lead induced changes in glutathione and phytochelatin in Hydrilla verticillata (l.f.) royle , 1995 .

[44]  Xiao-rong Wang,et al.  Effects of Interaction Between Cadmium and Plumbum on Phytochelatins and Glutathione Production in Wheat （Triticum aestivum L.） , 2005 .

[45]  N. Zawia,et al.  NMR identification of heavy metal-binding sites in a synthetic zinc finger peptide: toxicological implications for the interactions of xenobiotic metals with zinc finger proteins. , 2001, Toxicology and applied pharmacology.

[46]  Scott D. Cunningham,et al.  Phytoremediation of Lead-Contaminated Soils: Role of Synthetic Chelates in Lead Phytoextraction , 1997 .

[47]  Pavel Kotrba,et al.  Accumulation of Cadmium by Transgenic Tobacco , 2002 .

[48]  D. Lestan,et al.  Ethylenediaminedissuccinate as a new chelate for environmentally safe enhanced lead phytoextraction. , 2003, Journal of environmental quality.

[49]  V. Angelova,et al.  Effect of Chemical Forms of Lead, Cadmium, and Zinc in Polluted Soils on Their Uptake by Tobacco , 2004 .

[50]  I. Hwang,et al.  Functional Expression of a Bacterial Heavy Metal Transporter in Arabidopsis Enhances Resistance to and Decreases Uptake of Heavy Metals1[w] , 2003, Plant Physiology.

[51]  M. Firestone,et al.  Vesicular arbuscular mycorrhizal mediation of grass response to acidic and heavy metal depositions , 1983, Plant and Soil.

[52]  G. Díaz,et al.  Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum spartum and Anthyllis cytisoides , 1996, Plant and Soil.

[53]  M. Sunairi,et al.  Genetic improvement of heavy metal tolerance in plants by transfer of the yeast metallothionein gene (CUP1) , 1997, Plant and Soil.