The arbuscular mycorrhizal fungus Glomus mosseae can enhance arsenic tolerance in Medicago truncatula by increasing plant phosphorus status and restricting arsenate uptake

A pot experiment examined the biomass and As uptake of Medicago truncatula colonized by the arbuscular mycorrhizal (AM) fungus Glomus mosseae in low-P soil experimentally contaminated with different levels of arsenate. The biomass of G. mosseae external mycelium was unaffected by the highest addition level of As studied (200 mg kg⁻¹) but shoot and root biomass declined in both mycorrhizal and non-mycorrhizal plants, indicating that the AM fungus was more tolerant than M. truncatula to arsenate. Mycorrhizal inoculation increased shoot and root dry weights by enhancing host plant P nutrition and lowering shoot and root As concentrations compared with uninoculated plants. The AM fungus may have been highly tolerant to As and conferred enhanced tolerance to arsenate on the host plant by enhancing P nutrition and restricting root As uptake.     

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

In a pot experiment, red clover (Trifolium pratense) was grown in sterilized Zn-amended low available P soil (0, 50 or 400 mg Zn kg(-1)) with or without 100 mg kg(-1) added P and with or without inoculation with the arbuscular mycorrhizal (AM) fungus G. mosseae. When the plants were harvested after 40 days, AM colonization of the roots was still at an early stage, with only 14-38% of total root length colonized on average. AM colonization was highest in low-P soil, and was lowest in soil amended with 400 mg Zn kg(-1). Shoot yields were highest in AM plants with added P, but root yields were unaffected by AM inoculation. Shoot and root yields were higher with 100 mg added P kg(-1) soil, but lower with 400 mg Zn kg(-1) than 50 mg Zn kg(-1) or controls unamended with Zn. Shoot and root P concentrations were seldom higher in AM plants, but shoot P offtakes were higher in AM plants with added P. Concentrations of Zn and Cu were much higher in the roots than in the shoots. Shoot and root Zn and shoot Cu were lower, but root Cu was higher, in AM plants. Soil residual pH after plant growth was higher in AM treatments, and residual total Zn was also higher, indicating lower Zn uptake by AM plants. Soil solution pH was higher in AM treatments, and soil solution Zn was lower in the presence of mycorrhiza. The results are discussed in terms of AM protection of the plants against excessive shoot Zn uptake.     

Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment

A sand culture experiment was established to determine interactions between arbuscular mycorrhizae and heavy metals. Mycorrhizal infection rates, spore densities, maize root and shoot weights, and heavy metal contents in maize were as indexes of responses of arbuscular mycorrhizal fungi (Acaulospora laevis, Glomus caledonium and Glomus manihotis) to heavy metals (Cu and Cd). The mycorrhizal infection rates of G. caledonium were the highest among these three mycorrhizal fungi, but the sporulating ability of G. caledonium was the poorest in the heavy metal treatments. The shoot and root weights of non-mycorrhizal plants were usually greater than those of mycorrhizal plants when the Cu concentrations in solutions are less than 3 mg l(-1) or Cd concentrations less than 1 mg l(-1). When Cd concentrations were 0.5 and 1 mg(-1), the root and shoot weights of plants inoculated with A. laevis were significantly (p < 0.05) lower than those of other treatments. Copper concentrations in shoots of mycorrhizal plants were higher than those of non-mycorrhizal ones at all Cu concentrations in solution, especially at low Cu concentrations. As to A. laevis, Cu concentrations in roots and shoots of the host were higher than those of non-mycorrhizal plants in these treatments. Thus A. laevis was sensitive to Cu and Cd, especially Cd, and G. caledonium was more tolerant to these two heavy metals. It is suggested that G. caledonium might be a promising mycorrhizal fungus for bioremediation of heavy metal contaminated soil.     

Arbuscular mycorrhizal fungi can decrease the uptake of uranium by subterranean clover grown at high levels of uranium in soil

Subterranean clover inoculated or not with the arbuscular mycorrhizal (AM) fungus Glomus intraradices was grown on soil containing six levels of 238U in the range 0-87 mg kg(-1). Increasing U concentration in soil enhanced the U concentration in roots and shoots of both mycorrhizal and nonmycorrhizal plants but had no significant effects on plant dry matter production or root AM colonization. Mycorrhizas increased the shoot dry matter and P concentration in roots and shoots, while in most cases, it decreased the Ca, Mg and K concentrations in plants. The AM fungus influenced U concentration in plants only in the treatment receiving 87 mg U kg(-1) soil. In this case, U concentration in shoots of nonmycorrhizal plants was 1.7 times that of shoots of mycorrhizal plants. These results suggested that mycorrhizal fungi can limit U accumulation by plants exposed to high levels of U in soil.     

Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake

Plants of the Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen (Brassicaceae) inoculated or not with indigenous arbuscular mycorrhizal (AM) fungal mixture were grown in a highly Cd, Zn and Pb contaminated substrate in order to evaluate the functionality of symbiosis and assess the possible impact of AM colonisation on heavy metal uptake and tolerance. The results suggest AM development in the metal hyperaccumulating T. praecox is favoured at elevated nutrient demands, e.g. during the reproductive period. AM colonisation parameters positively correlated with total soil Cd and Pb. Colonised plants showed significantly improved nutrient and a decreased Cd and Zn uptake as revealed by TRXRF, thus confirming the functionality of the symbiosis. Reduced heavy metal uptake, especially at higher soil metal contents, indicates a changed metal tolerance strategy in colonised T. praecox plants. This is to our knowledge the first report on AM colonisation of the Zn, Cd and Pb hyperaccumulator T. praecox in a greenhouse experiment.     

Saprobe fungi decreased the sensitivity to the toxic effect of dry olive mill residue on arbuscular mycorrhizal plants

We studied the influence of olive mill dry residue (DOR) treated with saprobe fungi on growth of tomato and alfalfa colonized by Glomus deserticola. The application of 25g kg(-1) of dry DOR to soil decreased the shoot and root dry weight of tomato and alfalfa. Plants were more sensitive to the toxicity of DOR when colonized with the arbuscular mycorrhizal (AM) fungi. The sensitivity of both plants to the toxicity of DOR differed according to whether they were colonized by G. deserticola or by indigenous AM fungi. The phytotoxicity of DOR towards tomato and alfalfa was decreased by incubation the residue before planting with saprobe fungi for 20wk. The beneficial effects of AM fungi on plant growth added with DOR incubated with saprobe fungi depend of the type of the plant and AM fungi. The contribution of AM fungi to the beneficial effect of DOR incubated with saprobe fungi varied according to the type of the plant and AM fungi. G. deserticola increased the shoot and root dry weight of plants when they were grown in the presence of DOR incubated with saprobe fungi for 20wk. The beneficial effect of saprobe fungi on the dry weight and the level of AM mycorrhization of plants seem to be related to the decrease caused by these fungi in the phenol concentration in DOR. However, the toxicity of DOR due to substances other than phenols can not be ignored. The use of certain saprobe and AM fungi allows the possibility of using DOR as an organic fertilizer.     

Metallophyte status of violets of the section Melanium

Violets from metal-enriched soils have controversially been described as both heavy-metal accumulators and excluders in the literature. The present study solves the issue for violets of the section Melanium (zinc violets, Viola lutea ssp. calaminaria and V. lutea ssp. westfalica; hartsease or wild pansy, Viola tricolor; and mountain pansy, V. lutea). The aims were to determine the concentrations of heavy metals in the soil and in the roots and shoots of field-collected plants, to evaluate the potential impact of colonisation by arbuscular mycorrhizal fungi on heavy-metal concentrations in the plant tissues, and to quantitatively define the localisation of the elements in root cross-sections. When these violets grow in low-metal soils, higher concentrations of the heavy metals were found in the roots and shoots than in the soil, whereas the opposite was seen in samples from high-metal soils. Under all field conditions examined, the roots of all of these species were colonised by arbuscular mycorrhizal fungi. However, V. tricolor was marginally colonised when the concentrations of Zn and P were higher in the soil. Determination of the spatial distribution of the elements in root cross-sections of these violets indicates tissue-specific deposition of elements within the vascular tissue, the cortex, and the rhizodermis. These data indicate that violets of the section Melanium are heavy-metal excluders.     

The arbuscular mycorrhizal fungus Glomus mosseae induces growth and metal accumulation changes in Cannabis sativa L

The effect of arbuscular mycorrhiza on heavy metal uptake and translocation was investigated in Cannabis sativa. Hemp was grown in the presence and absence of 100 microg g-1 Cd and Ni and 300 microg g-1 Cr(VI), and inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. In our experimental condition, hemp growth was reduced in inoculated plants and the reduction was related to the degree of mycorrhization. The percentage of mycorrhizal colonisation was 42% and 9% in plants grown in non-contaminated and contaminated soil, suggesting a significant negative effect of high metal concentrations on plant infection by G. mosseae. Soil pH, metal bioavailability and plant metal uptake were not influenced by mycorrhization. The organ metal concentrations were not statistically different between inoculated and non-inoculated plants, apart from Ni which concentration was significantly higher in stem and leaf of inoculated plants grown in contaminated soil. The distribution of absorbed metals inside plant was related to the soil heavy metal concentrations: in plant grown in non-contaminated soil the greater part of absorbed Cr and Ni was found in shoots and no significant difference was determined between inoculated and non-inoculated plants. On the contrary, plants grown in artificially contaminated soil accumulated most metal in root organ. In this soil, mycorrhization significantly enhanced the translocation of all the three metals from root to shoot. The possibility to increase metal accumulation in shoot is very interesting for phytoextraction purpose, since most high producing biomass plants, such as non-mycorrhized hemp, retain most heavy metals in roots, limiting their application.     

Phenanthrene uptake by Medicago sativa L. under the influence of an arbuscular mycorrhizal fungus

Phenanthrene uptake by Medicago sativa L. was investigated under the influence of an arbuscular mycorrhizal fungus. Inoculation of lucerne with the arbuscular mycorrhizal fungus Glomus etunicatum L. resulted in higher phenanthrene accumulation in the roots and lower accumulation in the shoots compared to non-mycorrhizal controls. Studies on sorption and desorption of phenanthrene by roots and characterization of heterogeneity of mycorrhizal and non-mycorrhizal roots using solid-state ¹³C nuclear magnetic resonance spectroscopy (¹³C NMR) demonstrated that increased aromatic components due to mycorrhizal inoculation resulted in enhanced phenanthrene uptake by the roots but lower translocation to the shoots. Direct visualization using two-photon excitation microscopy (TPEM) revealed higher phenanthrene accumulation in epidermal cells of roots and lower transport into the root interior and stem in mycorrhizal plants than in non-mycorrhizal controls. These results provide some insight into the mechanisms by which arbuscular mycorrhizal inoculation may influence the uptake of organic contaminants by plants.     

Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp. isolated from cadmium polluted soil under increasing cadmium levels

The effect of inoculation with indigenous naturally occurring microorganisms (an arbuscular mycorrhizal (AM) fungus and rhizosphere bacteria) isolated from a Cd polluted soil was assayed on Trifolium repens growing in soil contaminated with a range of Cd. One of the bacterial isolate showed a marked PGPR effect and was identified as a Brevibacillus sp. Mycorrhizal colonization also enhanced Trifolium growth and N, P, Zn and Ni content and the dually inoculated (AM fungus plus Brevibacillus sp.) plants achieved further growth and nutrition and less Cd concentration, particularly at the highest Cd level. Increasing Cd level in the soil decreased Zn and Pb shoot accumulation. Coinoculation of Brevibacillus sp. and AM fungus increased shoot biomass over single mycorrhizal plants by 18% (at 13.6 mg Cd kg(-1)), 26% (at 33.0 mg Cd kg(-1)) and 35% (at 85.1 mg Cd (kg(1)). In contrast, Cd transfer from soil to plants was substantially reduced and at the highest Cd level Brevibacillus sp. lowered this value by 37.5% in AM plants. Increasing Cd level highly reduced plant mycorrhization and nodulation. Strong positive effect of the bacterium on inocula, are important in plant Cd tolerance and development in Cd polluted soils.     

Cu污染土壤接种丛枝菌根真菌对旱稻生长的影响

采用盆栽实验的方法,研究了不同Cu处理水平(0、100和200 mg/kg)下,接种丛枝菌根真菌(arbuscular my-corrhizal fungi,AMF)Glomus mosseae对旱稻(Oryzal Sativa L.)生长的影响。结果表明,未添加Cu处理下,旱稻菌根侵染率可达69%,随着土壤中Cu添加量增加,旱稻菌根侵染率显著下降(P<0.05)。与未接种处理相比,接种处理显著提高100mg/kg Cu处理下根系生物量以及200 mg/kg Cu处理下地上部分生物量(P<0.05);接种处理显著降低了100 mg/kg Cu处理下旱稻地下部Cu含量,却显著增加了200 mg/kg Cu处理下旱稻地上部分以及地下部分Cu含量(P<0.05)。     

重金属污染土壤接种丛枝菌根真菌对蚕豆毒性的影响

采用盆栽实验的方法,研究了重金属(包括Cu、Zn、Pb和Cd)复合污染和接种丛枝菌根真菌(arbuscular mycorrhizal fungi,AMF)Glomus mosseae对蚕豆(Vicia faba)生长及DNA损伤的影响.结果表明,虽然接种菌根真菌对蚕豆生物量的影响并不显著,但是却显著影响植物对重金属的吸收,接种菌根真菌对蚕豆吸收4种重金属元素的作用有差异.采用单细胞凝胶电泳(single cell gel electrophoresis,SCGE)法研究接种菌根真菌对蚕豆叶片的DNA损伤的影响,与重金属吸收的结果相吻合.结果表明,接种处理可显著增加蚕豆叶片的DNA损伤程度,这与接种处理可提高植物的重金属吸收相一致.     

Inoculation with arbuscular mycorrhizal fungi and addition of composted olive-mill waste enhance plant establishment and soil properties in the regeneration of a heavy metal-polluted environment

A greenhouse experiment was carried out in order to investigate the effects of arbuscular mycorrhizal (AM) fungi inoculation and the use of composted olive waste (COW) in the establishment of Tetraclinis articulata and soil properties in a heavy metal-polluted soil. The treatments assayed were as follows: AM?+?0 % COW, AM?+?1 % COW, and AM?+?3 % COW. The higher doses of COW in combination with AM fungi increased shoot and root biomass production of T. articulata by 96 and 60 %, respectively. These treatments trended to improve the soil properties evaluated, highlighting the C compounds and N as well as the microbiological activities. In relation to the metal translocation in T. articulata, doses of COW applied decreased the Cr, Ni, and Pb contents in shoot, as well as Cr and As in root, although the most of them reached low levels and far from phytotoxic. The COW amendment aided Glomus mosseae-inoculated T. articulata plants to thrive in contaminated soil, mainly through an improvement in both nutrients uptake, mainly P and soil microbial function. In addition, the combined use of AM fungi plus COW could be a feasible strategy to be incorporated in phytoremediation programs because it promotes soil properties, a better performance of plants for supporting the stress in heavy metal-contaminated soils derived from the mining process, and also can be a good way for olive-mill waste disposal.     

Changes in elemental uptake and arbuscular mycorrhizal colonisation during the life cycle of Thlaspi praecox Wulfen

Elemental uptake and arbuscular mycorrhizal (AM) colonisation were studied during the life cycle of field collected Cd/Zn hyperaccumulating Thlaspi praecox (Brassicaceae). Plant biomass and tissue concentrations of Cd, Pb, Zn, Fe and Ni were found to vary during development, while no variation in P, K, Ca, Mn and Cu tissue concentrations were observed. The lowest Cd bioaccumulation in rosette leaves (BAF(RL)) observed during seeding was partially attributed to lower translocation from roots to rosette leaves and partially to high translocation to stalks, indicating a high Cd mobility to reproductive tissues, in line with our previous studies. The highest intensity of AM colonisation (M%) was observed in the flowering phase and was accompanied by increased root Cd, Zn, Pb and Fe contents. In addition, a positive correlation between AM colonisation and Fe contents in rosette leaves was found. The results indicate developmental dependence of AM formation, accompanied by selective changes in nutrient acquisition in T. praecox that are related to increased plant needs, and the protective role of AM colonisation on metal polluted sites during the reproductive period.     

Microbial processes in the rhizosphere soil of a heavy metals-contaminated Mediterranean salt marsh: a facilitating role of AM fungi

We investigated the relationship of the zonal pattern followed by the vegetation in a polluted Mediterranean salt marsh, in semiarid south-eastern Spain, with the microbiological and biochemical properties (labile C fractions, oxidoreductases and hydrolases) of the rhizosphere soil of two halophyte species, Arthrocnemum macrostachyum and Sarcocornia fruticosa, and with the degree of arbuscular mycorrhizal (AM) colonisation in their rhizospheres. Levels of plant biomass and cover were inversely related to heavy metal contents and salinity. The concentrations of Fe, Cu, Mn and Pb extracted with DTPA hardly varied among the different zones of the salt marsh. The dehydrogenase and phosphatase activities, the soluble C and water-soluble carbohydrates concentrations and the extent of root colonisation were greater in the salt marsh zones of lower soil salinity and lower metal concentration. Urease and beta-glucosidase activities were not detected in the salt marsh. Plant biomass and cover showed positive relationships with mycorrhizal colonisation (R=0.773, P<0.001; R=0.874, P<0.001, respectively). Mycorrhizal colonisation was negatively correlated with the contents of Pb and Zn in plant tissues. This work supports the view that reduced plant uptake of toxic metals, particularly lead, could be involved in the beneficial effects of AM fungi on plant development in Mediterranean salt marshes contaminated with mining wastes.     

Effect of arbuscular mycorrhizal fungus (Glomus caledonium) on the accumulation and metabolism of atrazine in maize (Zea mays L.) and atrazine dissipation in soil

Effects of an arbuscular mycorrhizal (AM) fungus (Glomus caledonium) on accumulation and metabolism of atrazine in maize grown in soil contaminated with different concentrations of atrazine were investigated in a series of pot experiments. Roots of mycorrhizal plants accumulated more atrazine than non-mycorrhizal roots. In contrast, atrazine accumulation in shoot decreased in mycorrhizal compared with non-mycorrhizal plants. No atrazine derivatives were detected in the soil, either with or without mycorrhizal colonization. However, atrazine metabolites, deethylatrazine (DEA) and deisopropylatrazine (DIA), were detected in plant roots and the AM colonization enhanced the metabolism. After plant harvest atrazine concentrations decreased markedly in the soils compared to the initial concentrations. The decreases were the most in rhizosphere soil and then near-rhizosphere soil and the least in bulk soil. Mycorrhizal treatment enhanced atrazine dissipation in the near-rhizosphere and bulk soils irrespective of atrazine application rates.     

Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment

A sand culture experiment was conducted to investigate whether mycorrhizal colonization and mycorrhizal fungal vesicular numbers were influenced by metal lead, and whether mycorrhizae enhance host plants tolerance to metal lead. Metal lead was applied as Pb(NO3)2 in solution at three levels (0, 300 and 600 mg kg(-1) sand). Five mycorrhizal host plant species, Kummerowia striata (Thunb.) Schindl, Ixeris denticulate L., Lolium perenne L., Trifolium repens L. and Echinochloa crusgalli var. mitis were used to examine Pb-mycorrhizal interactions. The arbuscular mycorrhizal inoculum consisted of mixed spores of mycorrhizal fungal species directly isolated from orchard soil. Compared to the untreated control, both Pb concentrations reduced mycorrhizal colonization by 3.8-70.4%. Numbers of AM fungal vesicles increased by 13.2-51.5% in 300 mg Pb kg(-1) sand but decreased by 9.4-50.9% in 600 mg Pb kg(-1) sand. Mycorrhizae significantly enhanced Pb accumulation both in shoot by 10.2-85.5% and in root by 9.3-118.4%. Mycorrhizae also enhanced shoot biomass and shoot P concentration under both Pb concentrations. Root/shoot ratios of Pb concentration were higher in highly mycorrhizal plant species (K.striata, I. denticulate, and E. crusgalli var. mitis) than that in poorly mycorrhizal ones (L. perenne and T. repens,). Mycorrhizal inoculation increased the root/shoot ratio of Pb concentration of highly mycorrhizal plant species by 7.6-57.2% but did not affect the poorly mycorrhizal ones. In the treatments with 300 Pb mg kg(-1) sand, plant species with higher vesicular numbers tended to show higher root/shoot ratios of the Pb concentration. We suggest that under an elevated Pb condition, mycorrhizae could promote plant growth by increasing P uptake and mitigate Pb toxicity by sequestrating more Pb in roots.     

Root fungal colonisation in Deschampsia flexuosa: effects of pollution and neighbouring trees

In industrial barrens adjacent to a nickel-copper smelter at Monchegorsk, the Kola Peninsula, root colonisation in Deschampsia flexuosa by arbuscular mycorrhizal (AM)-type of hyphae was lower than in unpolluted forests (60.9 vs. 80.4%), while Olpidium-colonisation showed a marginally significant decline, and dark septate endophytic (DSE) hyphal colonisation was not affected. We detected an interactive effect of pollution and a neighbouring tree on DSE hyphal colonisation: at the highly polluted sites, colonisation was lower in D. flexuosa growing near trees, whereas at sites with low pollution the presence of the neighbouring tree had no effect on colonisation. High numbers of intracellular DSE sclerotia in the industrial barrens (13.3 vs. 3.4%) may indicate a survial strategy in an unfavourable environment and a dispersal strategy into a more favourable environment. While lower root colonisation by AM fungi has been also earlier reported in graminoids for heavy metal contamination, the results on other ubiquitous fungi colonising D. flexuosa roots are more novel.     

Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil

The contribution of arbuscular mycorrhiza (AM) to immobilisation of Cd in substrate was studied in two experiments. In the first experiment, substrates prepared by cultivating tobacco, either non-mycorrhizal or inoculated with the AM fungus Glomus intraradices were enriched with a range of Cd concentrations, and Cd toxicity in the substrates was assessed using root growth tests with lettuce as a test plant. The tests revealed lower Cd toxicity in the mycorrhizal than in the non-mycorrhizal substrate, and the difference increased with increasing total Cd concentration in the substrates. In the second experiment, extraradical mycelium (ERM) of G. intraradices exposed in vivo to Cd was collected and analysed on Cd concentration. The ERM accumulated 10–20 times more Cd per unit of biomass than tobacco roots. While Cd concentrations were lower in the biomass of mycorrhizal plants than of non-mycorrhizal plants, Cd immobilisation by ERM did not affect the total Cd content in mycorrhizal tobacco.

It is concluded that mycorrhiza may decrease Cd toxicity to plants by enhancing Cd immobilisation in soil. The results therefore suggest a potential role of AM symbiosis in the phytostabilisation of contaminated soils, where high Cd availability inhibits plant growth.     

A Cr(VI)-reducing Microbacterium sp. strain SUCR140 enhances growth and yield of Zea mays in Cr(VI) amended soil through reduced chromium toxicity and improves colonization of arbuscular mycorrhizal fungi

Pot culture experiments were conducted in a glasshouse to evaluate the effects of four efficient Cr(VI)-reducing bacterial strains (SUCR44, SUCR140, SUCR186, and SUCR188) isolated from rhizospheric soil, and four arbuscular mycorrhizal fungi (AMF—Glomus mosseae, G. aggregatum, G. fasciculatum, and G. intraradices) alone or in combination, on Zea mays in artificially Cr(VI)-amended soil. Presence of a strain of Microbacterium sp. SUCR140 reduced the chromate toxicity resulting in improved growth and yields of plants compared to control. The bioavailability of Cr(VI) in soil and its uptake by the plant reduced significantly in SUCR140-treated plants; the effects of AMF, however, either alone or in presence of SUCR140 were not significant. On the other hand, presence of AMF significantly restricted the transport of chromium from root to the aerial parts of plants. The populations of AMF chlamydospores in soil and its root colonization improved in presence of SUCR140. This study demonstrates the usefulness of an efficient Cr(VI)-reducing bacterial strain SUCR140 in improving yields probably through reducing toxicity to plants by lowering bioavailability and uptake of Cr(VI) and improving nutrient availability through increased mycorrhizal colonization which also restricted the transport of chromium to the aerial parts.