It has been reported that toxic metals often interfere with the root uptake of nutrients, such as Fe, P, Mg, K, Ca, and Zn, and with the metabolic functions of the essential nutrients, leading to plant growth retardation Ouzounidou et al.
In addition, soils augmented with toxic metals are often highly deficient in nutrients, which impose additional restraints to plant growth. Under such conditions, the fungal endophytes improve the acquisition of plant nutrients by mobilizing nutrients and making them available to the plant roots Cui and Nobel, ; Weyens et al. The Glomeromycota are obligatory biotrophs and lack saprotrophic capabilities.
Thus, their ability to decompose organic matter and to liberate compounds that are absorbable for the plant into the soil is limited. In contrast, endophytic fungi are saprotrophic microorganisms that can improve plant nutrition by decomposing organic matter Promputtha et al. This trait can be particularly useful in environments polluted with TMs that are devoid of available nutrients. AMF develop specialized structures — arbuscules — that allow an exchange between the fungus and the plant.
Abuscules are branched intracellular hyphae that are present in the root cortex. The absence of these structures in fungal endophytes suggests that the mechanism of nutrient transfer at the plant-endophyte interface differs from that employed by the AMF. Interestingly, the Mucoromycotina of the bryophytes formed characteristic intracellular coils of an unknown function Field et al.
We can only hypothesize that these structures may play a similar role in Mucoromycotina to that of the arbuscules in the AMF. Another possible way to improve plant nutrition by fungal endophytes is the rhizophagy cycle hypothesized to act in the interaction between plants and endophytic bacteria and yeast Paungfoo-Lonhienne et al.
The rhizophagy theory suggests that fungi and endophytic bacteria can be the prey of the plant root cells and serve as nourishing factors that enable the plants to survive even without available nutrients in the surroundings.
Endophytic fungi are associated with a wide range of plant growth promoting activities, including P solubilization and the production of siderophores and phytohormones Chhabra and Dowling, The role of fungal endophytes in the delivery of P to the plant was described in numerous studies.
Hiruma et al. Yadav et al. In addition, plants inoculated with S. This indicates that PiPT is involved in phosphorus transport and that S. Improved host phosphorus acquisition by S. The class 2 endophytic Fusarium tricinctum strain isolated from S. Inoculation tests revealed that these fungal endophytes enhance plant growth by promoting the uptake of K.
The role of microorganisms in the phenomenon of hyper-accumulation remains unknown, even though much progress in this matter has recently been accomplished reviewed in Furini et al. Turnau and Mesjasz-Przybylowicz reported several Ni hyper-accumulating plants from ultramafic soils in South Africa that were abundantly colonized by AMF.
The inoculated plants translocated Ni to the above-ground parts of the plant more efficiently. The effect of the endophytic fungi on these plants that are strongly dependent on mycorrhizae still awaits investigation, which could be useful for phytoextraction. In recent years, there has been an increase in studies on the influence of endophytic fungi on hyper-accumulating plant species. Khan et al. They isolated 42 culturable fungal strains that belonged to the Ascomycota. In another study, Khan et al.
They showed that one of the strains isolated RSF-6L exhibited the ability to reduce Cd uptake in the plant. Both the translocation factor TF and the bio-concentration factor were lower in the plants inoculated with endophytes than the control Khan et al. Interestingly, earlier studies showed that inoculation with the mycorrhizal fungi Claroideoglomus claroideum and R.
It would be interesting to compare these results with those of double inoculation and various metals. In addition, inoculation with the fungi conferred protection to the host plant, leading to an improvement in tolerance. The pollution of soils with toxic metals not only affects the composition and diversity of microbial communities, leading to a reduction in the overall abundance of microbial species, but also results in the enrichment of metal-tolerant microbial strains Yao et al.
These strains are extremely tolerant to metal toxicity and based on the studies available may facilitate plant growth in environments polluted with metals. The role of mycorrhizae in the adaptation of plants to metal pollution has been extensively studied over the last three decades. However, the role of other microbial components of the mycorrhizosphere cannot be overlooked. This is particularly important due to the fact that plants in their natural environments simultaneously interact with a wide array of microorganisms.
In case of the Brassicaceae metallophytes and hyper-accumulators that lost the ability to interact with mycorrhizae fungal endophytes may play a role resembling mycorrhizae in the adaptation of non-mycorrhizal plants to metalliferous soils; however, the mechanisms of the action of endophytes may distinguish them from other symbiotic fungi Table 1.
In nature plants, both mycorrhizal and non-mycorrhizal and microorganisms form complex assemblages termed the holobiont. The functioning of this super organism is determined by relationships between the interacting organisms, thus understanding the complexity and routs of mutual communication will allow us to utilize the potential of plant-based clean-up technologies more effectively.
In general, the influence of toxic metals on fungi and plants encompasses induced changes on the level of the epigenome, transcriptome, proteome, metabolome, and secretome. In addition, these changes further influence the interactions between the plant and symbiotic fungi and other soil microorganisms Figure 1. Endophytic fungi may alleviate TM stress in the host plants in various manners. They can serve as a barrier and prevent the entry of metal ions into plant tissues and optimize metal distribution within the plant.
These roles of fungi have been described on several occasions; however, very little is known about how the symbiont induces the metal phenotype in plants.
One of the most pending questions is whether the metal adapted fungus directly affects metal specific tolerance mechanisms or is improved adaptation to metal toxicity a result of indirect action such as improving water and nutrient availability in the soil and their subsequent uptake by plants that confer plant fitness? Another question is how much the endophyte influence on the plant TM tolerance differs from the analogous impact of mycorrhizal fungi?
To answer these questions more studies concerning the role of fungal symbionts in plant response to TM are needed. Bioremediation is a dynamically growing area of green biotechnology. Endophytes may have considerable potential applications not only in microbial-assisted phytoremediation practice but also in mycoremediation of the areas that cannot be used for plant growth.
AD and KT prepared the figures. AD and PR contributed equally to the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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This article has been cited by other articles in PMC. Abstract The contamination of soil with toxic metals is a worldwide problem, resulting in the disruption of plant vegetation and subsequent crop production. Keywords: fungal endophytes, toxic metals, mycorrhiza, phytoremediation, phytomining.
Introduction The deposition of toxic metals TMs in the topsoils of a significant acreage of land has become a major problem over a wide range of countries from both highly developed and developing regions of the world. Open in a separate window.
Figure 1. Endophytic Fungi: Lifestyle and Taxonomy Endophytic fungi exhibit a high degree of lifestyle versatility, and depending on the genetic traits of the partners, developmental stage, nutritional status, and other environmental factors, they can interact with their host in mutualistic, commensalic, or as latent pathogenic as summarized by Schulz et al.
Toxic Metal Tolerance of Endophytic Fungi Certain strains of endophytic fungi exhibit extraordinarily high resistance to toxic metals.
Plant Metal Tolerance Induced by the Fungi Plants inhabiting sites rich in toxic metals TMs developed a variety of mechanisms that allow them to survive in extremely adverse environments. Figure 2. Table 1 Comparison of plant toxic metal tolerance mechanisms activated by symbiotic fungi. The Influence of Endophytic Fungi on TM Detoxification by the Plant Endophytic fungi were also shown to affect the expression of the stress-related genes of the host plant, thus triggering resistance against TM toxicity.
Hyper-Accumulators and Symbiotic Fungi The role of microorganisms in the phenomenon of hyper-accumulation remains unknown, even though much progress in this matter has recently been accomplished reviewed in Furini et al. Conclusions The pollution of soils with toxic metals not only affects the composition and diversity of microbial communities, leading to a reduction in the overall abundance of microbial species, but also results in the enrichment of metal-tolerant microbial strains Yao et al.
Conflict of Interest Statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Footnotes Funding. References Adriaensen K. A zinc-adapted fungus protects pines from zinc stress.
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Microbes as potential tool for remediation of heavy metals: a review. The results indicate that interaction between endophyte and ECM fungus is species dependent, leading to increased or decreased nutrient content and growth of pine seedlings. Being considered as separate habitats, the phyllosphere, rhizosphere and endosphere, as well as the microbes colonizing them, are often studied separately e. However, in nature plants associate with diverse microorganisms simultaneously and different niches overlap.
Even if a microbe living in one part of the plant is not colonizing the other parts, interactions between microbes in different niches do exist Novas et al. The phyllosphere covers the surface of aerial parts of the plant and the rhizosphere the roots and the narrow area of the soil surrounding them. These habitats are colonized by several different epiphytic Yang et al. Mycorrhizae are one of the most well-known forms of symbiosis found in the plant rhizosphere.
A majority of conifers in boreal and temperate forests live with fungal symbionts forming an ectomycorrhizal ECM symbiosis Smith and Read The extraradical mycelium extending from the root covering the mantle to the surrounding soil can remarkably increase the surface area of plant root system and consequently, the nutrient uptake Landeweert et al. Symbiosis also improves the growth and resistance of the conifer against biotic and abiotic stresses Finlay et al.
Polyamines are known to be involved in several plant metabolic processes ranging from embryogenesis and development to defence reactions Bais and Ravishankar , Vuosku et al.
Besides mycorrhizae, plant health and growth are improved by plant growth-promoting bacteria PGPB Bashan and de-Bashan The most well-known group of PGPB is plant growth-promoting rhizobacteria PGPR , which can exist as free-living soil bacteria on the root surface, or as endophytes, inside the root tissues reviews by Gray and Smith , Compant et al. Plant growth-promoting rhizobacteria can improve plant growth directly by producing beneficial metabolites or by affecting the availability of soil nutrients, and indirectly by inhibiting the growth of pathogenic fungi or acting as mycorrhizal helper bacteria MHB Garbaye , Cardoso et al.
Only a few rhizosphere-derived microorganisms are able to colonize the aerial parts due to the host plants' structural barriers, such as root endosphere, and specific conditions including UV radiation, temperature and humidity fluctuations Compant et al. Endophytic microorganisms colonize the internal plant tissues without causing any symptoms of disease Bacon and Hinton These microorganisms can have a positive effect on the growth and development of the plant Basile et al.
Methylobacterium can enter the plant through the root and systematically colonize every tissue Podolich et al. Pohjanen, E. Ihantola, S. Different Methylobacterium strains have been shown to improve plant growth and arbuscular mycorrhization by producing plant hormones e.
In contrast to the hormone-producing Methylobacterium strains Ivanova et al. Despite the long history of symbiosis studies, many details of symbiotic interactions are still unclear and there is limited information on plants interacting simultaneously with several types of symbionts.
The aim of the current study was to find out how interaction with M. Specifically, we studied the growth, PA and nutrient content of Scots pine seedlings inoculated with endophytic bacterium, ECM fungi or both.
For inoculations, we applied either i endophytic bacterium M. Both fungi were maintained by cultivating mycelia on Hagem agar medium Modess To prepare the inoculants for the experiment, both fungi were cultivated for 4 weeks at room temperature RT in the dark on sterile filter paper strips on Hagem agar medium. Endophytic M. To prepare the inoculants for the experiment, M.
For inoculation, the bacterial culture was diluted with sterile water to a density of 2. After sterilization, seeds were rinsed with sterile water and germinated on sterile vermiculite in glass jars. To improve the visualization of M. The resulting transformants were selected on ammonium mineral salt medium containing 0. A clone exhibiting normal cell and colony morphology, growth rate and stable GFP fluorescence after consecutive batch cultures was selected, resulting in strain M.
Seeds were inoculated with the M. For the in situ hybridization and growth, PA and nutrient analysis, day-old seedlings were placed on sterile moist filter paper on modified Melin Norkrans MMN agar medium Marx as described by Niemi et al.
The fungal and control inoculations were performed as described by Niemi et al. For controls, as well as for M. Samples were collected at 3, 7, 14 and 60 days after inoculation DAI. The experimental set-up.
At the beginning of the experiment, Scots pine seedlings were placed on sterile moist filter paper that was overlaid on MMN agar medium and two sterile filter paper strips were placed on the root of the seedlings. Photo was taken at the end of the experiment 60 DAI. Background autofluorescence was detected using Long-pass filter. The shoot weight, root weight and root length were measured, and the number of lateral roots and root tips covered with fungal mantle was determined from all seedlings.
The degree of root mycorrhization was calculated by dividing the amount of root tips covered with fungal mantle with the number of all lateral roots.
The roots and shoots of five seedlings were pooled together to represent one sample. Altogether three replicates per sampling date and per treatment were taken. All statistical analyses were done with SPSS version To confirm the success of inoculation, M.
The Methylobacterium -specific probe MB hybridized to parenchymatous cells in stems and also to needle mesophyll of the inoculated seedlings Figure 2. GFP-tagged cells of M. Detection of M. In situ hybridization of a needle from MB seedling hybridized without probe as a negative control 60 DAI. The natural brown cells of the pine tissue, which contain tannins and other phenolic compounds, are marked with a T. Confocal laser scanning microscopy image f showing the cells of M. Treatments marked with the same letter did not significantly differ from each other.
At 60 DAI, the root and shoot DWs were significantly higher in all inoculation treatments when compared with the control seedlings Figure 4. No significant differences were observed in the mean root length or mean number of lateral roots during the first 14 days, or in the degree of mycorrhization see Table S2 available as Supplementary Data at Tree Physiology Online between the treatments, which might be due to the high variation within treatments.
Carbon and nitrogen contents were calculated as the percentage of DW and as the total content of roots and shoots. We also determined the carbon and nitrogen ratio between roots and shoots see Tables S3 and S4 available as Supplementary Data at Tree Physiology Online. Root nitrogen percentage was at the same level with control seedlings in all treatments and there were no differences between the total root nitrogen contents of different treatments. Differences were detected only at 60 DAI, and mainly for potassium and calcium.
There were no differences in the total magnesium content of root or shoot systems between different treatments. The inoculations had no effect on the shoot total phosphorus content. The ratios between the root and shoot total potassium, calcium, magnesium and phosphorus contents at 60 DAI were also determined. Differences between treatments were mainly found for calcium and phosphorus.
Concentrations of free and conjugated putrescine, spermidine and spermine of differently inoculated seedlings were compared. At 3 DAI, the only differences were found in contents of free and conjugated spermidine in the roots Figures 6 and 7. The quantities of free and conjugated spermine in root samples were below the detection limit.
FW, fresh weight. The endophyte M. In the present study, the effect of M. Our results show that i M. Methylobacterium extorquens significantly increased growth of the pine seedlings, measured as increased root and shoot dry weight. The most studied PGPRs of conifers affect plant growth through various mechanisms: hormone or siderophore production, increased phosphate solubilization, by acting as MHB, or by inducing systemic resistance reviewed by Cardoso et al.
The resulting effects on the host plant are observed as increased root and shoot length, dry weight and improved seed germination reviewed by Cardoso et al. Also, some bacterial strains living in plant rhizosphere Nassar et al. The most common phytohormones are not produced by the endophyte M. Niemi et al. The results of the present study indicated that there is a fungus-dependent pattern in the quantities of free and conjugated spermidine of roots during the early phases of symbiosis, but no changes induced by M.
In the previous studies with ECM fungi the changes in root PA contents were simultaneous with growth improvement Niemi et al. This might be due to large variation in the PA content of individual samples, the slow growth of the fungus during the first days of the experiment or the subsequent variation in the number of infected roots or active mycelium. Some methylotrophic bacteria can affect plant growth by altering host nitrogen metabolism by the bacterial urease enzyme or by production of vitamin B 12 Basile et al.
Furthermore, methylotrophic bacteria consume methanol, a toxic waste produced by the host plant during cell wall biosynthesis, as a carbon source Holland and Polacco , However, in the present work, inoculation with M. The growth effect induced by co-inoculation of the endophyte M. The variation in root length and mycorrhization was very high between the treatments and therefore no significant differences were found.
However, when the endophyte was inoculated with PT , several seedlings had clearly increased root length and higher number of mycorrhizal roots. High variation in the mycorrhization may also explain the variability in PA concentrations. Strain-specific changes in growth promotion by inoculants have been detected in previous studies.
For example, inoculation of Methylobacterium oryzae CBMB20 alone or together with rhizobacteria, the nitrogen-fixing Azospirillum brasilense or the phosphate-solubilizing Burkholderia pyrrocinia , increased shoot or root length and nutrient uptake in tomato Lycopersicon esculentum Mill.
Madhaiyan et al. A greenhouse experiment comparing two different strains of M. When inoculated together with arbuscular mycorrhizal AM fungi, increase in several plant growth parameters and chlorophyll content was observed, but the growth improvement was dependent on the M. Methylobacterium oryzae CBMBinduced improvement in growth and nutrient uptake was suggested to associate with IAA and cytokinins produced by this strain Madhaiyan et al.
Similarly, in another study on pine root mycorrhization together with various PGPR, the effect was dependent on the bacterial strain Barriuso et al. Overall, plant symbiosis with ECM fungi improves the uptake of nitrogen, phosphorus and magnesium reviewed by Chalot et al. Kim et al. Ectomycorrhizal infection also caused a shift in nitrogen allocation into the root system.
The macronutrient content was dependent on the combination of microorganisms inoculated. A similar phenomenon was seen in total root phosphorus content. Weathering of the minerals by ECM fungi has been reported to result in improvement of growth and potassium nutrition of trees Wallander and Wickman , Yuan et al.
In the present study, inoculation with M. However, potassium was added to the culture medium in soluble form KH 2 PO 4 , which means that the enhanced potassium uptake by the seedling was not due to weathering of a nutrient source, but rather by some yet unknown mechanism.
At present, the detailed mechanisms behind plant symbiosis are not well known. Therefore, it is obvious that the mechanisms of multiple simultaneous interactions between microbes and plant are more complicated and even less understood. In the present study, we investigated the effect of interactions with endophytic M. Despite the relatively short duration of the experiment and restricted number of simultaneously tested symbiotic organisms, we found significant differences in nutrient contents and growth of pine seedlings that were dependent on the symbiont, or the combination of specific symbionts, indicating a possible role in seed establishment and early development of Scots pine seedlings.
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