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TECHNICAL REPORTS

Ecosystem Restoration

Role of Mycorrhizal Fungi and Phosphorus in the Arsenic Tolerance of Basin Wildrye

^a Department of Ecosystem and Conservation Sciences, College of Forestry and Conservation, The University of Montana, Missoula, MT 59812
^b Bitterroot Restoration, Inc., 445 Quast Lane, Corvallis, MT 59828

^* Corresponding author (thd{at}forestry.umt.edu).

Received for publication August 23, 2002.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Revegetation of arsenic (As)-rich mine spoils is often impeded by the lack of plant species tolerant of high As concentrations and low nutrient availability. Basin wildrye [Leymus cinereus (Scribner & Merr.) A. Löve] has been observed to establish naturally in soils with elevated As content and thus may be useful for the stabilization of As-contaminated soils. An experiment was conducted to evaluate how variable phosphorus (P) concentrations and inoculation with site-specific arbuscular mycorrhizal fungi influence As tolerance of basin wildrye. Basin wildrye was grown in sterile sand in the greenhouse for 16 weeks. Pots of sterile sand were amended to create one of four rates of As (0, 3, 15, or 50 mg As kg^-1), two rates of P (3 or 15 mg P kg^-1), and ±mycorrhizal inoculation in a 2 x 4 x 2 factorial arrangement. After 16 weeks of growth, plants were harvested, shoots and roots thoroughly washed, and the tissue analyzed for total shoot biomass, total root and shoot As and P concentrations, and degree of mycorrhizal infection. Basin wildrye was found to be tolerant of high As concentrations allowing for vigorous plant growth at application levels of 3 or 15 mg As kg^-1. Arsenic was sequestered in the roots, with 30 to 50 times more As in the roots than shoots under low P conditions. Mycorrhizal infection did not confer As tolerance in basin wildrye nor did mycorrhizal fungi influence biomass production. Phosphorus concentrations of 15 mg kg^-1 effectively inhibited As accumulation in basin wildrye. Basin wildrye has the potential to be used for stabilization of As-rich soils while minimizing exposure to grazing animals following reclamation.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
ELEVATED CONCENTRATIONS OF ARSENIC (As) are characteristic of waste rock or tailings materials at many abandoned and active mine sites across the western United States. Elimination of As at these sites is impractical due to both a lack of remediation methods and the high cost for large-scale burial of wastes. Site stabilization through revegetation, however, presents a low-cost option for application to large areas. The use of plant materials tolerant of elevated As levels could provide site stabilization and prevent the off-site migration of contaminated materials via wind erosion.

Basin wildrye has been found to establish naturally in soils of elevated As content and limited nutrient availability (R.D. Taskey, unpublished M.S. thesis, 1972), and is a common invader of abandoned As-rich mine spoils in Montana, Idaho, and Nevada. A cool-season perennial bunchgrass native to western North America, it has adapted to a broad range of soils and is productive even under moisture limiting conditions (Stubbendieck et al., 1997). Basin wildrye is winter hardy and relatively tolerant of acid, alkaline, and saline soil conditions (Smoliak et al., 1990) and it demonstrates good establishment from seed producing large (1–3 m) plants with fibrous roots (Cash et al., 1998).

Although basin wildrye has been frequently observed growing in high As conditions, there has been little investigation of its mechanism for As tolerance. The As tolerance in species such as velvet grass (Holcus lanatus L.), tufted hairgrass [Deschampsia caespitosa (L.) Beauv.], and colonial bentgrass (Agrostis capillaris L.) is thought to be primarily an adaptation to the plants' phosphate uptake system (Meharg and Macnair, 1990, 1991; Meharg, 1994; Meharg and Hartley-Whitaker, 2002). In the case of arsenate-tolerant velvet grass, permanent suppression of the PO^3-₄ uptake system serves to suppress arsenate uptake, the main plant-available form of As under aerobic conditions. Arsenate is a PO^3-₄ analog and is known to be transported by the P uptake system in higher plants (Asher and Reay, 1979; Meharg and Macnair, 1990). Additionally, the P uptake system accumulates PO^3-₄ preferentially over AsO^-₃, such that AsO^-₃ uptake never exceeds PO^3-₄ uptake, regardless of the availability of either (Meharg et al., 1994). Recent investigations also point out the potential importance of phytochelatins in association with As-tolerant plants (Hartley-Whitaker et al., 2001, 2002).

Certain arbuscular mycorrhizal (AM) fungi have been shown to provide host plants with some tolerance of toxic conditions, including high metal concentrations (Sharples et al., 2000; Shetty et al., 1994, 1995; Jones and Hutchinson, 1986; Bradley et al., 1981, 1982). This is accomplished through various mechanisms ranging from selective binding to complete immobilization of toxins by the AM fungi (Leyval et al., 1997; Gildon and Tinker, 1981; Read and Stribley, 1975; Nieboer et al., 1976). A major function of these fungi is to increase the surface area of plant root systems, greatly facilitating uptake of soil water and nutrients, especially in harsh conditions. In particular, AM fungi can greatly enhance the uptake of PO^3-₄, as well as NH⁺₄, K⁺, and NO^-₃ (Marschner and Dell, 1994; Hayman, 1983). It has been observed that basin wildrye plants growing in As-rich soils are colonized by AM fungi, but the specific benefits of this relationship are poorly understood.

The role of soil P availability in the As tolerance of basin wildrye is also unknown. While As uptake can be fatal to plants by eventually disrupting ATP formation (Ullrich-Eberius et al., 1989), the presence of adequate available P in the soil has been shown to prevent cell death by competing with As for P binding sites in the roots. Reduced As uptake can then allow the plant time to detoxify (Meharg and Macnair, 1992; Hurd-Karrer, 1939; Woolson et al., 1973). In order for this defense mechanism to be successful, however, sufficient P availability is required in the soil.

The purpose of this work was to investigate the potential role of mycorrhizal infection and P concentration on As tolerance in basin wildrye. With an understanding of the tolerance mechanisms used in basin wildrye, it was our hope that remediation efforts using this plant could be improved. Experiments were designed as a factorial arrangement to allow for assessment of interactions between As, P, and mycorrhizal fungi, and were conducted under highly controlled conditions to minimize variation and interference.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
A controlled greenhouse study was performed where growing conditions for basin wildrye were manipulated for 16 weeks through the combined application of three variables (As, P, and mycorrhizal status) at different levels. The As availability was split into four application levels (0, 3, 15, or 50 mg As kg^-1 sand). The P availability was split into two application levels, low and high (3 and 15 mg kg^-1). Mycorrhizal status was defined as basin wildrye grown in the presence or absence of mycorrhizal inoculation. These three variables were combined into a 4 x 2 x 2 factorial arrangement to create 16 different treatments applied to basin wildrye grown in sterilized sand. Each treatment was replicated nine times.

Plant and Mycorrhizal Material
Seed of basin wildrye (cv. Trailhead) was obtained from the USDA Plant Materials Center at Bridger, Montana. This cultivar is considered to have better establishment, higher productivity, and greater persistence in arid conditions than other basin wildrye lines, including the other main available cultivar (Magnar). The Trailhead variety was released in 1991 and originates from indigenous plants of a nonmined subirrigated range site near Roundup, Montana (Cash et al., 1998; Majerus, 1992; USDA Natural Resource Conservation Service, 2002). The soils of the range site are silty and have been classified as Korchea series (fine-loamy, mixed, superactive, calcareous, frigid Mollic Ustifluvents). There is no indication of high As content at the collection site (USDA Natural Resource Conservation Service, 1996) and there are no documented historical mechanisms for heavy metal contamination at the collection site; however, there has been some coal mining activity in the surrounding areas (R. Krause, Natural Resource Conservation Service Technician, NRCS Field Office, Roundup, MT, personal communication, 2003). Mycorrhizal inoculum was collected from the rhizosphere and immediately adjacent soils of basin wildrye growing on an As-rich site in north-central Nevada. This soil was determined to be a sandy loam with a pH of 8.3 and total As concentration of 879 mg kg^-1, and was comprised of native soils overlain by a mine tailings. Available As (Gavlak et al., 1994) and P (Olsen et al., 1954) concentrations were 1.26 and 23 mg kg^-1. Specifically, the collected mycorrhizal inoculum consisted of soil and fine root fragments clipped from the root mass of the plants. The inoculum was refrigerated (3°C) until usage. A composite soil sample, three root, and three shoot samples were also taken at this site for laboratory analysis of As content as described below.

Plant Preparation and Treatment
Basin wildrye seeds were sown in 5.7-L plastic pots, each filled to 80% capacity with sterilized (160°C for 2 h) 20/30 grit silica sand. Mycorrhizal treatments were established via the application of 20 g of inoculum on top of the sand with initial seed sowing. Twenty grams of autoclaved inoculum (220°C for 1 h, repeated after 24 h) was applied to the nonmycorrhizal treatments with seed sowing to control for unavoidable nutrient inclusion with inoculum additions. The seeds were then covered with 2.5 cm of sand. Once seed germination was complete, application of the appropriate As and P solution was initiated. The As was applied at 0, 3, 15, or 50 mg As kg^-1 sand as KH₂AsO₄·2 H₂O. The P was applied at 3 or 15 mg P kg^-1 sand as KH₂PO₄. The As and P solution was combined with a P-free 25% Hoaglands solution, applied at a rate of 750 mL of solution per pot per week. Before each application, pots were flushed with 1.5 L of water to prevent accumulation of As and P over time. Four plants were grown in each pot to ensure adequate biomass for analyses, and pots were randomized on the greenhouse benches within nine different blocks to avoid light, heat, and moisture gradient effects. Plants were maintained at 24 and 18°C day and night temperatures, watered biweekly, and given supplemental lighting (400 µÅ) in early spring to create a 16-h daylength.

Plants were grown for 16 weeks after germination, then harvested and separated into roots and shoots. After being thoroughly washed with water in an effort to remove both sand and any As or P that might be present on the outside surface of the roots, the plants were dried at 60°C for 3 d after which shoot biomass was determined. Accurate determination of root biomass could not be obtained due to loss of root mass in the harvesting and washing process. Root subsamples were stained using the procedure of Phillips & Hayman (1970), and examined to confirm presence and absence of mycorrhizal fungi. Percent root colonization was determined using the methodology developed by McGonigle et al. (1990). The remaining dried root and shoot samples were ground and total concentrations of As were determined by inductively coupled plasma–mass spectrometry (ICP–MS) using USEPA Method 200.8 (USEPA, 1991). Total P concentrations were determined using automated colorimetry using the ascorbic acid method, USEPA Method 365.1 (USEPA, 1983). A subsample of plant shoots from the different treatments was analyzed for K concentrations by ICP–MS using USEPA Method 200.7 (USEPA, 1991). A bulk sample of sand from each treatment was also analyzed for As (USEPA 200.8) and P (USEPA 365.1) content to confirm that As and P concentrations had not accumulated in the pots over time. The pH of the treatment solutions at each application level was determined using electrometric USEPA Method 150.1 (USEPA, 1983). The root and shoot samples collected at the mycorrhizal inoculum source site were analyzed for As concentrations as above. Analyses of the soil samples from the inoculum source site included determination of pH using Method S-2.10 (Gavlak et al., 1994) and determination of total As (Risser and Baker, 1990). Available As was determined using Method S-5.10 (Gavlak et al., 1994), and available P using sodium bicarbonate (Olsen et al., 1954).

Statistical Analysis
Data for each dependent variable (root As concentrations, shoot As concentrations, root P concentrations, shoot P concentrations, shoot biomass) were analyzed using a univariate three-way analysis of variance. Four of the five dependent variables were transformed to obtain homogeneity of variance for valid treatment comparison. A square root transformation was used on shoot As concentrations, and log₁₀ transformations were used on root As concentrations and root and shoot P concentrations. Shoot biomass was normalized by dividing the total biomass in each pot by the number of plants in each pot. Light, defined as the differences in light gradients available to the plants from overhead lighting, was analyzed as a covariate. All data were analyzed using SPSS statistical software (SPSS, 1998).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Plant Response to Mycorrhizal Inoculation
Mycorrhizal inoculation did not appear to significantly benefit plant growth or nutrient uptake. Mean dry weights of plant shoots were not significantly different between mycorrhizal and nonmycorrhizal treatments, nor were there significant differences in root or shoot As or P concentrations as a result of mycorrhizal inoculation (Table 1). Analysis of plant roots confirmed that 95% of all inoculated plants showed some level of infection, while no mycorrhizal presence was detected in the noninoculated roots. The mean colonization level of all plants infected was 14%, ranging from a colonization level of 5% in the 3 mg kg^-1 As, 3 mg kg^-1 P treatment, to 29% in the 50 mg kg^-1 As, 15 mg kg^-1 P treatment (Fig. 1) . Colonization was demonstrated by the presence of vesicles, arbuscules, and/or hyphae in root tissue.

View larger version (22K): [in this window] [in a new window]   Fig. 1. Mean mycorrhizal colonization levels per treatment of those plants grown in the presence of mycorrhizal inoculum. It was observed that 95% of all plants inoculated for this experiment demonstrated some level of mycorrhizal infection, with no evidence of colonization observed in the nonmycorrhizal treatments. Error bars indicate one standard error. Means with letters in common are not significantly different (P > 0.05).

Plant Response to Phosphorus and Arsenic Applications
Effects on Tissue Phosphorus and Arsenic Concentrations
Phosphorus uptake in basin wildrye plants significantly increased with P availability (Table 1), with up to four times the P accumulation in the high compared with the low P treatments (Table 2). Shoot P concentrations were higher than those found in the roots with minimal As application; a shift in root to shoot P ratios occurred with increased As availability and the subsequent interactions of As and P. Mean shoot biomass of the plants generally failed to increase with higher P availability, in contrast to that seen in grasses such as big bluestem (Andropogon gerardii Vitman) (Hetrick et al., 1986), perennial ryegrass (Lolium perenne L.) (Baligar et al., 1997), and wheat (Triticum aestivum L.) (Goh et al., 1997).

Shoot P concentrations were primarily dependent on P availability. Plants grown in the presence of higher P consistently demonstrated much higher P concentrations in the shoots than those grown at low P concentrations, regardless of As availability. Root concentrations of P were less affected by increased P availability, demonstrating significantly higher root P uptake only in the absence of substantial As availability (0 and 3 mg kg^-1 treatments).

The effect of As availability on plant P content was dependent on the amount of P available to the plants. Under conditions of high P availability (15 mg kg^-1), shoot P concentrations decreased dramatically with increased As application (Table 2). Plants grown in the absence of applied As demonstrated mean shoot concentrations of more than 2000 mg kg^-1 P, versus 1000 mg kg^-1 P at the highest As application rate.

Under conditions of low P availability (3 mg kg^-1), shoot P concentrations were only affected at the highest As application level. Root P concentrations, on the other hand, increased significantly with each increase of As application except for the high As application level. From these results it is clear that shoot P concentrations are not a direct product of concentrations observed in the roots.

The As accumulation in the roots was either balanced or exceeded by P accumulation, regardless of P or As application level (Table 2). The response of plants exposed to 1:1 concentrations of P and As was of particular interest. Plants grown at 15 mg kg^-1 P and 15 mg kg^-1 As accumulated three times more P in their roots than As. Plants grown at the lower P application level demonstrated essentially equal concentrations of P and As in their roots, even when exposed to 5 and 15 times more As than P.

Shoot P concentrations exceeded As concentrations, regardless of P or As availability. Concentrations of P to As in the shoots never dropped below 9:1 in the low P treatments, or 18:1 in the high P treatments. These results are similar to findings with velvet grass, where shoot P to As ratios never dropped below 2:1, regardless of P and As availability (Meharg et al., 1994).

Effects on Plant Biomass Production
Basin wildrye appeared to require higher P availability to sustain normal growth when exposed to high As concentrations. While plants exposed to 3 and 15 mg kg^-1 As appeared healthy and showed no significant difference in shoot biomass between high and low P treatments, there was a significant reduction in the biomass of plants exposed to 50 mg kg^-1 As in the low P treatments (Tables 1 and 2). At this As application level, plant growth was not inhibited in the presence of ample P (15 mg kg^-1 P). The difference in mean biomass between the low (1.00 g) and high (4.14 g) P treatments at this high As level demonstrates the role of P in preventing As toxicity (and growth inhibition).

Over time, it is possible that adequate P availability is necessary to sustain healthy basin wildrye plants even at lower (15 mg kg^-1) As concentrations. The stress of increased P uptake (in a P-limited environment) to counteract As concentrations may eventually compromise plant health. At both the 15 and 50 mg kg^-1 As application levels, plant P uptake in the low P treatments was dramatically higher than that seen at the other two As application levels, with P uptake paralleling that of the high P treatments. Sustaining this level of P accumulation at 20% of the P availability would probably come at the cost of reduced biomass production in the low P plants.

The greatest plant biomass production was observed in the high P, high As treatment (Table 2). This may be related to the increasing amount of P taken up by the plants to counteract the high As availability. It was suspected that the application of K associated with both the As (KH₂AsO₄) and P (KH₂PO₄) influenced plant productivity, therefore plant shoots were analyzed to determine K concentrations. There were, however, no significant differences in plant K concentrations regardless of P or As application levels. It is thus unlikely that the K application made a significant contribution to biomass production.

Analysis of the composite sand samples from each treatment confirmed that no buildup of applied salts had occurred. The pH of the eight different solution combinations varied slightly, ranging from 4.41 (50 mg kg^-1 As, 15 mg kg^-1 P) to 5.04 (0 mg kg^-1 As, 3 mg kg^-1 P), although this did not appear to contribute significantly to the results. It is important to note, however, that soil pH may be an influential factor in field trials, as AsO^-₃ sorption to soil particles can change with pH (Wells and Richardson, 1985; Heeraman et al., 2001; Goldberg and Glaubig, 1988; Jones et al., 1997). This is an important consideration in soils with multiple contaminants where methods such as liming may be employed to reduce the availability of other toxins.

Plants grown in the greenhouse demonstrated As concentrations comparable with those found in the sampled roots and shoots of wild plants growing at the mycorrhizal inoculum collection site. The mean available As concentration of wild roots and shoots on-site was 24.67 and 6.53 mg kg^-1, respectively. As shown in Table 2, small amounts of As were observed in both the roots and shoots of the 0 mg kg^-1 As treatments as a result of the unavoidable one-time application of 1.26 mg kg^-1 As (mixed in with the mycorrhizal inoculum) at the beginning of the experiment. Statistical analysis showed that light may have contributed significantly to root As and P concentrations, while not significantly affecting any of the other dependent variables such as shoot biomass. The implications of these results are unclear, and may be a case where statistical significance does not imply practical significance.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
The robust growth of basin wildrye under experimental conditions of limited P and high As availability demonstrates the hardiness of this grass and its potential utility as a revegetation tool in site remediation. The As accumulation in basin wildrye is regulated at the root level, and appears to represent the primary mechanism of As tolerance in the plant. This is supported by the much greater As concentrations in the roots than shoots, as well as by the dynamic interactions of P and As observed in the roots, but not in the shoots. In the treatments receiving 15 mg kg^-1 As or lower, it appeared that no additional P fertilization might be required (assuming a minimum concentration of 3 mg kg^-1 available P on-site). At high available As concentrations (50 mg kg^-1), however, it appeared that P availability of at least 15 mg kg^-1 would be required to prevent As toxicity. Mycorrhizal inoculation did not influence the degree of As tolerance in basin wildrye, but further studies should be performed in the field under conditions of limited water and nutrient availability to determine aggregate benefits of mycorrhizal infection. It should be noted that while the ‘Trailhead’ cultivar of basin wildrye used here demonstrated As tolerance, the tolerance of other varieties of basin wildrye is not yet known. Additionally, further investigation would be required to determine if genetic variability within the Trailhead cultivar plays a role in As tolerance. It has been shown for the plant velvet grass that within a given population, both tolerant and nontolerant plants can exist (Meharg et al., 1993).

	ACKNOWLEDGMENTS

 
This research was conducted with support from Getchell Gold Corporation, in coordination with Bitterroot Restoration, Inc. of Corvallis, MT. Special thanks to Cathy Zabinski and October Seastone-Moynahan for their assistance with mycorrhizal work and to John Barta for his assistance, genuine interest, and concern for environmental restoration.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

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