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Department of Microbial Ecology, University of Lund, Ecology Building, SE-223 62 Lund, Sweden
Jan Pallon
Department of Nuclear Physics, University of Lund, P.O. Box 118, SE-221 00 Lund, Sweden
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A laboratory experiment was performed to estimate the elemental composition of rhizomorphs of an ectomycorrhizal (EM) fungus growing in a patchy environment. Successive samples of Rhizopogon rhizomorphs, located adjacent to patches with organic matter or patches with acid-washed sand, were taken over a period of 45 d. The mass per unit area was analyzed with scanning transmission ion microscopy (STIM), and the elemental content of elements heavier than Mg were analyzed with particle induced X-ray emission (PIXE). Rhizomorphs associated with the organic matter on average were three times heavier per unit area than rhizomorphs associated with sand. The Ca concentration (mg g–1) increased in rhizomorphs adjacent to patches with sand, while it decreased in rhizomorphs adjacent to patches with organic matter. Fe concentration was higher in rhizomorphs adjacent to patches with sand. We concluded that the EM fungus responded to the organic matter by producing larger rhizomorphs, rather than increasing the concentration of elements in the rhizomorphs, to improve the transport of elements to the roots. The elemental composition of rhizomorphs varied considerably over time, and the accumulation of Ca in rhizomorphs in the sand-filled compartments could be the effect of acropetal flow of solutes from the plant roots toward the mycelial front.
Key words: mycorrhiza, phosphorus, PIXE, potassium, translocation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Many EM fungi form rhizomorphs or cords (Agerer 1988, Rayner and Boddy 1988), which are linear structures of vegetative hyphae facilitating the transport of mineral nutrients and carbon over considerable distances (Smith and Read 1997). Agerer (1987–1998) divided rhizomorphs into six groups, where the most differentiated ones have thick central vessel hyphae to improve the transport of elements. Acropetal translocation of carbon toward the mycelial front occurs mainly in the apoplast of empty vessel hyphae in the rhizomorphs, while basipetal translocation of mineral nutrients toward the roots occurs in the symplast of living hyphae (Cairney 1992).
The elemental composition of rhizomorphs is dependent on substances transported in the rhizomorphs and material deposited on the surface. When EM mycelia and rhizomorphs senesce after a nutrient source has been exhausted (Bending and Read 1995b), it is likely that the concentration of solutes being transported in the rhizomorphs will decrease while the concentration of waste elements deposited on the surface of rhizomorphs might increase.
When an EM mycelium grows out into the soil from a mycorrhizal root, the exploring mycelial front responds to a nutrient patch in the soil by increasing its branching frequency to form a dense mycelium that exudes nutrient-mobilizing enzymes (Bending and Read 1995a) and organic acids (Grifftiths et al 1994) into the soil. The hyphal tips at the mycelial front are usually hydrophilic while hyphae behind the mycelial front usually are hydrophobic and can differentiate into hydrophobic rhizomorphs (Unestam and Sun 1995). Nutrients mobilized from the soil are transported to the host trees via the rhizomorphs. Bending and Read (1995b) demonstrated that Suillus bovinus and Thelephora terrestris mycelia mobilized significant amounts of N, P and K from a small amount of partly decayed forest floor litter added to a microcosm. Between 13 and 30% of the original content of these elements in the organic matter was mobilized within 40 d, when the mycelium started to senesce, presumably due to exhaustion of the available nutrients in the patch. Ca and Mg however, were not mobilized, and the concentrations of these elements even increased in the organic matter after colonization by T. terrestris (Bending and Read 1995b), presumably because elevated Ca content in the organic matter after colonization by EM fungi precipitated with oxalic acid exuded by the fungus to form calcium oxalate, which often covers mycelia sampled from soil (Cromack et al 1979).
Export of elements from a nutrient patch by EM fungi can result in elevated translocation velocities in the rhizomorphs, elevated concentrations of elements in the rhizomorphs or elevated sizes or numbers of the rhizomorphs connecting the mycelial front with the host plant. Translocation velocity for P has been measured in some rhizomorphs of EM fungi (Kammerbauer et al 1989, Timonen et al 1996). Very little is known about the elemental composition of EM rhizomorphs, especially the temporal variation in elemental composition of rhizomorphs connected to a foraging mycelium in forest soil.
Wallander et al (2003) sampled T. terrestris rhizomorphs from mesh bags buried in forest soil and found that the Ca concentration increased 1 to 3 mg Ca g–1 when mesh bags were amended with apatite compared with mesh bags containing pure quartz sand. Furthermore, in a laboratory experiment, it was found that the Ca content in rhizomorphs of Rhizopogon sp. increased from 1 to 3 mg Ca g–1 to 20–30 mg Ca g–1 when the fungus colonized apatite and large amounts of calcium oxalate were found on the surface of the rhizomorphs (Wallander et al 2002). Wallander et al (2002) suggested that oxalic acid was exuded to release P from the apatite, although Unestam and Sun (1995) suggested that oxalate crystals on the outside of hyphae also might be the result of the exudation of waste products.
Similarly to Ca accumulation on the outside of hyphae, Fe has been found to accumulate on the outside of root cell walls when growing in low-fertility soils. This might be a mechanism for the release of P from sparingly soluble Fe phosphates, as suggested by Sattelmacher (2002, and references therein).
In the present study we used Pinus muricata seedlings inoculated with Rhizopogon sp. in a laboratory experiment where individual mycelia were exposed to either an inert material (acid-washed quartz sand) or fresh organic matter. Successive samples of rhizomorphs were taken between the root tips and the colonized material over 45 d to follow the temporal change in chemical composition of the rhizomorphs. The mass (per unit area) of the rhizomorphs was estimated by scanning transmission ion microscopy (STIM) and the elemental composition was analyzed by particle-induced X-ray emission (PIXE).
The objective of our study was to investigate how Rhizopogon rhizomorphs responded to nutrient patches in terms of elemental composition and morphology. Exploitation of a nutrient patch was expected to result either in elevated concentrations of K and P in the rhizomorphs or larger sizes of the rhizomorphs. We expected the Ca and Fe content of the rhizomorphs to increase over time because these elements can precipitate on the outside of the rhizomorphs while concentrations of P and K were expected to decrease when rhizomorphs started to senesce. To ascertain whether different elements were associated through cotransport or coprecipitation, correlation analysis was performed on all areas of the rhizomorphs where the elements were quantified.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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between Pinus muricata D. Don seedlings and Rhizopogon 2272 (Boletales, species group IV in Kretzer et al 2000) isolated by M. Bidartondo from a monotropoid mycorrhiza of Pterospora andromeda in a Pinus ponderosa forest at the Sierra National Forest, California, USA). Three mycorrhizal seedlings were transferred to three transparent polystyrene microcosms (245 x 245 x 25 mm (Nunc A/S, Roskilde, Denmark). These microcosms are a variation of those used by Ek (1997) (FIG. 1).
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). The soil was sieved through 2 mm mesh and microwaved to 90 C twice with an interval of 2–3 d to eliminate propagules from mycorrhizal fungi. Thereafter the soil was not maintained under aseptic conditions. Soil in the fungal compartments was changed every 3 mo, and this added mineral nutrients to the system. Water was added regularly to the root compartment, while no addition of water was required in the fungal compartments. Each microcosm was wrapped in aluminum foil, placed in a ventilated plastic bag and maintained at 200 µmol m–2 s–1 PAR (photosynthetically active radiation), 80% relative humidity, and an 18/6 h, 18/16 C, day/night cycle in a growth cabinet. Seedlings were approximately 18 mo old when they were used in the experiment. Three microcosms were selected with both fungal compartments colonized, and the soil in the fungal compartments was replaced with 75 g of acid-washed sand (0.36–2.0 mm, 99.6% SiO2, Ahlsell, Sweden). Three containers (2.5 cm diam) were placed in each fungal compartment. In each microcosm the three containers in one fungal compartment were filled with organic matter from the fermentation layer collected from the same Pinus sylvestris forest described above. The three containers in the other fungal compartment were filled with acid-washed sand (controls). The elemental composition of the sand and organic matter is reported (TABLE I). The fungal mycelium colonized the containers by growing over the edge of the container, which was 0.5 mm thick.
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). Care was taken to minimize disturbance of the mycelium around the residual containers. Therefore samples first were taken from the two outer containers and the final sample was taken from the central container. The rhizomorph segments were immediately lyophilized and frozen at –20 C until PIXE/STIM analysis. PIXE analysis.— – PIXE analysis is a multi-elemental technique based on the detection of characteristic X-rays produced by MeV ions; protons or heavier. PIXE is analogous to energy-dispersive X-ray analysis (EDX), but its sensitivity is much higher and can detect elements at the ppm level. The analyses were performed at the Lund Nuclear Micro-probe Laboratory where a focused, micrometer-size beam was scanned across the sample. At each point of the sample, data were acquired for elemental analysis and stored on a CD. In parallel, data were evaluated to yield quantitative elemental maps for monitoring and to select parts of the sample for more detailed analysis.
Scanning transmission ion microscopy (STIM) (Overley et al 1988, Lefevre et al 1987) was performed at the same time as PIXE analysis to determine the mass per unit area of the sample. STIM is based on the detection of energy loss when protons pass through the sample. In these experiments STIM measurements were performed in an on-axis/off-axis geometry (Pallon et al 2004, Pallon 1987) permitting simultaneous PIXE and STIM measurements.
Samples of rhizomorphs or mycelia were placed on 2.0 µm plastic foil (Kimfol®), mounted on a plastic ring and covered with a second foil to form a sandwich. A 2.5 MeV proton beam with a current of 300 pA was focused to about 5 µm. Each sample typically was scanned over an area of 256 x 256 µm for 25–35 min or until the data collected presented sufficiently detailed elemental maps of P, S, K, Ca and Fe. Some samples were scanned several times at different locations. The averages of these scans were used to calculate the content of different elements in these samples, while the individual measurements were used in the correlation analysis. After analysis images were created by the CSIRO Dynamic Analysis method (http://www.nmp.csiro.au/dynamic.html), which enables quantitative, true-elemental images to be unmixed from the generally complex PIXE energy spectrum (Ryan and Jamieson 1993). The program is built with the software package IDL 5.6 (Research Systems 2002, www.ResearchSystems.com). The elemental images were inspected to select regions for precise quantitative evaluation. We selected regions that appeared to represent whole samples and avoided parts contaminated by soil particles. From these regions detailed PIXE spectra were constructed from resorted data and the spectra were fitted to yield quantitative information. From the corresponding STIM spectra, the local mass per unit area of the sample was determined and the elemental content per unit dry weight calculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). On the final sampling occasion the mycelium inside the patches had turned brown, and the rhizomorphs collected on this occasion were also brown. The rhizomorphs sampled from the sand-filled compartments however were white during the experiment, including the final sampling occasion.
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The elemental composition varied considerably between microcosms and between different sampling occasions, which hampered the detection of statistically significant changes between different sampling occasions. However some significant trends were observed. The Ca content decreased with time in rhizomorphs that were associated with organic material in all three seedlings (TABLE II). The values on average had declined to a third of the value on the first sampling occasion. Ca concentration in rhizomorphs from the sand compartment conversely had increased on average 9x between the first and the last sampling occasion. Values were less clear for other elements but most elements (including P, K, S and Fe) tended to decrease on the last sampling occasion when the rhizomorphs had degenerated in the compartments containing organic matter (TABLE II). In general P, K and S were distributed more uniformly in the rhizomorphs while Ca was distributed irregularly in the rhizomorphs (FIG. 3).
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The content of P was positively correlated with the contents of K, S and Zn, and the Ca content was positively correlated with the contents of Fe, Si and Cu (TABLE III, FIGS. 4 and 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Unestam 1991). The rhizomorphs connecting this exploring mycelium with the root tips responded by increasing the mass per unit area by an average of 3x the mass of rhizomorphs growing in the compartments containing pure sand. The concentration of elements in the rhizomorphs remained constant or decreased during the period when the organic material was colonized. This suggests that the fungus responded to the nutrient patch by increasing the volume of the connective rhizomorphs to facilitate transport, rather than increasing the concentration of elements in the solute transported in the rhizomorphs. This enhanced capacity for transport can be expected to occur in both directions because carbon is needed to produce enzymes to facilitate the utilization of the nutrient patch and mineral nutrients from the nutrient patch (N, P) are transported toward the roots (Cairney 1992). Translocation in rhizomorphs is driven by concentration gradients toward sinks for various compounds, according to Cairney (1992). Mineral nutrients and water are transported basipetally toward the roots, where mineral nutrients and water are consumed by the host. This maintains the concentration gradient while carbon is transported acropetally to the hyphal front where enhanced use of carbon stimulates C translocation. This probably occurred in the compartments containing organic matter in our experiment. The much lower concentrations of Ca and Fe in rhizomorphs associated with organic matter compared to rhizomorphs associated with sand also could be an effect of dilution because the rhizomorphs associated with organic matter were much larger.
The accumulation of Ca in the Rhizopogon rhizomorphs with time (TABLE III, FIG. 4) in the sand-filled compartments could be an indication of a net flux of water toward the hyphal front rather than the root. Ca must have been transported acropetally from the root compartment to the sampled rhizomorphs because almost no Ca is available in the acid-washed sand. Among the primary plant nutrients, Ca is the least mobile (McLauglin and Wimmer 1999) and because it is taken up passively from the soil and transported by mass flow driven by the transpiration stream (Bangerth 1979) it usually accumulates in plant tissue that has had access to large volumes of transpiration solutes, such as older needles (Rosengren-Brinck and Nihlgård 1995). The accumulation of Ca in the rhizomorphs of the sand compartment in our study could be an effect of acropetal flow of solutes from the plant roots toward the mycelial front. The high relative humidity around the shoots probably resulted in low transpiration rates, which favor transportation of solutes toward the mycelial front. No water was required in the fungal compartment while water was added regularly in the root compartment. And this indicates that net water moved toward the mycelial front. The flow of water probably is pressure driven, which might result in exudation of droplets at hyphal tips. These droplets of water on mycorrhizal hyphae have been found to contain oxalate, which can precipitate with calcium in the soil to form calcium oxalate crystals on the surface of the hyphae (Unestam and Sun 1995). The high amounts of Ca present in the Rhizopogon rhizomorphs in the sand-filled compartments in our study is likely to be calcium oxalate produced in this way. Long distance Ca transport by the wood-decomposing fungus Resinicium bicolor was demonstrated by Connolly and Jellison (1995), who showed that Ca moved from wood blocks and precipitated as calcium oxalate on the outside of the rhizomorphs up to 10 cm from the source. A large capacity to take up and transport Ca also is evident in the fungus Serpula lacrymans, which can cause serious deterioration in buildings (Low et al 2000). Rhizopogon rhizomorphs also were found to accumulate Ca when colonizing apatite, while the P released from the apatite presumably was transported to the host (Wallander et al 2002). Hagerberg et al (200x) similarly found that the content of Ca increased in distant parts of an EM mycelium when a portion of the mycelium was exposed to Ca-containing wood ash granules, indicating distribution of Ca over large parts of the mycelium.
Water released from hyphal tips and pores in the hyphae also has been suggested to facilitate nutrient uptake by increasing the contact with soil particles. Querejeta et al (2002) demonstrated that water hydraulically lifted by Quercus agrifolia roots was allocated to mycorrhizal hyphae, which could thereby maintain their activity in dry soil. Furthermore Sun et al (1999) demonstrated that a pressure gradient could form to move water from mycorrhizal roots toward the mycelial front, which potentially can stimulate nutrient uptake from a dry soil.
Rhizopogon mycelia are highly unlikely to use Ca as a nutrient source because the concentration of Ca in the cytosol must be strictly controlled and maintained at a low level (Alberts et al 1994). It is much more likely that Ca has followed the water flow in the apoplast of the fungal tissue, as discussed above. However a more important role of EM fungi in Ca uptake was suggested by Blum et al (2002), who demonstrated that ectomycorrhizal fungi could obtain large amounts of calcium from apatite sources in the soil and make this source available to trees in calcium-poor forest ecosystems in the USA. The importance of calcium availability for the structure and function of forest ecosystems also had been emphasized by McLauglin and Wimmer (1999).
No accumulation of Fe was found in degenerating rhizomorphs collected from the compartments containing organic material. Thus we found no indication that the fungus had released P from iron phosphates in the organic material by binding Fe to cell wall components, as suggested to occur in plants (Sattelmacher 2002). The Fe content of Rhizopogon in the present study was low and comparable to the Fe content of Suillus granulatus collected from mesh bags buried in the forest floor (Wallander et al 2003). EM species such as Tylospora fibrilosa and Thelephora terrestris by contrast can contain much larger amounts of Fe (Wallander et al 2003) and it is possible that these species are more important in releasing P from iron phosphates.
The positive correlation among P, K and S content might exist because these compounds are associated with cytoplasmic and vacuolar constituents in the hyphae, while the correlation among Ca, Fe and Mn might indicate that these elements are more associated with the outer surface of the rhizomorphs. Sulphur is a component of proteins and phosphorus is part of the polyphosphate that is located in the vacuoles. Ashford et al (1999) demonstrated that K+ was the most common counter-ion to polyphosphate in motile vacuoles of Pisolithus tinctorious mycorrhizas. And the positive correlation between P and K and the lack of correlation between P and Ca in our study also suggests that K rather than Ca is associated with P in EM rhizomorphs. Jentschke et al (2001) found that translocation of K and Mg increased when P was added to EM mycelia, suggesting that these elements were cotransported.
In conclusion mycelia of Rhizopogon responded to an organic nutrient patch by forming a dense mycelium and increasing the size of the rhizomorphs to increase the flow of nutrients from the nutrient patch to the mycorrhizal roots. Elemental composition of fungal rhizomorphs can vary considerably over time when a fungus explores the soil for nutrients. This will influence the heterogeneity of elements in the forest floor, especially of elements such as Ca and Fe, which can accumulate to high concentrations in EM rhizomorphs and mycelia.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: Hakan.Wallander{at}mbioekol.lu.se
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