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Doi:10.1078/1433-8319-00012

Vol. 4/1, pp. 13–27 in Plant Ecology,
Urban & Fischer Verlag, 2001 Evolution and
Ectomycorrhizas:
their role in forest ecosystems
under the impact of acidifying pollutants

WSL Swiss Federal Research Institute for Forest, Snow and Landscape Research, 8903 Birmensdorf,Switzerland; e-mail: brunner@wsl.ch The physiologically active lateral rootlets of all main trees in temperate forests arecolonised by ectomycorrhizal fungi, forming so-called ectomycorrhizas. These symbi-otic organs are the sites of exchange of nutrients, mainly P and N, provided from thefungal partner, and C from the host. Emerging from the ectomycorrhizas, fungal hy-phae exploit the soil for the mobilisation and absorption of water and nutrient ele-ments. By doing so, they connect the tree roots intimately with the soil and provideanchorage. The deposition of acidifying pollutants into forest ecosystems is a poten-tial threat to the health and vitality of forest trees because it leads to the acidificationand eutrophication of forest soils. Pollutants are also a threat to the functioning of ec-tomycorrhizas. Increased N concentrations in the soil lead to enhanced fungal N up-take and storage, and to enhanced N transfer to the host plants, and therefore tohigher plant biomass of above ground parts. In consequence, there is a decrease of Callocation to the plant roots. This in turn leads to reduced ectomycorrhization, and toreduced production of external mycelia and fruiting bodies. Soil acidification leads toenhanced availability of Al, heavy metals, and radionuclides in the soil, all of whichcan be toxic to plants and fungi. Reduced growth of roots and hyphae are amongstthe first symptoms. In ectomycorrhizas, the hyphae of the fungal tissues contain vac-uolar polyphosphates which have the ability to bind Al, heavy metals, radionuclidesand N. These electronegative polymers of phosphates represent an effective storageand detoxifying mechanism which otherwise is lacking in roots. Therefore, ecto-mycorrhizas have the potential to increase the tolerance of trees to acidifying pollu-tants and to the increased availability in the soil of toxic elements.
Key words: ectomycorrhizas, forests, heavy metals, nitrogen, radionuclides, soil
acidification
In the winters of 1990 and 1999, the hurri- consequences for the valleys and their canes "Vivian" and "Lothar" swept across Eu- human populations. Damaged forests can no rope and destroyed or damaged large areas longer entirely fulfil their protective functions of forest, and uprooted or snapped thou- against avalanches, rockfalls, land slides, sands of trees. In mountainous and subalpine flooding, and erosion. Following these regions of the Alps such destruction of forests events, the question arose as to whether soil has dramatic socio-economic and ecological acidification and eutrophication from aerial 1433-8319/01/4/01-13 $ 15.00/0 pollutants contributed to the problem because The ectomycorrhizal symbiosis
the trees had damaged roots and reduced an-chorage in the soils. Many foresters remark Ectomycorrhizal organs arise spontaneously that trees today appear to have smaller root when hyphae of ectomycorrhizal fungi come systems than in earlier days. into contact with compatible and un- In nature, all physiologically active lateral colonised young lateral rootlets. After the hy- rootlets of the major trees of the forests in bo- phae have contacted the root surface, which real or temperate regions are colonised by is associated with a switch of the hyphal mycorrhizal fungi to form "mycorrhizas" (from growth pattern from an apical-dominated to the Greek meaning "fungus-root", Frank a multibranched and multiple apices mode 1885). Because these mycorrhizas of trees (Brunner & Scheidegger 1992), they pene- have ectotrophic fungal tissues they are trate the rootlets intercellularly. A densely in- called "ectomycorrhizas" (Smith & Read terwoven, two-dimensional fungal tissue 1997). Ectomycorrhizas are the sites for the composed of so-called palmettes develops exchange of nutrients between the plant and between the epidermal and cortical cells, the fungus, and are therefore regarded as and forms the Hartig net (Scheidegger & mutualistic symbioses (Smith & Read 1997).
Brunner 1999; Fig. 1). The growth of the hy- Ectomycorrhizas develop on the lateral phae is probably restricted by increased lev- rootlets of long roots and are composed of els of phenylpropanoids and cell wall thick- both fungal and plant tissues. An ectomycor- enings (Weiss et al. 1999). As a result, api- rhiza consists of the following fungal and cal meristem and stele remain uncolonised plant components: (i) the fungal mantle en- by fungal hyphae. The Hartig net tissue sep- veloping the rootlet, (ii) the intercellular fungal arates epidermal and cortical cells from tissue (the so-called "Hartig net") occurring each other, although they are still connected between the epidermal and cortical cells, (iii) by plasmodesmata (Scheidegger & Brunner plant epidermal, cortical and endodermal 1993). Root cap cells which accumulate cells, (iv) the plant apical meristem, and (v) polyphenolics are lysed by the fungal hy- the plant stele. Root hairs are lacking be- phae and incorporated into the fungal man- cause their formation is suppressed due to tle (Weiss et al. 1997). the fungal interactions with the rootlet. In- In ectomycorrhizas, fungal hyphae take up stead of root hairs, starting from the fungal nutrients and water from the pedosphere and mantle, a vast external fungal mycelium in- transport them to the fungal mantle where vades the surrounding soil, penetrating into they are metabolised and stored (Fig. 2). The the finest soil pores. By doing that they con- Hartig net hyphae then transfer the nutrients nect the roots with the soil and provide stabil- to the host in exchange for plant C. The major ity to the trees. Due to their high absorption nutrients which are taken up, metabolised, surfaces, fungal hyphae have higher capaci- stored, and exchanged with the host are N ties than root hairs for mobilising and absorb- and P (Read 1999). Absorbed inorganic N is ing water and nutrient elements. By exuding metabolised in the fungal hyphae to the organic acids fungal hyphae are even able to amino acids glutamate and glutamine (Fig.
enter into weatherable minerals and utilise 3). There is evidence that glutamine from the mineral nutrients (Jongmans et al. 1997). El- fungus is exchanged for non-nitrogen con- ements absorbed are transported in the fun- taining organic molecules such as ketoacids gal mycelium to the fungal mantle and Hartig from the plants (Botton & Chalot 1999; net for metabolisation and storage. In the Hampp & Schaeffer 1999). However, the Hartig net, which represents the interfacial main plant carbohydrates which are taken up exchange zone of the two organisms, the fun- by the fungal Hartig net hyphae are glucose gus N and P are exchanged for plant C and fructose; these are derived from sucrose (Smith & Read 1997). As a result, ectomycor- after hydrolisation by root cell wall acid inver- rhizal plants often have higher N and P con- tase. After absorption by the fungal hyphae, tents than non-mycorrhizal plants (Colpaert these compounds are converted into the fun- et al. 1999; Brunner & Brodbeck 2001; gal carbohydrates trehalose, mannitol, and et al. 2001). They may also exhibit glycogen (Hampp & Schaeffer 1999). Absor- higher resistance against drought, frosts, and ped inorganic phosphates are transferred pathogens (Read 1999), and possibly higher into vacuolar pools of inorganic polyphos- phates and stored as linear polymers in the


Ectomycorrhizas in forest ecosystems under acidifying pollutants 15
Fig. 1. Stages of ectomycorrhizal development (modified after Brunner & Scheidegger 1992; Martin & Tagu
1999; Scheidegger & Brunner 1999). Sign, signalling between fungal and root cells; Adh, adhesion of hy-
phae to root surface; Bran, branching of hyphae; Man, mantle formation; Pen, penetration of hyphae be-
tween root cells; Har, Hartig net formation; Met, alteration in metabolism; Stor, storage of elements in vac-
uoles and vacuolar P-rich particles (arrows) of Hartig net hyphae (h); Tran, transfer of nutrients between
symbionts (bars, 5 µm). Blackwell Science Ltd (Adh, Man; Brunner & Scheidegger 1992, New Phytologist,
120, 359–369; Stor; Frey et al. 1997, Plant, Cell and Environment, 20, 929–937) and Springer-Verlag
(Har; Scheidegger & Brunner 1999, Mycorrhiza: Structure, Function, Molecular Biology, and Biotechnology,
pp. 205–228, Springer, Berlin) are acknowledged as original sources of the photographs.
mantle and Hartig net hyphae. It is still a mat- partners play an active role in the acquisition ter of debate to what extent these polyphos- of nutrients from localities and sources not phates are present in vivo in a particulate available to roots, and to transport them over form ("polyphosphate granules"; Bücking long-distances in hyphae or mycelial strands et al. 1998; Bücking & Heyser 1999) or dis- to the ectomycorrhizas (Brandes et al. 1998; persed in the vacuoles (Ashford et al. 1999).
Jentschke et al. 2001). As a result, ecto- Polyphosphates give the ectomycorrhizal mycorrhizal plants often have a higher uptake fungi the potential to accumulate phosphate of P, N, K or Mg than non-mycorrhizal plants, and possibly re-mobilise it under low phos- resulting in higher plant tissues concentra- phate conditions in order to maintain a contin- tions (Colpaert et al. 1999; Brunner & Brod- uous P supply to the plant (Bücking & Heyser beck 2001; Jentschke et al. 2001).
1999, 2000). They are associated with accu- Ectomycorrhizal organs have a lifespan of mulations of other nutritional elements such one to two vegetation periods (Egli & Kälin as Ca, K, Mg, N and S (Frey et al. 1997; 1991), but they can, after the regrowth of the Bücking et al. 1998; Bücking & Heyser 1999; apical meristems, become recolonised by the Vesk et al. 2000). The exchange of nutrients same or by another ectomycorrhizal fungus.
between the two symbionts is such that the In central Europe, about 1,500 fungus species roots are a permanent sink for C, while the or about one third of the known macromycete external mycelia are a sink for N and P. These flora are thought to be ectomycorrhizal sym- symbiotic relationships mean that the fungal bionts. They include many well known edible Fig. 2. Uptake, transport, metabolism, storage, and transfer of nutritional elements in ectomycorrhizas
(modified from Brunner & Scheidegger 1995; Scheidegger & Brunner 1999; bar, 10 µm). Springer-Verlag is
acknowledged as original source of the photograph (Scheidegger & Brunner 1999, Mycorrhiza: Structure,
Function, Molecular Biology, and Biotechnology, pp. 205–228, Springer, Berlin).
basidiomycetes and ascomycetes such as Inputs of acidifying pollutants
boletus, truffles and chanterelles. Ectomycor- into forest ecosystems
rhizal fungi are polyphyletic, but they have incommon, that they all depend upon the sym- By-products of human activities since the biotic stage to produce fruiting bodies in order onset of the industrial revolution have caused to complete their life cycles. However, the inadvertent changes to ecosystems. It is in- successful production of fruiting bodies in as- creasingly realised that pollution of soil, water, sociation with their hosts has been possible in and air has economic, social and ecological culture only for Hebeloma cylindrosporum consequenses. Gaseous pollutants originate and Laccaria bicolor (Debaud & Gay 1987; from the combustion of fossil fuels in power Godbout & Fortin 1992). generation, industry and transportation. Pro- Ectomycorrhizas in forest ecosystems under acidifying pollutants 17
Fig. 3. Nitrogen (k) and C (c) metabolism in ectomycorrhizas under elevated N inputs (modified from
Dähne et al. 1995; Botton & Chalot 1999; Hampp & Schaeffer 1999; v, vacuolar storage pool).
cesses related to agriculture and land use, plants (Nihlgård 1985; Magill et al. 1997). In such as decomposition of animal wastes in long-lived trees the impact of an altered soil large-scale livestock production systems, chemistry can result in chronic stress (Shafer paddy rice cultivation, and deforestation also & Schoeneberger 1991).
release some of the same and other gases(Shafer & Schoeneberger 1991). Much of theinterest in pollutant effects during the last Ectomycorrhizas in the chal-
decades has been focussed on forests, be- lenge of altering forest soils
cause of a widespread decline of tree healthin both North America and Europe (Fowler It is believed, that ectomycorrhizas have et al. 1999). In central Europe, high atmo- evolved to overcome the general deficiency of spheric inputs of acidifying pollutants (SO , low nutrient availability in terrestrial ecosys- tems (Allen 1991; Colpaert & van Tichelen last decades have led to an acceleration of 1996; Cairney 2000). It has also been sug- soil acidification, the loss of base cations, and gested that the ectomycorrhizal symbiosis the release of Al ions into soil solution as a made it possible for trees to colonise boreal consequence of proton-buffer processes zones where there is a low availability of N and (Matzner & Murach 1995; Blaser et al. 1999).
P (Read 1991). In view of the association of Acidification of soils also results in increased ectomycorrhizas with low nutrient conditions it availability of trace elements including heavy is not surprising that an altered soil chemistry metals and radionuclides. Excessive inputs of due to air pollutants, with more available N or atmospheric N result in soil acidification and trace metals, can result in stress. In ecto- in nitrate leaching, and can lead to a relative mycorrhizas, the site of action of a stress factor shortage of other nutritional elements for can either be the fungus or the plant, with Fig. 4. Effects of varying N loads (0 or 100 kg N ha-1.year-1 as NH NO ) on the substrate-attachment (vermi-
culite) of the root systems of ectomycorrhizal Norway spruce seedlings associated with Hebeloma crus-tuliniforme or of non-mycorrhizal control plants (bars, 2 cm).
primary responses being either positive or negative (Anderson & Rygiewicz 1991; Col-paert & van Tichelen 1996). Furthermore, pri- Agriculture, combustion of fossil fuels, and mary (direct) responses may be followed by other human activities have altered the global secondary (indirect) responses. Conse- cycle of N substantially, and increased both quenses of stress can either be altered plant C the availability and the mobility of N over large supply to the roots, altered fungal absorption of regions. In terrestrial ecosystems the conse- nutrients from the soil, or altered exchange ca- quences of these changes are (i) higher input pacities between the Hartig net and the host rates of N into N cycles, (ii) increased concen- cells (compare also Dighton & Jansen 1991).
trations of the potent greenhouse gas N O, Through a series of metabolic feedbacks, ecto- (iii) increased transfer of N, mainly nitrate, into mycorrhizas eventually reach a new steady ground water, (iv) soil acidification, (v) losses state enabling the symbiosis to be stress toler- of soil nutrients such as Ca and K, (vi) in- ant (Anderson & Rygiewicz 1991). Indicators creased storage of organic C in terrestrial of stress in ectomycorrhizas include alterations ecosystems, and (vii) accelerated losses of in the accumulation and metabolism of ele- biological diversity of plants, animals and mi- ments, and ultrastructural changes. Further- croorganisms (Vitousek et al. 1997). more, the abundance and diversity of external Tree growth in boreal and temperate re- mycelia, of ectomycorrhizas, and of fruiting gions is typically N-limited (Vitousek & bodies are also thought to be sensitive indica- Howarth 1991). There is considerable evi- tors of antropogenic pollutants.
dence that microbial processes in forest soils, Ectomycorrhizas in forest ecosystems under acidifying pollutants 19
metabolic processes in forest trees and forest antagonistic relationship. This alteration is pos- ecosystem functioning tend to be adapted to sibly caused by a disturbed recognition be- N limitations rather than N excess (Rennen- tween the two partners (Anderson 1988). Ele- berg & Gessler 1999). However, atmospheric vated N conditions at polluted sites or after inputs of reactive N compounds have in- fertilisation treatments also induce changes in creased in the last decades from less than 10 the species composition of the fungal partners kg N ha-1.year-1 to values of 60 kg N ha-1.year-1 in the ectomycorrhizal root tips and in the fruit- or more in polluted regions (Rennenberg ing bodies (Arnolds 1991; Arnolds & Jansen & Gessler 1999). If ectomycorrhizas have 1992; Brandrud 1995; Karen & Nylund 1997; evolved to overcome the general stress of low Peter et al. 2001). nutrient availability in terrestrial ecosystems Ectomycorrhizas and their extramatrical (Allen 1991; Colpaert & van Tichelen 1996), mycelia influence N mobilisation, uptake and the increased N availability is likely to have metabolism, and, as a consequence, the N considerable impact upon the function of status of the whole plant. The uptake of N is ectomycorrhizas as organs of nutrient uptake, enhanced due to the extramatrical mycelia ex- transport, metabolism, storage and transfer. ploiting the substrate efficiently and enlarging It is widely accepted that the provision of the absorbing surface, and due to the exuda- plant photoassimilates to the fungal partners tion of organic acids and enzymes responsible is the key factor for the formation and main- for mobilising and taking up inorganic and or- tainance of ectomycorrhizas (see also Wal- ganic N resources (Chalot & Brun 1998; Read lenda & Kottke 1998). Increased N inputs into 1999). Ectomycorrhizal hyphae take up inor- trees leads to an increase of above ground ganic N (NH +, NO -) as well as organic N com- biomass (van Dijk et al. 1990; Flückiger & pounds such as amino acids, and metabolise Braun 1998) but to a reduction of C allocation and store N as amino acids and proteins in the to the roots (Wallenda et al. 1996). This leads hyphae of the fungal mantles (Chalot & Brun in turn to a C deficiency for ectomycorrhizal 1998; Wallenda et al. 2000). In fungal mantles, fungi, which is reflected in a decrease of ecto- the concentrations of N ranges from 2.9–4.4% mycorrhization (Haug & Feger 1990/1991), whereas in the inner part of ectomycorrhizas it reduced amounts of external mycelia (Wallan- is only 0.9–2.1% (Högberg et al. 1996). Recent der & Nylund 1992; Arnebrant 1994), and investigations after applying fertilisers have lower production of fruiting bodies (Godbout & shown that storage of N in mantle hyphae Fortin 1992). An obvious visible indication of mainly occurs in vacuolar deposition bodies the inhibited growth of the external mycelia is (Kottke et al. 1995). Bücking et al. (1998) pro- the small amounts of substrate which are at- posed that these N storage bodies are identi- tached to root systems developed at elevated cal to the polyphosphate granules in vacuoles, N loads (Fig. 4). Further investigation under and that, as has been shown for Neurospora, experimental conditions reveals a decrease of these negatively charged granules can bind the fungal tissues within rootlets and a de- basic amino acids such as arginin. In ecto- crease of fungus-specific compounds such as mycorrhizas of Xerocomus badius, N was con- ergosterol, trehalose and mannitol (Wallander centrated chiefly in large, rather diffuse-lined & Nylund 1991; Wallenda et al. 1996). High N vacuolar bodies but not in small, well-defined concentrations also cause enlarged cortical bodies (Kottke et al. 1998). Kottke et al.
cells (Brunner & Scheidegger 1995), and con- (1995), Beckmann et al. (1998) and Turnau et tacts with fungal hyphae induce cell wall thick- al. (2001) observed that the numbers and N enings (Haug et al. 1992; Brunner & Schei- contents of these granules increased in hy- degger 1995) which contain elevated Ca con- phae of ectomycorrhizal mantles after N fertili- centrations (Frey et al. 1997) and callose (Brunner & Schneider 1996). These re- A significant increase is also evident in the N sponses are similar to the defense responses concentration in root tips colonised by Paxillus of hosts upon attack by pathogenic fungi. In- involutus following N additions (Wallander et al.
tracellular penetrations of hyphae into cortical cells (Jentschke 1990; Holopainen & In general N fertilisation leads to increased Heinonen-Tanski 1993; Brunner & Scheideg- plant biomass, but reduces ectomycorrhiza ger 1995) support the suggestion that high N formation and decreases the root/shoot ratio.
concentrations affect the mutualistic symbio- Further, while N concentrations in the plants sis of ectomycorrhizas and alter it to a more usually increase, P and K concentrations tend to decrease (Termorshuizen & Ket 1991; mycorrhizal function results not only in in- Seith et al. 1996; Wallenda et al. 1996). In a creased nitrification and nitrate mobility (Aber greenhouse study, in which varying N loads et al. 1998), but also to changes in the ele- were applied to ectomycorrhizal Norway ment supply to plants.
spruce seedlings associated with Hebelomacrustuliniforme or with Laccaria bicolor or tonon-mycorrhizal controls, elevated N loads Metals and radionuclides
led to enhanced nitrate reductase activities infine roots and ectomycorrhizas (Brunner et al.
Atmospheric pollution leading to soil acidifica- 2000), and to enhanced N concentrations in tion and elevated concentrations of trace met- the plants (Brunner & Brodbeck 2001). Phos- als is a significant threat to many forest phorus and Zn concentrations decreased ecosystems (Innes 1993; Godbold 1994). In- under high N loads. In the same experiment, creased inputs of acidifying substances accel- ectomycorrhization led to enhanced N and P erate weathering processes and increase the but decreased Mn concentrations (Table 1; availability of Al and heavy metals in soils.
Brunner & Brodbeck 2001). Thus, to a certain Additionally, heavy metals enter into both extent, the ectomycorrhization compensated agricultural and non-agricultural lands via for the decrease in plant P concentration many routes including disposal of industrial caused by enhanced N loads. effluents, sewage sludge, deposition of air- Aber et al. (1998) posed the hypothesis borne industrial wastes, mining, industrial that ectomycorrhizal assimilation and exuda- solid waste disposal, and use of agricultural tion is the dominant process involved in im- chemicals (Saxena et al. 1999). The metal mobilisation of added N due to incorporation species commonly found include Cd, Co, Cu, of N into soil organic matter. During N satura- Hg, Ni, Pb and Zn. Although some of these tion, the composition of microbial communi- metals are required in small amounts by ties shifts from a high abundance of fungi, plants for their normal physiological activities, probably ectomycorrhizal fungi, to dominance excessive accumulation is toxic. The problem by bacteria (Tietema 1998). This loss of ecto- of metal toxicity is further aggravated by the Table 1. Mean element concentrations (mg g-1) in ectomycorrhizal Picea abies seedlings associated with
Hebeloma crustuliniforme or Laccaria bicolor or non-mycorrhizal controls after treatment with various N
loads of nitrate (kg N ha-1.year-1) (modified from Brunner & Brodbeck 2001). Probability level for 2-factorial
ANOVA: ns, not significant; *, P ≤ 0.05, **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.
Fungus inoculations (F) Ectomycorrhizas in forest ecosystems under acidifying pollutants 21
persistence of the metals in the environment.
reactive oxygen species, resulting in an in- Radionuclides, on the other hand, have been crease of antioxidative enzymes as a detoxifi- deposited within the past decades as fallout cation mechanism (Dietz et al. 1999). The de- from nuclear weapon testing and nuclear ac- gree of cell damage depends on the formation cidents. The predominant isotopes are 137Cs of these free radicals or reactive oxygen and 90Sr. The very long half-life times of these species, and on the efficiency and capacity of radionuclides, 30.2 and 28.5 years respec- detoxification and repair mechanisms. tively, renders them problematic. It is probable Heavy metals induce both plant and fungal that they are fixed in bacteria and fungal hy- cells to produce a wide range of low molecular phae of forest soils (Guillitte et al. 1994), and weight polypeptides and proteins with high very high activites have been measured in the cysteine contents; these are the so-called edible fruiting bodies of ectomycorrhizal fungi metallothioneins and metallothionein-like pro- (Haselwandter & Berreck 1994). teins (Gadd 1993; Prasad 1999). One of the An excess of heavy metals causes cell most important compounds in plants is a met- death in plants and fungi. These metals inacti- allothioneine of class III ("phytochelatin"), an vate enzymes and structural proteins by act- oligomer of glutathione, which is induced pre- ing on metal-sensitive groups such as sulfhy- dominantly by Cd, Cu and Pb stress (Zenk dril or histidyl groups (van Assche & Clijsters 1996). Phytochelatins form complexes with 1990; Gadd 1993); as a result they diminish metals and thus decrease the concentrations the integrity of biomembranes and reduce the of free metal cations in the cytoplasm. The activity of key enzymes such as nitrate reduc- metal-phytochelatin-complex can subsequently tase (Ernst 1996). Metals also bind to DNA be detoxified after transportation into vacuoles and affect cell division and cell elongation by (Dietz et al. 1999). Recently a gene coding for disruption of DNA synthesis (Godbold 1994).
the enzyme phytochelatin synthase was dis- Toxic concentrations of metals in plants cause covered and sequenced from Arabidopsis a wide range of morphological and structural (Clemens et al. 1999; Ha et al. 1999; Vatama- effects such as decreased root elongation, niuk et al. 1999). Homologs of this gene family root tip damage, collapse of root hairs, en- have also been found in yeasts. Less is known hancement of suberisation and lignification, about such proteins in ectomycorrhizal fungi.
and structural alterations of hypo- and endo- The only report is from Howe et al. (1997) who dermis (Barcelo & Poschenrieder 1999). They isolated metallothionein-like proteins from Cu- also influence the uptake of other mineral ele- tolerant strains of Laccaria laccata and Paxil- ments (Kabata-Pendias & Pendias 1992; lus involutus. The proteins had similar weights Turner 1994; Ernst 1996). Furthermore, met- (2.2–2.8 kDa) to those of known Cu-metalloth- als stimulate the formation of free radicals and ioneins in Neurospora or Agaricus. Table 2. Mean net counts of metals in compartments of freeze-fractures of ectomycorrhizas of Picea abies
seedlings associated with Hebeloma crustuliniforme after treatments with Al, Cd, Ni, or Zn, and after
measurements using a SEM-EDX (modified from Brunner & Frey 2000; highest values are in bold print;
nd, not detected; detection limit 80 counts).
Table 3. Mean element concentrations (mmol kg–1 dry weight) of cell compartments in cryosections within
ectomycorrhizas of Picea abies seedlings associated with Hebeloma crustuliniforme after Cs and Sr expo-
sure, and after measurements using a STEM-EDX (modified from Frey et al. 1997; highest values are in
bold; nm, not measured).
Hartig net hyphae Recent studies have indicated that coloni- Such electron-beam dense particles consisting sation of tree roots by ectomycorrhizal fungi of polyphosphates have been shown to bind can increase tolerance of their hosts to metals not only Al (Väre 1990; Kottke & Martin 1994; present in toxic concentrations in the soil (God- Martin et al. 1994), but also heavy metals such bold 1994; Turner 1994; Wilkinson & Dickinson as Cd and Zn (Turnau et al. 1993,1996; Bück- 1995; Leyval et al. 1997; Godbold et al. 1998).
ing & Heyser 1999) and the radionuclide Sr Studies under experimental conditions have (Table 3; Frey et al. 1997). shown, that a lower phytochelatin content in It is a matter of debate to what extent ecto- roots of Cd-treated Norway spruce can be ob- mycorrhizas can ameliorate metal stress in served when the plants where ectomycorrhizal plants (Godbold et al. 1998). Whether non- with Laccaria laccata compared to the non- mycorrhizal or ectomycorrhizal plants contain mycorrhizal controls (Galli et al. 1993). Ecto- more or less of the metals appears to depend mycorrhizal fungi confer metal tolerance by on the ectomycorrhizal fungal species used binding metals to electronegative sites on the and on the treatments applied. In investiga- cell walls of the hyphae, or binding to phos- tions under experimental conditions, Colpaert phates and sulfhydryl compounds within the & van Tichelen (1996) found similar Zn con- cells (Galli et al. 1994; Godbold et al. 1998).
tents in the shoots of Scots pines inoculated High amounts of metals in ectomycorrhizas of with Laccaria laccata and in non-inoculated Norway spruces seedlings associated with plants. In contrast, in Suillus bovinus inocu- Hebeloma crustuliniforme can be found pre- lated plants, most of the Zn was bound in the dominantly in the fungal mantle, Hartig net and external mycelium, and there were lower Zn cortical cells (Table 2; Brunner & Frey 2000). In concentrations in shoots compared to the un- Rhizopogon roseolus ectomycorrhizas from infected controls. Jentschke et al. (1999) calamine dumps, Turnau et al. (1996) found found that Norway spruces inoculated with that Cd was concentrated in the cytoplasm, Laccaria bicolor or Paxillus involutus and whereas Al was bound to P in vacuoles, and treated with Cd did not have significantly al- also extracellularly on the surface of the fungal tered Cd contents in the needles compared cell walls. In contrast, in Hebeloma crustulini- with non-mycorrhizal plants. In the needles forme ectomycorrhizas treated with heavy of Scots pines associated to Suillus luteus metals, there was cytosolic sequestration of Zn or Pisolithus tinctorius, van Tichelen et al.
but extracellular complexation of Cd in the Har- (1999) found significantly lower concentra- tig net (Frey et al. 2000). In Xerocomus badius tions of Cu than in plants which were non-my- ectomycorrhizas from acidic soils, Kottke et al.
corrhizal. Hartley-Whitaker et al. (2000) ob- (1998) demonstrated the occurrence of small served that Paxillus involutus inoculated distinct vacuolar bodies containing P and Al.
Scots pines had reduced Cd and Zn concen- Ectomycorrhizas in forest ecosystems under acidifying pollutants 23
trations in the shoots, whereas Suillus varie- detoxifying mechanism which prevents dam- gatus inoculated plants did not. Riesen & age to the host trees. If this mechanism is im- Brunner (1996) found in Norway spruces portant for the tree, a decrease of ectomycor- exposed to the radionuclides 134Cs and 85Sr rhizas and external mycelia due to pollutants that plants associated with Hebeloma crus- will have negative impacts on tree pollutant tuliniforme had significantly lower activities tolerance, on tree nutrition and possibly on than non-mycorrhizal controls, but only when tree anchorage. In this context, it has been a high N treatment was applied. However, in shown that Norway spruce seedlings react a similar study using 134Cs, activities were sensitively to forests soils with low pH result- only reduced significantly when plants were ing in reduced biomass and reduced Ca/Al treated with a Cs/K ratio above 1 (Brunner molar ratios (Brunner et al. 1999). The con- centrations of Al or the Ca/Al molar ratio in In view of the increasing metal deposition fine roots or in ectomycorrhizas, therefore, and metal solubility in the soils due to human might be valuable indicators in the assess- activities, the metal binding capacities of ecto- ment of the ecological risk of soil acidification mycorrhizal fungal mycelia and of ectomycor- (Cronan & Grigal 1995; Zysset et al. 1996). rhizas potentially gain an important role in Advances in the past few years using making trees tolerant of the new conditions.
molecular techniques have greatly increased Some frequently found ectomycorrhizas, e.g.
our ability to identify the fungal partners of ec- Xerocomus badius, have a high capacity for tomycorrhizas (Mehmann et al. 1995; Karen & element storage, including Zn and Fe, in par- Nylund 1997; Jonsson et al. 1999; Peter et al.
ticular in acidic soils (Kottke et al. 1998). This 2001). However, many questions still remain is, among others, one important reason why open and much research is required. The fol- ectomycorrhizal fungi are often considered in lowing issues will be particularly important for restoration programs for contaminated soils future progress: (i) to measure and quantify (Haselwandter & Bowen 1996; Haselwandter the external fungal hyphae emanating from 1997; Leyval et al. 1997).
ectomycorrhizas into the soil, (ii) to discoverhow different ectomycorrhizas vary in theirsensitivity, (iii) to determine the physiologicalconsequences for the trees being colonised by different ectomycorrhizal fungi, and (vi) toassess the importance of a high biodiversity Whether ectomycorrhizas can contribute sig- of ectomycorrhizas compared to a low bio- nificantly to the resistance of forest trees diversity. Acidifying pollutants remain a prob- against acidifying pollutants or whether they lem in many countries, despite international suffer in a similar manner to tree roots cannot attempts to control pollutants such as S diox- be finally concluded. In ectomycorrhizas, the ides and N oxides within the programs of the binding of N, metals and radionuclides to UN/ECE Convention on Long-Range Trans- polyphosphates in the vacuoles of fungal hy- boundary Air Pollution. It is evident that in fu- phae represents a detoxifying mechanism ture calculations of critical loads (N, acidity, which plant tissues alone do not have. Thus, heavy metals) as the scientific rationale for one of the advantages of the ectomycorrhizal the development of an effects-based new symbiosis could be in improving the tolerance protocol on the further reduction of emissions of the trees to acidifying pollutants (compare in the ECE countries, ecological processes also Leyval et al. 1997). On the one hand, ec- below ground – including ectomycorrhizas – tomycorrhizal systems have evolved to over- must receive the attention they deserve.
come low nutrient availability by producingvast external mycelia exploiting the soil andby evolving mechanisms to store and accu-mulate elements. At low deposition of acidify- ing pollutants, binding of, for instance, smallamounts of heavy metals to polyphosphates I am most grateful to P. Blaser and B. Frey for might not disturb the nutrient supply to the stimulating collaboration and for critical reading of host; indeed, in the case of physiologically the manuscript, to the whole soil ecology group, essential metals, it might even be useful. On C. Scheidegger and T. Riesen (PSI-Villigen) for the other hand, if deposition of pollutants is collaboration, and to M. Sieber for correcting the high, binding to the polyphosphates means a English text.
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Received 23 April 2001 New Phytologist, 119, 405–411.
Revised version accepted 10 June 2001

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