Download symbiotic mediators of rhizosphere and ecosystem processes

MYCORRHIZAS: SYMBIOTIC MEDIATORS OF RHIZOSPHERE AND ECOSYSTEM PROCESSES
Nancy Collins Johnson, Catherine A. Gehring
I. Introduction
Roots of most terrestrial plants form symbiotic associations with fungi. These ubiquitous
symbioses, called mycorrhizas, function as conduits for the flow of energy and matter
between plants and soils. Most plants have evolved to be highly dependent upon mycorrhizal
associations for acquiring resources from the soil. Mycotrophy, the degree to which plants
“feed” through mycorrhizas, is generally determined by the balance between carbon costs and
nutrient benefits of the association. To a large extent, mycorrhizal roles in structuring biotic
communities and mediating fluxes of matter and energy are manifestations of the net costs
and benefits of individual pairs of plants and mycorrhizal fungi.
Mycorrhizas challenge our traditional view of the rhizosphere. Mycorrhizal fungi
frequently stimulate plants to reduce root biomass while simultaneously expanding nutrient
uptake capacity by extending far beyond root surfaces and proliferating in soil pores that are
too small for root hairs to enter. Mycelial networks of mycorrhizal fungi frequently comprise
the largest portion of soil microbial biomass (Finlay and Söderström 1992; Olsson et al. 1999;
Högberg and Högberg 2002). Mycorrhizas physically and chemically structure the
rhizosphere, and they impact communities and ecosystems because their mycelial networks
often connect plant root systems over broad areas. Excellent reviews of mycorrhizal biology
(Smith and Read 1997; Varma and Hock 1998) physiology (Kapulnik and Douds 2000),
evolution (Brundrett 2002; Sanders 2002), and ecology (van der Heijden and Sanders 2002;
Read and Perez-Moreno 2003; Allen 1992) are available. The purpose of this chapter is to
examine how mycorrhizal interactions mediate rhizosphere processes at individual,
community, and ecosystem scales and explore responses of these interactions to
anthropogenic environmental changes.
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II. Background
A. Evolution of Mycorrhizal Symbioses
With few exceptions, plant roots have evolved to accommodate, utilize and control
mycorrhizal fungi. Both molecular and fossil evidence indicate that the earliest land plants
were mycorrhizal (Simon et al. 1993; Redecker et al. 2000). These bryophytic plants did not
possess true roots but rather stem-like rhizomes that were colonized with fungi that appear
similar to modern day arbuscular mycorrhizal (AM) fungi (Stubblefield et al. 1987;
Pirozynski and Dalpe 1989). Pirozynski and Malloch (1975) argue that plants could not have
colonized land without fungal partners capable of acquiring nutrients from the undeveloped
soils that existed during the Silurian and Devonian. Once terrestrial plants became established
and soil organic matter accrued, more mycorrhizal partnerships evolved as plant and fungal
taxa radiated into the newly forming terrestrial niches rich in organic matter. These disparate
symbioses have been grouped into six general types of mycorrhizas: arbuscular (also called
vesicular-arbuscular), ecto, ericoid, arbutoid, monotropoid and orchid (Table 1; Smith and
Read 1997).
Mycorrhizas are highly variable in structure, yet they have evolved two common
features: an elaborate interface between plant root and fungal cells, and extraradical hyphae
that extend into the soil. This chapter will focus primarily on arbuscular, ecto-, and to a
limited extent, ericoid mycorrhizas. However, a brief examination of the similarities and
differences of all six types of mycorrhizas reveal points of evolutionary convergence and
divergence of mycorrhizal symbioses.
B. Mycorrhizal Structure
Arbuscular mycorrhizas are widespread and abundant. They are formed by
bryophytes, pteridophytes, gymnosperms and angiosperms, and are ubiquitous in most
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temperate and tropical ecosystems including agricultural systems. The fungal partners in AM
associations are remarkably abundant, accounting for 5 to 50% of the microbial biomass in
agricultural soils (Olsson et al. 1999). These fungi are members of the Glomeromycota, a
monophyletic phylum containing 150 to 160 described species (Table 1). Arbuscular
mycorrhizas are sometimes called “endomycorrhizas” because the fungal partner forms
intraradical structures (i.e. inside plant roots). In AM associations, the interface between plant
and fungal tissues that facilitates exchange of materials between plant and fungal symbionts
takes the form of arbuscules (in classic Arum-type associations) or coils (in less well known
but potentially equally important Paris-type associations). Arbuscules and coils are modified
fungal hyphae that provide a large surface area for resource exchange. Several genera of AM
fungi also form intraradical vesicles that function as fungal storage organs. The extraradical
hyphae of AM fungi lack regular cross walls allowing materials, including nuclei, to flow
relatively freely within the mycelium. These hyphae can be very abundant, one gram of
grassland soil may contain as much as 100 m of AM hyphae (Miller et al. 1995). The
taxonomy of AM fungi is based upon the morphology of large (10-600 μm diameter) asexual
spores produced in the soil or within roots.
Ectomycorrhizas occur in certain families of woody gymnosperms (e.g. Pinaceae) and
angiosperms (e.g. Dipterocarpaceae, Betulaceae) and are extremely important in many
temperate and boreal forests. The fungal partners in ectomycorrhizal (EM) associations
account for an estimated 30% of the microbial biomass in forest soils (Högberg and Högberg
2002). These fungi are a diverse assemblage of at least 6,000 species of basidiomycetes,
ascomycetes, and zygomycetes (Table 1, Smith and Read 1997). This estimate of EM fungal
diversity is extremely conservative, and is likely to increase as more systems are examined
(Cairney 2000). Ectomycorrhizal basidiomycetes are obviously polyphyletic, many EM fungi
belong to large basidiomycete families like Amanitaceae, Boletaceae and Russulaceae
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(Brundrett 2002). Ascomycetes that form EM associations have four or more separate origins
(LoBuglio et al. 1996), and a few species of zygomycetes in the genus Endogone form EM
associations (Smith and Read 1997). The oldest fossils providing clear evidence of EM
associations date back 50 million years (Le Page et al. 1997), yet the association is
hypothesized to have evolved 130 million years ago (Smith and Read 1997). Molecular
evidence indicates that the EM habit has evolved repeatedly from saprotrophic ancestors and
that there have been multiple reversals back to a saprotrophic way of life (Hibbett et al. 2000).
Structurally, ectomycorrhizas are characterized by the presence of a fungal mantle that
envelops host roots and a Hartig net that surrounds root epidermal and/or cortical cells and
provides a large surface area for resource exchange. Hormonal interactions between plant and
fungus lead to dramatically altered root architecture including the suppression of root hairs.
The external component of EM associations consists of hyphae with cross walls that partition
cellular components. These hyphae sometimes coalesce into macroscopic structures called
rhizomorphs that attach the mycelium to sporocarps or can be morphologically similar to
xylem and serve in water uptake (Duddridge et al. 1980). The external mycelium of EM fungi
may be more extensive than that of AM fungi (Jones et al. 1998), with as much as 200 m of
hyphae per gram of dry soil (Read and Boyd 1986). Ectomycorrhizal fungi also are
frequently classified using the morphology of colonized roots and their sporocarps, such as
the familiar mushrooms and truffles.
The plant order Ericales contains a natural group of closely related families with
worldwide distribution. Plants in this order form three distinctive forms of mycorrhizas:
ericoid, arbutoid, and monotropoid (Table 1). Ericoid mycorrhizas involve partnerships
between ascomycetes and members of the Ericaceae, Epacridaceae, and Empetraceae families.
In the ericoid mycorrhizas, the epidermal cells of small diameter roots lack root hairs and
instead are frequently filled with fungal hyphae. Arbutoid mycorrhizas form between
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basidiomycetes and members of the Pyrolaceae and some genera of Ericaceae, most notably
Arbutus and Arctostaphylos. Structurally, arbutoid mycorrhizas are similar to
ectomycorrhizas as they possess a thick fungal mantle and a Hartig net, yet they are
characterized by the formation of dense hyphal complexes within root epidermal cells.
Monotropoid mycorrhizas are partnerships between certain non-photosynthetic members of
the Monotropaceae and basidiomycetes. In these associations, the fungus transfers
carbohydrates from a photosynthetic plant to its achlorophyllous (myco-heterotrophic) host
plant. In addition to a fungal mantle and Hartig net, these mycorrhizas are characterized by a
characteristic “peg” of fungal hyphae that proliferates within the epidermis of the root (Smith
and Read 1997).
Members of the Orchidaceae form a unique type of mycorrhizas with some
basidiomycetes (Table 1). Orchids differ from other plants because they pass through a
prolonged seedling (protocorm) stage during which they are unable to photosynthesize and are
dependent upon a fungal partner to supply exogenous carbohydrate (Smith and Read 1997).
Adult plants of most species of orchids are green and photosynthetic, but an estimated 200
species remain achlorophyllous throughout their life. These orchids are considered to be
“myco-heterotrophic” because they acquire fixed carbon heterotrophically through their
mycorrhizal fungal partner (Leake 1994). Orchid mycorrhizas are morphologically distinct as
well, consisting of intracellular hyphae that form a complex interface between plant and
fungal symbionts termed a peloton. Smith and Read (1997) and Leake (1994) question
whether or not these associations should be even considered mycorrhizas because there is no
demonstrated benefit of the association to the fungus.
Throughout their evolution, plant roots have repeatedly formed symbioses with fungi.
Except for orchid and monotropoid mycorrhizas, these associations involve plant exchange of
photosynthates in return for fungal exchange of mineral nutrients. The convergence of so
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many unrelated forms of mycorrhizas is a testament for the mutual benefits of these trading
partnerships.
III. Mycorrhizal Interactions
A. Individual-scale interactions
Interactions between individual plant-fungus pairs affect gene expression, resource
acquisition, biomass allocation and ultimately, the fitness and population dynamics of the
associated plant and fungal partners (Figure 1). Formation of mycorrhizas is accompanied by
the up- and down-regulation of both fungal and plant genes (Lapopin and Franken 2000).
Complex two-way communication occurs as fungal structures in the soil contact, recognize,
and integrate with root systems of host plants (Harrison 1999). For example, AM colonization
has been shown to cause Zea mays to up-regulate sucrose metabolism genes (Ravnskov et al.
2003) and Medicago trunculata to down-regulate phosphorus transporters (Liu et al. 1998).
In EM associations the hexose availability at the plant-fungus interface has been linked to
both plant and fungal gene expression (Hampp et al. 1999).
Resource exchange and biomass allocation
To understand the dynamics of resource exchange in mycorrhizas, we must examine
the mechanisms by which resources are acquired by both partners. Mycorrhizal fungi
improve nutrient uptake for plants, in part, by exploring the soil more efficiently than plant
roots. Mycorrhizal fungal hyphae occupy large volumes of soil, frequently extending beyond
the nutrient depletion zone that develops around roots. Simard et al. (2002) estimated that, on
average, the external hyphae of EM fungi produce a 60-fold increase in surface area. The
small diameter of fungal hyphae allows them to extract nutrients from soil pore spaces too
small for plant roots to exploit (Jongmans et al. 1997; Van Breemen et al. 2000). Recent
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studies on phosphate and ammonium uptake also reveal that mycorrhizal fungi improve
uptake kinetics through reductions in Km and increases in Vmax (van Tichelen and Colpaert
2000; Javelle et al. 1999).
Some of the previously described mechanisms by which mycorrhizal fungi improve
nutrient uptake are likely to be effective only for nutrients with poor mobility in the soil such
as phosphate and ammonium (Marschner 1996). However, mycorrhizal fungi can also access
nutrients from inorganic and organic sources that are generally completely unavailable to
plants directly (Dighton 1991). Ectomycorrhizal fungi increase the weathering of soil
minerals including iron (Watteau and Berthelin 1994), phosphorus (Wallander et al. 1997b;
Hagerberg et al. 2003) and calcium (Lapeyrie et al. 1990; Blum et al. 2002), apparently
through the secretion of organic acids into the rhizosphere (van Breemen et al. 2000).
Although AM fungi appear to have little ability to degrade complex organic molecules (Smith
and Read 1997), EM and ericoid mycorrhizas can derive nitrogen, phosphorus and sulfur
through the enzymatic breakdown of complex organic compounds (Read and Perez-Moreno
2003). The degradative abilities of EM fungi are generally inferior to those of saprotrophic
fungi (Bending and Read 1996, 1997; Colpaert and van Laere 1996); however, they can
provide an effective short-cut to the nitrogen cycle, potentially influencing the likelihood or
outcome of competitive interactions between plants and microbes (Abuzinadah et al. 1986).
Plant water balance is also impacted by mycorrhizas. Stomatal conductance and
drought tolerance of plants is frequently increased by the presence of mycorrhizal fungi (Augé
2000). These effects on plant water balance are often attributed solely to improved nutritional
status of mycorrhizal plants (e.g. Safir et al. 1972); however, there is evidence that
mycorrhizas also influence plant water balance through non-nutritional mechanisms including
hormonal changes and improved water holding capacity of rhizosphere soil (Augé 2001).
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Variation among mycorrhizal associations in resource acquisition is important to
rhizosphere dynamics. Both AM and EM fungi actively forage in the soil, yet Olsson et al.
(2002) proposed that AM fungi have evolved a foraging strategy that optimizes the search for
new potential root hosts while EM fungi optimize nutrient capture in competition with the
mycelia of other fungi. Species of both AM and EM fungi vary in the degree to which they
explore the soil with extraradical hyphae (Hart and Reader 2002; Erland and Taylor 2002).
Species of EM fungi have been shown to vary more than three-fold in their nutrient uptake
rates (Colpaert et al. 1999) suggesting large differences in their effects on both host plant
performance and rhizosphere nutrient cycling. Intraspecific variation can also be substantial
as different strains of the same mycorrhizal fungal species can vary more than different
species in aspects of nutrient uptake (Cairney 1999; Sylvia et al. 1993; Graham and Abbott
2000). Later we will discuss the importance of this variation for communities and
ecosystems.
Costs and benefits of mycorrhizas
Most mycorrhizal fungi depend heavily on plant photosynthate to meet their energy
requirements, AM fungi are considered obligate biotrophs though EM and ericoid fungi have
some saprotrophic abilities. The carbon cost of mycorrhizas is difficult to accurately estimate,
but field and laboratory studies suggest that plants allocate 10-20% of net primary production
to their fungal associates (Jakobsen and Rosendahl 1990; Smith and Read 1997). Root
colonization by mycorrhizal fungi often increase rates of host plant photosynthesis (e.g.
Nylund and Wallander 1989; Hammp et al. 1999; Lovelock et al. 1997). This effect has been
attributed to mycorrhizal enhancement of plant nutritional status in some systems (Black et al.
2000), and a greater assimilate sink in other systems (Dosskey et al. 1990; Miller et al. 2002;
Wright et al. 1998a)
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Mycorrhizal fungi are a significant carbon sink for their host plants and if nutrient
uptake benefits do not outweigh these carbon costs, then both plant and fungal growth can be
depressed (Nylund and Wallander 1989; Peng et al. 1993; Colpaert et al. 1996). Mycorrhizal
biomass has been shown to both increase and decrease with increasing availability of soil
nitrogen (Wallenda and Kottke 1998; Johnson et al. 2003a). Treseder and Allen (2002)
proposed a conceptual model to account for this apparent contradiction (Figure 2). The model
is based on three premises:
1. Both plants and mycorrhizal fungi have minimum N and P requirements and plants
have a higher total requirement for these nutrients than fungi.
2. Biomass of mycorrhizal fungi is limited by the availability of plant photosynthate.
3. Plants allocate less photosynthate belowground when they are not limited by nitrogen
and phosphorus; thus, mycorrhizal growth decreases when availability of these
nutrients is high.
At very low soil nitrogen and phosphorus availability, both plants and mycorrhizal fungi are
nutrient limited, so enrichment of these resources will increase mycorrhizal growth. At very
high nitrogen and phosphorus availability, neither plants nor fungi are limited by these
elements; consequently mycorrhizal biomass is reduced as plants allocate relatively less
photosynthate belowground and more aboveground to shoots. This model is useful because it
provides a simple heuristic framework for understanding how the relative availability of
belowground (minerals) and aboveground (photosynthate) resources control mycorrhizal
biomass. Considering the interplay between nitrogen and phosphorus availability may further
enhance the predictive value of this model. Because AM fungi generally acquire phosphorus
more readily than their host plants, we predict that the mutualistic value of AM associations
will be highest at low soil P:N ratios and diminish as P:N ratios increase. There is great
variability in abilities of EM fungi to acquire nitrogen and phosphorus from the organic soil
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horizon (Bending and Read 1995; Read and Perez-Moreno 2003); better understanding of the
distribution of this variability both geographically and phylogenetically will likely lead to
important ecological and evolutionary insights.
Two lines of evidence suggest that mycorrhizal plants have evolved mechanisms to
actively balance photosynthate costs with mineral nutrient benefits. First, environmental
factors that reduce photosynthetic rates, such as low light intensity, lead to reductions in
mycorrhizal development (e.g. Tester et al. 1986; Whitbeck 2001; Gehring 2003). Second,
plant allocation to root structures is sensitive to mycorrhizal benefits. This is observed at both
a gross taxonomic level as well as within ecotypes of the same plant species. Plant taxa with
coarse root systems (low surface area) are generally more dependent upon mycorrhizas than
those with fibrous root systems (high surface area; Baylis 1975). This suggests that for highly
mycotrophic plant taxa, it is more adaptive to provision a fungal partner with photosynthates
than to maintain fibrous root systems (Hetrick 1991; Newsham et el. 1995). Also, it appears
that mycotrophic plants have evolved a certain degree of plasticity in their allocation to roots
in response to their mycorrhizal status. Mycorrhizal plants often have reduced root:shoot
ratios compared to non-mycorrhizal plants of the same species grown under identical
conditions (Mosse 1973; Colpaert et al. 1996).
There is evidence that local ecotypes of plants and mycorrhizal fungi co-adapt to each
other and to their local soil environment (Figure 3a). A comparison of Andropogon gerardii
ecotypes from phosphorus-rich and phosphorus-poor prairies show that each ecotype grew
best in the soil of its origin. Furthermore, the A. gerardii ecotype from the phosphorus-poor
soil was three times more responsive to mycorrhizal colonization and had a significantly
coarser root system than the ecotype from the phosphorus-rich soil (Schultz et al. 2001).
These results suggest that the genetic composition of plant populations evolve so that
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mycorrhizal costs are minimized and benefits are maximized within the local soil fertility
conditions.
Mycorrhizal effects on plant and fungal fitness
Arbuscular mycorrhizal plants commonly produce more seed with a higher viability
compared to non-mycorrhizal plants (Koide and Lu 1995). This enhanced reproductive
success is likely a function of improved mineral nutrition and disease resistance among AM
plants, although plant species vary considerably in this regard (Koide 2000). Also, species
and isolates of AM fungi may differ in their influence on plant reproduction (Streitwolf-Engel
et al. 1997).
Plants obviously influence the fitness of their fungal partners because mycorrhizal
fungi range from strongly (EM) to completely (AM) biotrophic. Although many greenhouse
studies suggest little specificity between AM fungi and their plant hosts, field studies indicate
that taxa of AM fungi produce more spores when they are associated with some species of
plants rather than others (e.g. Johnson et al. 1992; Bever et al. 1996; Eom et al. 2000). The
connection between spore production and fungal fitness is likely to be strong for the
Gigasporaceae, a family of AM fungi that reproduce primarily through spores (Biermann and
Linderman 1983; Klironomos and Hart 2002). However, the relationship between spore
production and fitness is not as clear for members of the Glomaceae family because these
fungi reproduce through both spores and hyphal spread (Biermann and Linderman 1983;
Klironomos and Hart 2002). Indeed, some molecular studies indicate that there is little
correspondence between populations of Glomaceae spores in the soil and their abundance
within plant roots (Clapp et al. 1995) while others show a close correspondence between the
species composition of spore populations and root inhabitants (Jansa et al. 2002). Among EM
associations there seems to be no relationship between the species composition of sporocarps
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and root inhabitants (Gardes and Bruns 1996; Horton and Bruns 2001). However,
environmental factors that affect the production of plant photosynthate, such as defoliation,
have been shown to significantly reduce sporocarp production by EM fungi (Last et al. 1979;
Kuikka et al. 2003), suggesting a fitness link. Differential reproductive success among plant
and fungal taxa generate community structure. This structure and its functional importance
will be discussed in the next sections.
B. Community-scale Interactions
Mycorrhizal interactions influence the species composition, diversity, and dynamics of
biotic communities (Figure 1). Assessing mycorrhizal roles in communities is challenging
because the ubiquity and abundance of these associations makes it difficult to remove them
from intact communities so that their function can be accurately measured. Nevertheless,
experiments using microcosms (e.g. Grime et al. 1987; Wilson and Hartnett 1997; van der
Heijden et al. 1998) selective fungicides (e.g. Hartnett and Wilson 1999), and theoretical and
empirical studies (e.g. Bever et al. 1997) indicate that mycorrhizal feedbacks are a significant
force in structuring plant communities.
Mycorrhizal feedbacks on plant community structure
A community model developed by Bever (1999, Bever et al. 1997) assumes that the
population growth rates of plants and mycorrhizal fungi are mutually interdependent and
identifies the potential for two very different community dynamics. Symmetrical delivery of
benefits between plants and fungi will generate a positive feedback, and asymmetrical
delivery of benefits will generate a negative feedback. Positive feedback strengthens the
mutualism between individual pairs of plants and fungi, yet decreases community diversity;
while negative feedback weakens the mutualism between individual plant-fungus pairs and
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maintains community diversity. Recent experiments indicate that both of these mechanisms
occur within natural communities, and that variation in the balance of mycorrhizal costs and
benefits may be extremely important in structuring plant communities. Klironomos (2002)
found that populations of mutualistic AM fungi were selected for in the rhizospheres of
individual plants grown in pots for two ten-week cycles. In contrast, when ten plant species
were each randomly paired with ten AM fungal isolates from the same grassland, the function
of the partnerships varied from strongly mutualistic to strongly parasitic (Klironomos 2003a).
These studies indicate that co-adaptation of plant-fungus pairs occurs at the centimeter scale
within individual plant rhizospheres, not at the hectare scale within grassland swards.
Furthermore, this work provides solid experimental support for the hypothesis that ecotypes
of plants and mycorrhizal fungi co-adapt to one another and to their local soil environment
(Figure 3a), and this process may be an important determinant of community structure.
Common mycelial networks
Extraradical hyphae from individual clones of mycorrhizal fungi frequently link the
root systems of neighboring plants of the same as well as different species. In this way, most
mycorrhizal plants are interconnected by a common mycorrhizal network (CMN) at some
point in their life (Newman 1988). Isotope labeling studies show that carbon and mineral
nutrients can be transferred among neighboring plants within this CMN; however the
magnitude and rate of this transfer appears to vary greatly between AM and EM systems as
well as among plant and fungal taxa (Simard et al. 2002). Although it is well established that
interplant transfer of carbon and nutrients occurs, there is debate over whether the amount of
material transferred is large enough to affect plant physiology and ecology and whether the
materials leave the fungal tissues in the roots and reenter the shoots of the receiver plant
(Simard et al. 2002). In this regard, EM and AM associations appear to differ. In a field
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study using dual 13C / 14C labeling, Simard et al. (1997) showed significant bi-directional
shoot to shoot carbon transfer between adjacent Pseudotsuga and Betula seedlings colonized
by a common EM fungus. In contrast, Fitter et al. (1998) found that although AM fungi
transferred a significant amount of carbon between the root systems of the grass Cynodon and
the forb Plantago, this carbon was never released into the receiving plant’s shoots. Thus,
Fitter et al. (1998) suggest that inter-plant movement of carbon via common AM mycelia is
less likely to impact plant fitness than AM fungal fitness. There is a great need for field based
research to test the claims that CMNs influence seedling survival, assist species recovery
following disturbance, influence plant diversity by altering the competitive balance of plant
species, reduce nutrient loss from ecosystems, and increase productivity and stability of
ecosystems. Simard et al. (2002) reviews studies that both support and contradict these claims.
Future research will help resolve the role of CMN’s in community and ecosystem processes.
Bacteria-mycorrhiza interactions
Effects of mycorrhizal fungi on the quantity and quality of root exudates (Linderman
1988; Garbaye 1991) may generate a cascade of effects on populations and communities of
rhizosphere bacteria. Recent data suggest that different combinations of plant-fungal pairs
will generate different effects on bacteria communities (Andrade et al. 1997; Söderberg et al.
2002). For example, Söderberg et al. (2002) observed that the outcome of AM colonization
by Glomus intraradices on bacterial communities varied among plant species. While some
studies suggest that mycorrhizal fungi and soil bacteria may compete for carbon in the
rhizosphere (e.g. Christensen and Jakobsen 1993), plant growth promotion by mycorrhizal
fungi may counteract this effect and actually stimulate rhizosphere bacterial activity
(Söderberg et al. 2002).
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Some bacteria, such as a number of fluorescent pseudomonads, are known to function
as mycorrhization helper bacteria (MHB) because of their ability to consistently enhance
mycorrhizal development (reviewed by Garbaye 1994). Rates of ectomycorrhiza formation
on Eucalyptus diversicolor in plant nurseries were increased up to 300% by MHBs (Dunstan
et al. 1998), leading to significant increases in seedling biomass. The mechanisms for these
effects are poorly understood, but the release of volatile compounds by MHBs has been
shown to stimulate fungal growth (Garbaye and Duponnois 1993). Available data suggest
that these interactions are extremely complex. A strain of Pseudomonas monteilii enhanced
mycorrhization by one species of AM fungus and several species of EM fungi in Acacia
holosericea (Duponnois and Plenchette 2003). In contrast, MHBs isolated from the
Pseudotsuga menziesi-Laccaria laccata symbiosis were fungus-specific, but not plant
specific. These bacteria promoted EM establishment of the fungus, Laccaria laccata, but
inhibited the formation of ectomycorrhizas by other species of fungi (Garbaye and Duponnois
1993).
Fungal-mycorrhiza interactions
Mycorrhizal fungi co-inhabit the rhizosphere with many saprotrophic and pathogenic
fungi. Interactions with saprotrophic fungi may be more likely for the EM and ericoid fungi
that have significant abilities to degrade organic matter. Based on a trenching study, Gadgil
and Gadgil (1971; 1975) suggested that EM fungi might reduce decomposition rates by
competing with saprotrophic fungi for limited nutrients. Microcosms studies in which
saprotrophic and mycorrhizal mycelial systems are allowed to interact provide evidence for
significant retardation of the growth of saprotrophic fungi by EM fungi and vice versa (e.g.
Leake et al. 2002). Ectomycorrhizal fungi may outcompete saprotrophic fungi for rhizosphere
territory (Lindahl et al. 2001), release organic acids into the rhizosphere that inhibit
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saprotrophs (Rasanayagam and Jeffries 1992), or indirectly reduce litter decomposition by
saprotrophs by extracting water from the soil (Koide and Wu 2003).
Fungal pathogens and mycorrhizal fungi also interact with one another. Many studies
demonstrate significant protection from pathogens by mycorrhizal fungi. In a meta-analysis
of studies of interactions among AM fungi and fungal pathogens, Borowicz (2001) showed
that plants generally grow better when they are mycorrhizal and this is especially true when
plants are challenged by pathogens. Fungal pathogens also generally reduce root colonization
by arbuscular mycorrhizal fungi (Borowicz 2001). Newsham et al. (1995) suggests that
pathogen suppression may be more important than other benefits of AM symbioses in natural
ecosystems. The mechanisms of pathogen suppression are highly varied and include
improved nutrition of the host plant, changes in the chemical composition of plant tissues, and
changes in rhizosphere bacteria communities (Strobel and Sinclair 1998; Linderman 2000;
Graham 2001).
Animal-mycorrhiza interactions
Interactions among soil animals and mycorrhizal fungi may potentially alter the
function of the symbiosis. Many studies of relationships among soil fauna and mycorrhizal
fungi focus on the impacts of fungus-feeding animals, such as collembola, on mycorrhizal
function. Hiol et al. (1994) found that grazing by the collembolan Proisotoma minuta
significantly reduced EM colonization and also that the collembolan had distinct preferences
for the hyphae of certain species of EM fungi. Several studies suggest that hyphal grazers
prefer to feed on saprotrophic or parasitic fungi over mycorrhizal fungi and thus may have
limited impact on the symbiosis (e.g. Hiol et al. 1994; Klironomos and Ursic 1998;
Klironomos et al. 1999). Even when hyphal grazing results in substantial reductions in
mycorrhizal fungal hyphae, the mutualism may not be negatively affected (Setälä 1995;
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Larsen and Jakobsen 1996). For example, Setälä 1995 found that although soil fauna reduced
EM fungal biomass by as much as 50%, the growth of both birch and pine seedlings was 1.5
to 1.7 fold greater in the microcosms with soil fauna compared to those without.
Non-intuitive outcomes of interactions between soil fauna and mycorrhizal fungi
reveals how little is known about the natural history of most soil organisms. Klironomos and
Hart (2001) showed that the EM fungus Laccaria laccata actively kills and consumes the
collembolan Folsomia candida and the host plant benefited from this unconventional foraging
behavior of its EM fungus. Stable isotope labeling showed that up to 25% of the nitrogen
found in Pinus stroba seedlings colonized by L. laccata was of collembolan origin.
Mycorrhizal fungi also affect the growth of plant pathogenic nematodes and generally reduce
the detrimental effects that these animals have on plant growth. Borowicz (2001) found that
AM fungi significantly impact nematode growth and that this effect varies with the type of
nematode. Sedentary nematodes are negatively affected by AM fungi while migratory species
actually grow better in their presence.
The studies that we have reviewed here were selected to demonstrate that complex
interactions among communities of mycorrhizal fungi and other soil organisms can mediate
rhizosphere processes. Yet these studies represent only a small sample of the myriad of
interactions among mycorrhizal fungi and other rhizosphere organisms. For example, we did
not discuss the role of animals such as earthworms in dispersing fungal propagules or the
indirect effects of root herbivores on mycorrhizal fungi (Gange and Brown 2002). Likewise,
we have limited our discussion to belowground interactions despite increasing evidence that
mycorrhizal symbioses are influenced by aboveground organisms such as herbivores, sporedispersing vertebrates and leaf fungal endophytes (e.g. Vicari et al. 2002; Gehring and
Whitham 2002; Gehring et al. 2002).
17
C. Ecosystem-scale Interactions
Mycorrhizas physically, chemically, and biologically modify the soil environment.
The term “mycorrhizosphere” was coined to describe the unique properties of the rhizosphere
surrounding and influenced by mycorrhizas (Oswald and Ferchau 1968; Rambelli 1973;
Linderman 1988). Figure 4 illustrates EM pine seedlings to highlight some of the unique
properties of the mycorrhizosphere. In this section, we discuss the importance of
mycorrhizosphere processes for soil structure, nutrient cycling and the global distribution of
biomes (Figure 1).
Soil structure
One of the most important functions of mycorrhizas is their role in physically
structuring soils. This is significant because soil structure mediates fertility, water content,
root penetration and erosion potential of soils. Mycorrhizas generate stable soil aggregates.
Miller and Jastrow (2000) suggested that mycorrhizas physically and chemically bind soil
particles into stable macroaggregates like “sticky string bags” of mycorrhizal hyphae and
associated roots. Furthermore, in many but not all soil types, mycorrhizal hyphae are
involved with the hierarchical arrangement of macro- and microaggregates within the soil
matrix. The contributions of mycorrhizas to soil structure vary with soil types and the
phenotypes of plants and mycorrhizal fungi. For example, AM fungi generally play a greater
role in aggregate formation in sandy soil than in clayey soil (Degens et al. 1996; Miller and
Jastrow 2000). Although both saprotrophic and mycorrhizal fungi facilitate the formation of
soil aggregates, mycorrhizal fungi stabilize soil much more effectively than saprotrophic fungi
(Tisdall and Oades 1980). Miller and Jastrow (2000) propose three reasons for this: 1)
mycorrhizal fungi have direct access to plant photosynthate and consequently they are less
carbon limited than saprotrophic fungi, 2) hyphae of mycorrhizal fungi are often more
18
persistent than hyphae of saprotrophic fungi, and 3) hyphae of ericoid, EM and AM fungi
exude sticky glycoproteinaceous slimes that facilitate the binding of particles within the
mycorrhizal “string bags.” Glomalin is a glycoprotein that has been linked with stability of
soil aggregates (Wright and Upadhyaya 1998). Wright et al. (1996) used a monoclonal
antibody to detect glomalin on the surfaces of actively growing hyphae from representatives
of five different genera of AM fungi and also, to a lesser extent, on the hyphae of some nonAM fungi. Further studies are needed to thoroughly characterize this apparently important
soil binding agent.
Decomposition and nutrient cycling
The total effect of roots and associated mycorrhizal fungi on soil structure is related to
their turn-over and decomposition rates. Fungal hyphae contain high amounts of chitin, a
compound known to be resistant to decomposition. Although it is not yet well characterized,
glomalin also appears to be remarkably recalcitrant. Rillig et al. (2001a) used radiocarbon
dating to estimate a residence time of 6 to 42 years! Hungate and Langley concluded that
mycorrhizas can be important controllers of root decomposition rates and also that the tissues
and exudates formed in EM associations are more recalcitrant than those formed in AM
associations (Langley and Hungate 2003). The species of mycorrhizal fungi is an important
consideration. Wallander and colleagues found that five morphotypes of EM fungi on Pinus
sylvestris varied more than twofold in chitin concentration (Wallander et al. 1999).
Earlier sections of this chapter describe the important role that mycorrhizal fungi play
in nutrient uptake by plants and in the decomposition of organic matter. The chemical and
physical changes they induce in the rhizosphere, their interactions with other organisms in the
root zone and beyond, and their intimate linkage with host plants suggest that mycorrhizal
fungi could influence nutrient cycling by a number of mechanisms. Perhaps the most
19
important point to consider is the variation among types of mycorrhizal fungi in the ability to
utilize organic sources of nitrogen and thus provide host plants with a short-cut of the nitrogen
cycle. It is also possible that digestion of soil animals by mycorrhizal fungi as observed by
Klironomos and Hart (2001) is widespread, providing an additional means by which
mycorrhizal fungi acquire resources independently of microbial decomposers.
Traditional models of nutrient cycling consider soil microbes as carbon-limited
decomposers that provide plants with inorganic nutrients in the soil. While these models may
apply well to AM dominated ecosystems, they likely misrepresent key aspects of nutrient
cycling in ecosystems dominated by ericoid and EM mycorrhizas. Several authors have
argued for a different view of nutrient cycling that better incorporates interactions among soil
microbes including mycorrhizal fungi. Abuzinadah et al. (1986) and Lindahl et al. (2002)
suggest that mineralization and the inorganic nutrients that result from it are relatively
unimportant to nutrient cycling in many coniferous forests. Instead, organic sources of
nutrients predominate in these ecosystems and plant access to these nutrients depends upon
the outcome of interactions between decomposers and EM fungi. In this view, EM and
ericoid mycorrhizal fungi acquire some nutrients from the soil directly, but also capture
organic nutrients from plant litter and perhaps more importantly, from other soil biota
including mycorrhizal and saprotrophic fungi, bacteria, protozoa, and soil microfauna.
Furthermore, EM fungi can sequester large quantities of nitrogen in their external mycelia.
These nitrogen stores can be mobilized and utilized by host plants when nitrogen demands are
high, for example during bud break in the spring (Wallander et al. 1997a).
Global patterns of mycorrhizas
Aerts et al. (2002) suggested that variation in access to different nutrient pools among
types of mycorrhizal fungi leads to positive feedbacks between the dominant plants in an
20
ecosystem, litter chemistry, and litter decomposition. These feedbacks, combined with abiotic
environmental constraints, can shape ecosystems at broad spatial scales including the global
distribution of biomes. Distinctive types of mycorrhizas correspond with the climatic and
edaphic conditions that characterize the major terrestrial biomes (Read 1991). Ericoid
mycorrhizas are most common at the highest latitudes and altitudes, EM associations
dominate boreal forests and temperate coniferous forests, and AM associations are abundant
in low latitude biomes (Figure 5). This pattern relates to soil fertility constraints imposed by
pedogenic processes (Read 1991). Cold and wet conditions at high latitudes and altitudes slow
decomposition. Organic matter accumulates in these regions and nitrogen and phosphorus is
largely contained within organic compounds (e.g. chitin, proteins, amino acids) and soil
humus. Consequently, it is extremely adaptive for EM and ericoid mycorrhizas within tundra
and boreal biomes to be capable of assimilating nitrogen and phosphorus from organic
sources. As latitude decreases, mean annual temperature increases along with decomposition,
mineralization, and soil pH. These changes influence resource availability and also enzymatic
activity. Read (1991) considered the pH optima of the enzymes utilized by EM fungi and
suggested that the progressive replacement of EM by AM associations as soil pH increases
above 5 reflects the loss of the selective advantage conferred by EM mobilization of organic
nutrients. The efficiency of AM fungi in acquiring inorganic phosphorus corresponds with the
general pattern for increasing phosphorus limitation with decreasing latitude (Read 1991;
Read and Perez-Moreno 2003; Figure 5).
IV. Changes in Mycorrhizal Function in a Changing World
It is well recognized that humans are changing global environments at an
unprecedented rate (Vitousek 1994). These changes are known to impact global climate and
biota, however, the ramifications for communities and ecosystems are not known (IPCC,
21
2001; Weltzin et al. 2003). Understanding mycorrhizal responses to anthropogenic
environmental changes can help predict the characteristics of future communities and
ecosystems. In this context, we will briefly consider mycorrhizal responses to changes in
resource availability, climate, and biodiversity. More detailed rhizosphere responses are
considered in chapter 10 (Pregitzer).
A. Resource Enrichment
Human activities have more than doubled annual inputs of nitrogen into the biosphere
(Vitousek et al. 1997) and increased atmospheric carbon dioxide concentrations by 31% since
1750 (IPCC, 2001). Mycorrhizal responses to nitrogen and carbon dioxide enrichment have
been reviewed (e.g. Fitter et al. 2000; Rillig et al. 2002; Staddon and Fitter 1998; Wallenda
and Kottke 1998; Cairney and Meharg 1999). Here we will summarize these responses and
consider their mechanisms. Enrichment of soil nitrogen and atmospheric carbon dioxide can
be expected to alter the balance of trade between mycorrhizal fungi and their plant hosts.
When phosphorus, water, and other soil resources are not in limiting supply, then nitrogen
enrichment is predicted to reduce mycorrhizal biomass as host plants decrease carbon
allocation to roots and fungal partners (Figure 2b). Using the same conceptual model, we can
expect that carbon dioxide enrichment should increase mycorrhizal biomass because plant
demands for nitrogen and phosphorus will increase concurrently with carbon assimilation
rates and plants will allocate more photosynthate belowground to roots and mycorrhizal fungi
to help satisfy the increased demand for nitrogen and phosphorus (Figure 2c). A serious
limitation of these conceptual models is that they are inherently phytocentric because they
assume that plant allocation of photosynthate is the sole controller of mycorrhizal
development. An alternative more mycocentric view has been proposed by Wallander (1995)
in which the fungus, rather that the plant, adjusts allocation patterns in response to resource
22
availability. Studies are clearly needed to assess the relative importance of plant and fungal
control of mycorrhizal growth and development. Biological market models that incorporate
the resource requirements and acquisition of both trading partners (e.g. Hoeksema and
Schwartz 2003) may help direct these future research efforts.
Nitrogen enrichment
Many studies support the prediction that nitrogen enrichment should decrease
mycorrhizal biomass (Figure 2b); however, there is considerable variability in this response.
The biomass of reproductive structures and extraradical mycelia of mycorrhizal fungi are
more consistently reduced by nitrogen enrichment than is intraradical colonization. Results of
long-term field studies show that nitrogen enrichment dramatically affect sporocarp
production by EM fungi (Arnolds 1991; Wallenda and Kottke 1998) and spore production by
AM fungi (Egerton-Warburton and Allen 2000; Egerton-Warburton et al. 2001). Long term
nitrogen enrichment of a spruce forest in Sweden reduced the growth of EM mycelia by 50%
(Nilsson and Wallander 2003). Similarly, long term nitrogen enrichment consistently reduced
AM hyphal lengths in North American grasslands with sufficient soil phosphorus (Johnson et
al. 2003a). Formation of EM root tips and intraradical AM colonization have been shown to
decrease, increase, or stay the same in response to nitrogen enrichment (Wallenda and Kottke
1998; Johnson et al. 2003a). This variability suggests that plant phenotypes, fungal
phenotypes, and edaphic conditions mediate mycorrhizal responses to nitrogen enrichment
and cautions against extrapolating the results from one system to other systems.
Some species of mycorrhizal fungi decline with nitrogen enrichment while others
proliferate (e.g. Egerton-Warburton and Allen 2000; Lilleskov et al. 2001; Avis et al. 2003).
Wallenda and Kottke (1998) reviewed the literature and concluded that EM fungal species
with a narrow host range (particularly conifer specialists) are more adversely affected than
23
species with a broad range of host plants. When soil phosphorus is not limiting, members of
the AM fungal family Gigasporaceae are often dramatically reduced by nitrogen enrichment
(Egerton-Warburton and Allen 2000; Egerton-Warburton et al. 2001; Johnson et al. 2003a).
In contrast, when soil phosphorus is in limiting supply, nitrogen enrichment increases
populations of Gigasporaceae (Eom et al. 1999; Johnson et al. 2003a). This suggests that
nitrogen enrichment of phosphorus deficient soils exacerbates phosphorus limitation and
increases the net benefits of mycorrhizas. Gigasporaceae populations seem particularly
sensitive to plant responses to changes in soil P:N ratios.
Carbon dioxide enrichment
The conceptual model presented in Figure 2c predicts that elevated atmospheric
carbon dioxide should increase mycorrhizal biomass as carbon becomes relatively less
limiting and soil nutrients become relatively more limiting to plant growth. Some studies
support this model, while others do not. For example, elevated carbon dioxide has been shown
to increase EM colonization of root tips (Godbold et al. 1997; Tingey et al. 1997), and
extraradical hyphal lengths of both AM and EM fungi (Rillig et al. 1999; 2001b; Treseder and
Allen 2000). In contrast, other studies have found no effects of carbon dioxide on EM (Walker
et al. 1997) and AM root colonization or hyphal production when plant size is factored out
(Staddon et al. 1999; Wolf 2001). As with mycorrhizal responses to nitrogen enrichment, it is
likely that these apparent contradictions arise from differences among the experimental
systems, and in particular, differences in the taxa of interacting plants and fungi.
The species composition of EM fungi in a spruce forest in northern Sweden responded
dramatically to carbon dioxide enrichment (Fransson et al. 2001). Similarly, AM fungal
communities have been shown to change in response to carbon dioxide enrichment
(Klironomos et al. 1998; Wolf et al. 2003). Klironomos (2003b) exposed plants and soil from
24
fourteen sites across North America to elevated and ambient levels of atmospheric carbon
dioxide. Fewer AM fungal taxa were detected at elevated than at ambient carbon dioxide and
Gigasporaceae populations were most often reduced by carbon dioxide enrichment.
Additional studies showed that these changes in AM fungal communities corresponded with
reduced beneficial effects of mycorrhizal fungi on plant growth. From this result we might
conclude that carbon dioxide enrichment will reduce the mutualistic properties of AM fungal
communities. However, Klironomos (2003b) added an ingenious evolutionary treatment to
this experiment that clearly shows that this conclusion is incorrect. Klironomos increased
atmospheric carbon dioxide concentrations from 350 PPM to 550 PPM either suddenly in one
step (as described above), or gradually over 21 generations. When carbon dioxide was
enriched gradually, allowing the plants and associated AM fungi to be preconditioned to
gradually increasing carbon dioxide levels, then the mutualistic properties of AM fungal
communities from the 550 PPM treatment were not different from those of the 350 PPM
treatment. Gradually increasing carbon dioxide levels is obviously a more realistic treatment
than a step increase; thus, results from the gradual treatment are likely to provide a more
accurate prediction of AM responses to carbon dioxide enrichment. Although evolution is
rarely incorporated into experimental designs, this study provides sobering evidence that
evolutionary responses must be considered to accurately predict biotic responses to
anthropogenic environmental changes.
B. Ozone depletion and climate change
Release of chlorofluorocarbons into the atmosphere is known to deplete stratospheric
ozone and increase UV-B radiation. As with atmospheric carbon dioxide enrichment, the
effects of increased UV-B radiation on mycorrhizal fungi are likely to be mediated through
plant responses. Increased UV-B radiation has been shown to change plant morphology and
25
biochemistry including increased production of secondary metabolites such as flavonoids that
can absorb excess UV-B radiation (van de Staaij et al. 2001). These changes in plant hosts
may alter their relationships with mycorrhizal fungi and other soil biota. Only a few studies
have explored these relationships. Three studies involving AM fungi observed that increased
UV-B radiation altered levels of total or arbuscular root colonization (Klironomos and Allen
1995; van de Staaij et al. 2001; Zaller et al. 2002), while two studies involving EM fungi
observed no significant response (Newsham et al. 1999; De la Rosa et al. 2003).
Average global temperature has risen over the past 25 years, and the
Intergovernmental Panel on Climate Change predicts land surface temperature will increase
3.1 C by 2085 (IPCC 2001). Likely changes in average precipitation vary throughout the
world, yet the probability of extreme precipitation events is expected to rise. For example,
drought frequency and severity is expected to increase over most mid-continental land
interiors in the coming decades (IPCC 2001). Effects of altered temperature and precipitation
regimes on mycorrhizas are difficult to predict for two reasons. First, these changes will
influence both above- and below-ground environments and thereby have the potential to both
directly and indirectly impact mycorrhizas (Rillig et al. 2002). Second, temperature and
precipitation changes are frequently linked to one another so that more realistic scenarios of
global change must include both factors along with the importance of altered temporal
patterns such as changes in growing season length or the timing of precipitation.
Rillig et al. (2002) concluded that temperature increases in the ranges predicted by
climate models may promote mycorrhizal fungi directly through temperature dependent
increases in fungal metabolism and indirectly through increases in plant growth and nutrient
mineralization in the soil. These changes were expected to be most dramatic in regions near
the poles where potential increases in nutrient mineralization could favor AM fungi in areas
formerly dominated by ericoid or EM associations. When combined with the changes
26
predicted for nitrogen enrichment, these patterns further suggest a world of increasing AM
dominance as human impacts increase.
More variable precipitation regimes are also likely to affect mycorrhizal fungi. Root
colonization by both AM and EM fungi can respond significantly to soil moisture content
(e.g. Allen 1983; Swaty et al. 1998) and the relationship may be nonlinear (Mullen and
Schmidt 1993) and variable depending upon the taxa of plants and fungi involved (e.g. Lodge
1989). Mycorrhizal fungi have been shown to affect plant water relations and drought
tolerance in a number of AM and EM hosts (e.g. Auge 2001; Boyle and Hellenbrand 1991).
Species and even isolates of mycorrhizal fungi vary in their ability to tolerate dry conditions
and to assist their hosts in doing so (Stahl and Smith 1984; Hetrick et al. 1986; Lamhamedi et
al. 1992; Dixon and Hiol-Hiol 1992). Simulated drought stress of beech (Fagus sylvaticus)
resulted in significant shifts in EM community composition and increases in the production of
sugar alcohols that are thought to play a role in compensation for drought stress (Shi et al.
2002). Querejeta et al. (2002) demonstrated that host plants may sustain mycorrhizal fungal
hyphae during times of drought through hydraulic lift of moisture from deeper soil layers
occupied by roots but not fungal hyphae. Maintenance of a functional mycorrhizal mycelium
will not only provide benefits to the host plant and fungus but also to a variety of other
rhizosphere organisms.
The drought tolerance of certain taxa of plants and fungi will be exceeded as climates
continue to change. Plants are expected to be less tolerant of water stress than fungi because
fungi can access smaller soil pore spaces and survive remarkably low water potentials. Some
fungi are among the most xerotolerant organisms known (Kendrick 2000), though the drought
tolerance of mycorrhizal fungi has not been broadly tested. Because of their dependence on
host plant carbon, when drought is extreme mycorrhizal fungi may share the same fate as their
host plants regardless of their individual drought tolerance. For example, recent droughts in
27
southwestern North America have resulted in substantial mortality of pinyon pines (Pinus
edulis). Surviving pinyons in high mortality areas supported a less abundant, less diverse and
compositionally different EM community than neighboring pinyons growing in nearby low
mortality sites on similar soils (Swaty et al. 2004). Furthermore, survival rates of pinyon
seedlings were 50% lower in high mortality sites that were depauperate in EM fungi
compared to sites with high populations of EM fungi. Because pinyons are the only hosts for
EM fungi in many of these habitats, their loss from the system may also mean loss of EM
fungi from large tracts of woodland. Interestingly, AM fungi predominate in most waterlimited desert environments (Allen 1991). Here again, predicted environmental changes
appear to favor AM fungi over EM fungi.
Increasingly, studies of relationships between mycorrhizal fungi and global change are
focusing on interactions among multiple factors rather that single factors (Rillig et al. 2002).
This is an important advance because few environments will experience only one change, and
interactions among multiple factors may generate complex outcomes. For example, carbon
dioxide enrichment is occurring at a global scale while nitrogen enrichment and drought are
more localized. Also, increased carbon dioxide availability may reduce the consequences of
drought, but it could amplify the effects of nitrogen enrichment on plant productivity,
potentially at the expense of mycorrhizal fungi. Recent mesocosm experiments indicate that
anthropogenic enrichment of carbon dioxide and nitrogen will have interactive effects on
mycorrhizal symbioses and community structure (Johnson et al. 2003b). Anthropogenic loss
of biodiversity and the introduction of exotic species will likely further complicate these
responses.
C. Biodiversity changes
28
There is growing concern about the consequences of the recent loss of global
biodiversity caused by human activities. Conventional high-input agriculture is an extreme
case of anthropogenic reduction of biodiversity. As human population increases, vast areas of
diverse natural communities have been replaced with crops, orchards, and plantation forests
consisting of genetically uniform cultivars. These changes clearly impact mycorrhizas and
other rhizosphere organisms. When compared to adjacent natural areas, communities of AM
fungi in cultivated fields are generally less diverse and dominated by a few agriculturetolerant taxa (Johnson and Pfleger 1992; Helgason et al. 1998). If agriculture-tolerant taxa of
mycorrhizal fungi are effective mutualists, then the changes in fungal communities that
accompany cultivation may benefit crop production. Unfortunately, there is no theoretical or
empirical evidence to support this scenario (Ryan and Graham 2002). Rather, there is
evidence supporting the hypothesis that many modern agricultural practices may inadvertently
generate less mutualistic communities of AM fungi (Johnson et al. 1992; Scullion et al. 1998;
Kahiluoto et al. 2000). For example, high levels of mineral fertilizer cause plants to reduce
allocation to roots and mycorrhizas. Because AM fungi are obligate biotrophs, reduced
availability of host carbon is a very strong selection pressure, and fungal phenotypes that best
commandeer plant carbon will have a strong advantage over less aggressive phenotypes. This
aggressive acquisition of host carbon is clearly adaptive for fungi living in high fertility soils,
however it also predisposes them to be less mutualistic, or even parasitic on their host plants
(Johnson 1993; Kiers et al. 2002).
Communities of plants and rhizosphere organisms are continually adapting to one
another in undisturbed ecosystems (Figure 3a). In contrast, the plant phenotypes that occur in
production agriculture are selected by the farmer, not by their ability to maximize the benefits
and minimize the costs of their rhizosphere symbioses (Figure 3b). Crop breeding programs
may exacerbate the proliferation of inferior mycorrhizal mutualists by selecting cultivars that
29
perform best with high fertilizer inputs, and consequently, with low levels of mycorrhizal
colonization. Older land races of crops are consistently more mycotrophic than modern
cultivars (Manske 1990; Hetrick et al. 1993). Efforts to incorporate mycorrhizas into more
sustainable agricultural programs need to recognize the mycotrophic properties of the crops as
well as the mutualistic properties of the fungi.
Complementary to our concern over global loss of species diversity is the growing
threat of exotic species that can significantly alter community and ecosystem processes.
Mycorrhizal fungi may indirectly enhance the success of exotic plant invaders (e.g. Marler et
al. 1999), but our understanding of the potential effects of mycorrhizal fungi as exotic species
is particularly rudimentary owing to our poor knowledge of the diversity and species
composition of mycorrhizal fungal community in any ecosystem. Recent studies indicate that
even the apparently species-poor AM fungi have substantially higher species richness and
genetic diversity than previous work suggested (Bever et al. 2001; Husband et al. 2002;
Sanders 2003). The more diverse EM fungi pose an even greater challenge as species
accumulation curves rarely show an asymptote at the sampling intensities used (Taylor 2002).
This poor knowledge of mycorrhizal fungal species composition and diversity makes it
difficult to know if a species is introduced or native, and thus to assess the role of exotic
mycorrhizal fungi in community and ecosystem processes.
One recent example concerning the introduction of an exotic pine and associated EM
fungi illustrates the potential importance of fungal species diversity and/or species
composition to ecosystem processes (Chapela et al 2001). The establishment of pine
plantations in many parts of the world requires the concomitant introduction of compatible
EM fungi. These alien plant-fungal combinations are introduced to novel environments
where they can inadvertently alter community and ecosystem processes. In this example, a
species-poor community of three EM fungi associated with one host tree, Monterey pine
30
(Pinus radiata), was introduced into a formerly AM-dominated grassland in Ecuador. It
should be stressed that the three introduced fungi comprise only a small component of the
approximately one hundred EM fungi that occur in native Monterey pine forests. In less than
twenty years, this introduced EM-pine system has had dramatic effects on grassland habitats,
removing up to 30% of stored soil carbon (Chapela et al. 2001). Stable isotope analysis was
used to link this carbon loss to the saprotrophic growth of Suillus luteus, an EM species whose
sporocarp production was three-fold greater than that of all EM species combined in native
pine forests (Chapela et al. 2001). Introduction of this plant-fungus combination altered
rhizosphere carbon pools and thus the carbon cycle in dramatic and unpredicted ways. While
we might be tempted to think that, as mutualists, exotic mycorrhizal fungi may not have the
dramatic negative impacts of introduced fungal pathogens, some types of mycorrhizal fungi
have flexibility in their trophic capabilities and under the right environmental conditions many
of them have the potential to act as parasites.
V. Directions for Future Research
To date, most studies of mycorrhizal mediation of rhizosphere processes have
examined individual plant-fungus pairs or interactions among individual mycorrhizas and
other rhizosphere biota or abiotic conditions. Although this scale of inquiry provides precise
understanding of specific plant-fungal systems, it can not provide meaningful information
about mycorrhizal function within communities and ecosystems (Read and Perez-Moreno
2003). Furthermore, these studies generally apply a plant-centric focus, yet incorporation of a
fungus-centric view is necessary to predict the long-term function of these interactions
because mycorrhizal fungi are continually evolving to maximize their own fitness rather than
the benefits that they convey to their host plants. The analytical challenge of holistic studies of
complex interactions among rhizosphere organisms and the environment is daunting.
31
Nevertheless, meeting this challenge is particularly important as we seek to manage
mycorrhizas in forestry, agriculture, and in the restoration of highly disturbed areas where
these complex interactions may be altered to the detriment of rhizosphere function.
In the spirit of G. Evelyn Hutchinson's “evolutionary play in an ecological theater,”
mycorrhizas are an evolutionary play performed in the rhizosphere theater by a cast of
myriads of plant and fungal ecotypes (Figure 3a). By cultivating plant ecotypes that have
been selected in the absence of endemic mycorrhizal fungi, humans have inadvertently
stopped the feedback mechanism in this evolutionary play (Figure 3b). Additionally, the
ecological theater has been altered by anthropogenic changes of biotic the environment.
Understanding long-term mycorrhizal function in communities and ecosystems requires a
holistic perspective that considers both the evolutionary play and the ecological theater.
Acknowledgements
We appreciate insightful suggestions from Pål-Axel Olsson, Håkan Wallander, and Jim
Graham and financial support from the National Science Foundation DEB-9806529, DEB0087017, DEB-0236204, DEB-0316136 and the Fulbright Commission.
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Figure Legends
Figure 1. Mycorrhizal function at the ecosystem scale is an emergent property of mycorrhizal
functions at individual and community scales.
Figure 2. Modification of Treseder and Allen’s (2002) model of the relationship between
mycorrhizal biomass and resource availability (a). Mycorrhizal biomass is expected to
decrease when soils are enriched with nutrients because fungi will become carbon limited as
plants reduce carbon allocation belowground – shown in the shaded area (b). Mycorrhizal
biomass is predicted to increase with elevated atmospheric carbon dioxide because plant
demands for N and P will rise as carbon assimilation rates increase, and mycorrhizal fungi
will be less carbon limited. Thus, at elevated carbon dioxide (dotted line) the mycorrhizal
biomass response curve will be higher and shifted to the right compared to ambient carbon
dioxide (solid line) (c).
Figure 3. Ecotypes of co-occurring plant and mycorrhizal fungi are expected to evolve in
response to each other and their local rhizosphere environment (a). Agriculture, horticulture,
and plantation forestry uncouple evolutionary feedbacks between plant and mycorrhizal
fungal ecotypes (b). Remake 3a to have stacks of circles over time.
Figure 4. The rhizosphere (left) and mycorrhizosphere (right) of a pine seedlings differ
dramatically from one another in plant and soil attributes. Mycorrhizal plants typically have
larger shoots and smaller root systems compared to non-mycorrhizal plants. The extent of the
soil explored by fungi vastly exceeds that of the root system, though the average magnitude of
this effect is underemphasized in this illustration. More than one species of EM fungi
frequently colonizes a host plant imparting its own unique properties on the portion of the root
system it colonizes. In this figure, hypothetical fungus species A is shown in black, B in
dashed lines and C in grey. Fungi A, B, and C may differ in their drought tolerance, ability to
utilize organic nutrient sources, extent of soil exploration, ability to compete with saprotrophs,
energetic cost to the plant or in a variety of other ways. Fungus species C is shared by two
conspecific plants and may allow exchange of resources between adjacent plants. In addition
to these differences, ectomycorrhizal fungi alter rhizosphere chemistry through unique fungal
compounds such as chitin, and ergosterol, and through the production of diverse
carbohydrates, enzymes, organic acids and secondary metabolites. The combined physical,
chemical, and biotic changes associated with the mycorrhizosphere influence the fitness of
individual pine seedlings and also have ecosystem-scale consequences.
Figure 5. Characteristic mycorrhizal types and soil properties of major terrestrial biomes.
Mycorrhizal fungi with advanced saprotrophic capabilities predominate in high latitude and
altitude biomes wehre decomposition and mineralization processes are inhibited. Modified
from Read and Perez-Moreno 2003.
49
Table 1. Characteristics of six distinct groups of mycorrhizs. Sources of information: Smith and Read 1997; Brundrett 2002
Mycorrhiza
Arbuscular
Fungal partners
Plant partners
Resources exchanged
Ecosystems where mycorrhiza
from plant/from fungus
predominates
Glomeromycota:
Bryophytes, Pteridophytes,
CHO / mineral forms of P,
Agroecosystems, grasslands, deserts,
Glomales
Gymnosperms, Angiosperms
N, Zn, Cu etc.
temperate decidous forests, tropical
rainforests
Ectomycorrhiza Basidiomycota,
Gymnosperms, Angiosperms
Ascomycota and
CHO / organic & mineral
Boreal forests, evergreen and deciduous
forms of N, P, Zn, Cu etc.
temperate forests
Zygomycota
Ericoid
Ascomycota:
Ericales: Ericaceae,
CHO / organic & mineral
All ecosystems where the Ericales
Leotiales
Epacridaceae, Empetraceae
forms of N, P, Zn, Cu etc.
occur, particularly abundant in tundra,
heathlands, boreal forests
Arbutoid
Basidiomycota
Ericales: Arbutus,
CHO / organic & mineral
Chaparral and other ecosystems where
Arctostaphylos, Pyrolaceae,
forms of N, P, Zn, Cu etc.
the Arbutoideace occur
Bryophytes
Monotropoid
Basidiomycota
Ericales: Monotropoideae
CHO ( from photosynthetic Evergreen and deciduous temperate
plant) / CHO (to
forests of the northern hemisphere
heterotrophic plant),
minerals
Orchid
Basidiomycota
Orchidaceae
? / CHO and minerals
All ecosystems where orchids occur,
particularly abundant in tropical systems
50
Figure 1.
Interactions among mycorrhizas, abiotic factors and biotic
communities influence ecosystem properties:
 Rhizosphere structure
 Soil fertility & nutrient cycling
 Ecosystem production
Interactions among mycorrhizas, plants, fungi, bacteria,
and animals influence community properties:
 Species composition
 Diversity
 Dynamics Interactions between single plant – fungus
pairs influence individual properties:



Gene expression of partners
Fitness of partners
Population dynamics of partners
MYCORRHIZAL
FUNCTION
51
Figure 2.
Plant N or P
limitation
a.
Mycorrhizal
Biomass
Fungal N or P
limitation
Low
Reduced allocation
of C to fungus
High
Soil N or P availability
52
Plant N or P
limitation
b.
Mycorrhizal
Biomass
Fungal N or P
limitation
Low
Reduced allocation
of C to fungus
High
Soil N or P availability
Plant N or P
limitation
c.
Mycorrhizal
Biomass
Fungal N or P
limitation
Low
Reduced allocation
of C to fungus
High
Soil N or P availability
53
Figure 3.
(a)
Rhizospher
ee
Rhizosphere
Plant
ecotyp
Plant
es
Rhizosphere
ecotypes
Fungal
ecotypes
PlantRhizosphere
ecotypes
Fungal
Plant Rhizosphere
ecotypes
ecotypes
Plant ecotypes
Fungal
ecotypes
Time
Fungal ecotypes
Fungal ecotypes
(b)
Cultivar
Rhizosphere
Fungal ecotypes
Environment
54
Figure 5.
Heathland
Boreal Forest
Temperate Forest
Grassland
Ericoid (some EM)
EM (Ericoid understory)
EM (AM understory)
AM
Humus and soil organic N and P
Nitrification and mineralization
Soil P availability
Soil pH
55
56