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. The term “mycorrhizosphere” was coined to describe the unique properties of the rhizosphere surrounding and influenced by mycorrhizas (Linderman 1988). Figure 1illustrates pine seedlingswith and without mycorrhizas to highlight some of these properties. 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 often connect plant root systems over broad areas. These fungi frequently comprise the largest portion of soil microbial biomass (Olsson et al. 1999; Högberg and Högberg 2002). Thus, mycorrhizal symbioses physically and chemically structure the rhizosphere, and they impact communities and ecosystems.

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 the roles of mycorrhizas in the structure and functioning of communities and ecosystems, and explore their responses to anthropogenic environmental changes.

II. Convergent Evolution of Mycorrhizas

Throughout their evolution, plant roots have repeatedly formed symbioses with fungi. With remarkably 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 (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 Malloch (1975) suggest 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.

A. Arbuscular mycorrhizas

Arbuscular mycorrhizas are widespread and abundant. They are formed by bryophytes, pteridophytes, gymnosperms and angiosperms, and are ubiquitous in most 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 or coils. 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.

B. Ectomycorrhizas

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 (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 (LePage 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.

C. Mycorrhizas in the Ericales

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 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 “peg” of fungal hyphae that proliferates within the epidermis of the root (Smith and Read 1997).

D. Orchid Mycorrhizas

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.

III. Mycorrhizas as Nutritional Mutualisms
Except for orchid and monotropoid associations, mycorrhizas involve plant exchange of photosynthates in return for fungal exchange of mineral nutrients. The convergence of so many unrelated forms of mycorrhizas is a testament for the mutual benefits of these trading partnerships. 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, extending far 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 (Van Breemen et al. 2000). Recent 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).

Most mycorrhizal fungi depend heavily on plant photosynthate to meet their energy requirements, AM fungi are obligate biotrophs while EM and ericoid fungi are biotrophs with 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 (Smith and Read 1997). Root colonization by mycorrhizal fungi often increase rates of host plant photosynthesis. 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; Wright et al. 1998a)

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 (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 2a). 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 carbon allocated belowground.
  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 (shaded area in figure 2a). 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 mycorrhizal fungi generally acquire phosphorus more readily than their host plants, we predict that the mutualistic value of mycorrhizal associations will be highest at high soil N:P ratios and diminish as N:P ratios decrease.

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. 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 provide a fungal partner with photosynthates than to maintain fibrous root systems (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; Figure 1).

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 mycorrhizal costs are minimized and benefits are maximized within the local soil fertility conditions.

IV. Community Interactions

Mycorrhizal interactions influence the species composition, diversity, and stability of biotic communities. 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. 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.

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; Graham and Abbott 2000).

A. 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 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 mutualistic isolates of AM fungi were selected for within the rhizospheres of individual plants grown in pots during two ten-week cycles. In contrast, when ten plant species were randomly paired with ten AM fungal isolates from the same grassland, the function of the partnerships varied from strongly mutualistic to strongly parasitic (Klironomos 2003). 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.

Extraradical hyphae from individual clones of mycorrhizal fungi frequently link the root systems of neighboring plants of the same as well as different species (Figure 1). 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 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 structure and ecosystem processes.