|Mycorrhizas: symbiotic mediators of rhizosphere and ecosystem processes
Nancy Collins Johnson, Catherine A. Gehring
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.
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 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 (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 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 many unrelated forms of mycorrhizas is a testament for the mutual benefits of these trading partnerships.