A Diversity of Types
Last time, we examined a general definition of mycorrhiza and found that it was surprisingly complex. This time, we'll begin to delve into the diversity of mycorrhizas, beginning with their anatomical and taxonomic aspects. As you'll see, there are several different types of mycorrhiza, they differ in their global distribution and abundance, and they have different evolutionary histories. So let's get started.
A Brief Recap
The term mycorrhiza is derived from the Greek words for fungus and root. It is one of several types of plant/fungus symbiosis and can be defined as "a mutualistic symbiosis between plant and fungus localized in a root or root-like structure in which energy moves primarily from plant to fungus and inorganic resources move from fungus to plant" (Allen 1991). If more than the name sounds Greek to you, check out the first installment. As last time, terms are defined in the glossary.
Anatomical Diversity of Mycorrhizas
There are many types of mycorrhiza. However, before we can understand the different types, we need to appreciate the features used to differentiate them, such as the portions of the root involved and the types of structures produced by the fungi. First we'll consider the structure of a non-mycorrhizal plant root with centralized conducting tissue (some plants have multiple bundles of conducting tissue arranged in a ring). For our purposes, the root can be seen as consisting of four main regions (Figure 1):
Figure 1: Idealized cross-section of a non-mycorrhizal root showing the four principal regions -- epidermis, cortex, endodermis, and stele. Note that root hairs are modified epidermal cells.
(Drawings by Maggie Rogers)
The epidermis ("outer skin") is the outermost layer of cells and its function is to protect the inner tissues. Root hairs are greatly enlarged and extended epidermal cells; however, they are much less abundant in nature than botany textbooks would lead you to believe. The cortex, or ground tissue, makes up most of the root's mass. It is comprised of soap-bubble-shaped cells and often serves as a storage place for food reserves and waste materials.
The endodermis ("inner skin") consists of a single layer of cells separating the cortex from the stele. These cells have strips of impervious cork-like material in their walls, which serve to prevent movement of substances between cortex and stele through the cell walls. All movement therefore must be through the cell interiors where passage can be closely regulated by the cell membrane.
The innermost region is the stele, or conducting tissue. It includes the xylem, which transports water and minerals mostly from the roots to the shoot, and the phloem, which transports food materials mostly from shoot to roots.
Now, with the root structure as a framework, we can look at where the fungi occur in mycorrhizas. Most mushroom field guides use a generic Amanita to illustrate the different parts of a mushroom such as cap, stipe, and volva, because many amanitas have all the possible parts -- whereas many other mushrooms come only partially equipped. In similar fashion, I'll describe the possible parts of a mycorrhiza from the fungus's perspective -- but keep in mind, you'll soon see that, unlike amanitas, no mycorrhizas come fully equipped. The four parts ("phases") of the fungus that we'll consider are:
The intraradical ("within root") phase is comprised of simple hyphae, with or without additional structures, that occur within the root epidermis and cortex, either between and within individual cells or just between them. The fungus is restricted to the cortex and epidermis -- it does not cross the endodermis and enter the stele.
The periradical ("around root") phase is comprised of a layer of hyphae that surrounds the root like a sock or glove.
The extraradical ("beyond root") phase is comprised of hyphae which extend in typical mycelial fashion into the soil surrounding the root. Part of the extraradical phase may also consist of rhizomorphs, which are relatively tough aggregations of many hyphae. They often are visible with the naked eye -- for instance, many mushroomers have seen the black, "bootlace" rhizomorphs produced by honey mushrooms (Armillaria spp.).
The reproductive phase is the spores, which may be produced within a fruiting body or sporocarp, such as a mushroom or truffle. Now we're ready to look at the anatomically different types of mycorrhiza.
Traditionally, two classes of mycorrhiza have been recognized -- ectomycorrhiza and endomycorrhiza (also referred to as ectotrophic and endotrophic mycorrhizas, although these terms aren't used much anymore). However, over the years as more observations have been made and the significance of earlier observations appreciated, we have come to realize that this simple two-part categorization cannot adequately describe the range of diversity in mycorrhizas. Thus, Jack Harley and Sally Smith (1983) recognized seven types that, for the most part, still comprise the generally accepted classification. I'll describe the key features of each of these seven types, paying greatest attention to the three types that are most widespread and ecologically important (Figure 2).
Figure 2:Cross-sections of three types of mycorrhizal root. From left to right, arbuscular mycorrhiza, ectomycorrhiza, and ericoid mycorrhiza. Roots are not drawn to same scale -- ectomycorrhizal roots would be the largest of the three types, ericoid roots the smallest. In the arbuscular mycorrhiza and ectomycorrhiza, the external hyphae typically would be much more numerous and extend much farther out into the soil than could be shown in these illustrations. Redrawn with modifications from Molina et al. (1992).
Ectomycorrhizas ("outside" mycorrhizas) are the easiest type to recognize in the field, being discernible with the unaided eye. Their name comes from the fact that they have an often well developed periradical phase (called the mantle or sheath), present as a thin-to-thick mass of hyphae that covers the outside of the fine root tips and provides a characteristic appearance (Figure 3). Abundant hyphae emanate from the mantle into the surrounding soil to form the extraradical phase, and sporocarps, often as mushrooms or truffles, develop from the extraradical mycelium. However, many ectomycorrhizal fungi appear to produce infrequent or inconspicuous sporocarps or none at all. This has implications for trying to characterize the ectomycorrhizal fungi of an area solely by collecting mushrooms and other sporocarps, a topic I'll discuss in a later installment.
Figure 3: Examples of ectomycorrhizal root tips. Many are easy to recognize with the unaided eye, but are better observed with a hand lens or dissecting microscope.
The intraradical phase of ectomycorrhizas consists of the so-called Hartig net, named for Robert Hartig, a 19th-century German plant pathologist. It consists of a network of hyphae that extends between the cortex cells in much the same way that mortar surrounds bricks in a wall. The fact that these hyphae do not enter the cells, but instead stay outside them, provides another rationale for calling this type of mycorrhiza ectomycorrhiza.
Endomycorrhizas ("inside" mycorrhizas) do not form a mantle around the root, so have no periradical phase. They have an often well developed extraradical phase, as a typical mycelial network permeating the soil. The fungi do not form complex sporocarps, instead reproducing by means of large spores that remain in the soil and are moved around with it. These spores can be large enough to be seen with the naked eye (they often are 10 to 50 times larger than typical mushroom spores), and thus cannot be transported readily by air currents the way that mushroom spores are.
The intraradical phase of endomycorrhizas consists of hyphae that meander between the cortex cells, and often enter them (hence the name endomycorrhiza). Although the hyphae do penetrate the cortical cell walls, they do not penetrate the cell membrane but merely invaginate it. This relationship can be understood by envisioning a shoe-box (cell wall) with a balloon (cell membrane) blown-up tightly against its insides. Just as you can poke your fingers "into" an inflated balloon without actually being inside it, the fungal hyphae and associated structures remain physiologically outside the cell membrane despite being present within the cells. Inside the cells, the hyphae may form dense coils, loop around once or twice, or form structures called arbuscules and vesicles. Arbuscules ("little trees") are branched shrub-like features that are believed to be the sites of material exchanges between the fungus and plant. All endomycorrhizas appear to produce them, although they may not be present at all times of the year. Vesicles are balloon-shaped storage structures.
Based on these latter two features, this type of mycorrhiza has long been called vesicular-arbuscular or VA, terms you've probably heard before. However, because not all of the endomycorrhizal fungi appear to produce vesicles, the current trend is to call them arbuscular mycorrhizas. As you read the literature on mycorrhizas, you undoubtedly will encounter all three terms -- endomycorrhiza, vesicular-arbuscular mycorrhiza, and arbuscular mycorrhiza. In general, you can consider them to be equivalent.
Ericoid mycorrhizas are the third of the three more ecologically important types, along with ectomycorrhizas and arbuscular mycorrhizas. They have a simple intraradical phase, consisting of dense coils of hyphae in the outermost layer of root cells. There is no periradical phase and the extraradical phase consists of sparse hyphae that don't extend very far into the surrounding soil. They might form sporocarps (probably in the form of small cups), but their reproductive biology is little understood.
The remaining four types of mycorrhiza and their key features can be summarized as follows:
- Ectendomycorrhizas (with or without mantle, with Hartig net and cellular penetration by hyphal coils)
- Arbutoid mycorrhizas -- (with mantle, Hartig net, and cellular penetration by hyphal coils)
- Monotropoid mycorrhizas -- (with mantle, Hartig net, and cellular penetration)
- Orchid mycorrhizas -- (without mantle and with cellular penetration by hyphal coils)
These types are not as important ecologically as the other three, either because they are not as common, or because they don't involve the dominant members of the plant communities in which they occur. However, as we will see in later installments, some of them are extremely interesting biologically, and raise some thorny issues concerning how mycorrhizas should be defined.
Survey of Mycorrhiza Types (and the Plants and Fungi That Form Them)
A relatively small percentage of the roughly 70,000 species of fungi described to date and a rather large percentage of the roughly 300,000 species of higher plants are mycotrophic. Arbuscular mycorrhizas are by far the most common and widespread, being formed by about 170 species of mold-like fungi from the Order Glomales of the zygomycetes and plants from nearly all families.
Ectomycorrhizas are formed by more than 5000 species of basidiomycetes and ascomycetes and perhaps 2000 species of plants, mostly conifer trees and woody . Virtually all species in families such as the Pinaceae (pines, firs, spruces, etc.), Fagaceae (oaks, beeches, and southern beeches), and Betulaceae (birches) are mycotrophic.
Ericoid mycorrhizas are formed by a small number of ascomycetes and plants in the Ericaceae and closely related plant families. Although this mycorrhiza type involves relatively few species of both plants and fungi, it is widely distributed and constitutes the dominant mycorrhiza type in certain environments (see below). Typical ericoid mycorrhizal plants include huckleberries and rhododendrons.
Ectendomycorrhizas have been observed in conifers and seem to involve basidiomycete fungi. They represent the least understood type of mycorrhiza. Arbutoid mycorrhizas are formed by the ericaceous plants Arbutus (madrone) and Arctostaphylos (manzanita) and basidiomycete fungi that apparently are capable of forming ectomycorrhizas with other plants. Monotropoid mycorrhizas are formed by monotropes and ectomycorrhizal fungi such as russulas, rhizopogons, and suilluses. Monotropes are herbaceous plants that lack chlorophyll and thus cannot manufacture their own food. They have been classified in the Ericaceae, as well as in their own family, the Monotropaceae. Orchid mycorrhizas, logically enough, are formed by orchids and basidiomycete fungi, many of which are regarded as plant pathogens, such as Armillaria.
Thus, mycorrhizas are thought to occur in at least some members of nearly all plant families and at least 80-90% of higher plant species. Arbuscular mycorrhizas also occur in so-called lower plants such as whisk fern (Psilotum nudum), ground pines (Lycopodium spp.), mosses, liverworts, and ferns.
Although the mycotrophic status of only a small percentage of all plant species has been determined directly, Harley and Smith (1983) concluded that "In any ecosystem, not only are most species and individuals of plants mycorrhizal, but most are extensively infected in situations of nutrient deficiency." That statement still appears to be justified.
It is clear that different plants vary widely in the degree to which they depend on mycorrhizas. Some, such as members of the Pinaceae, appear to be obligately mycotrophic, that is, they cannot survive in nature without being associated with mycorrhizal fungi. The largest number in most other families appear to be facultatively mycotrophic -- depending on variables such as environmental conditions, time of year, and associated plants, individuals of these species may or may not be mycorrhizal at a given time. For instance, horsetail or scouring rush (Equisetum spp.) often has been thought to be non-mycotrophic based on collections from wet habitats; however, when growing in relatively dry habitats, some species form mycorrhizas. In arctic and alpine areas, the activity of arbuscular mycorrhizas in plants such as buttercups (Ranunculus spp.) varies seasonally in response to temperature, moisture, and day-length, so collections made at different times of year could produce very different conclusions about mycotrophic status.
Overall, only a relatively small number of species appears to be non-mycotrophic. These tend to be mostly weedy species in families such as the Brassicaceae (mustards), Cyperaceae (sedges), and Chenopodiaceae (spinach, lamb's quarters).
Evolutionary History of Mycorrhizas
Mycorrhizas have a long evolutionary history. This can be inferred from three main lines of evidence. The presence of branched hyphae (some with coils) and spheres that resemble vesicles within the "roots" (actually underground stems) of early land plant fossils indicates that arbuscular mycorrhizas originated no later than the Silurian Period, over 400 million years ago.
Although it is difficult to prove a physiological relationship from fossil structures, the ubiquity of arbuscular mycorrhizas in today's world and the tremendous taxonomic range of the plants involved in them strongly reinforce the notion of their great antiquity. Molecular clock techniques also have lent support, placing the origin of the zygomycetes (the phylum of fungi involved in arbuscular mycorrhizas) at about 500 million years ago (Late Cambrian or Early Ordovician Period, not long after the appearance of the first complex multicellular organisms). Because these first land plants had no true roots, and their underground stems clearly were not capable of efficient extraction of nutrients from the soil, it is easy to believe that mycorrhizas were necessary for colonization of land by plants. Parallels in the histories of the terrestrial plant groups and mycorrhiza types suggest that the diversification and spread of land plants also may have been linked closely to diversification of the fungi and development of new physiologically distinct types of mycorrhiza.
Thus, the development of different mycorrhiza types could have been a major factor in allowing plants to exploit the wide range of physical habitats that resulted from continental breakup during the Mesozoic Era (roughly 220 to 65 million years ago) and increasingly diverse climates that have developed since the end of the Eocene Epoch of the Tertiary Period (roughly 40 million years ago).
Ectomycorrhizas evolved much more recently than did arbuscular mycorrhizas (perhaps 130 to 200 million years ago, along with dinosaurs during the Mesozoic Era), as indicated by molecular clock evidence on the origins of the basidiomycetes and ascomycetes, and their restricted occurrence in more recently evolved plant groups (conifers, especially Pinaceae, and woody angiosperms).
Most of the other mycorrhiza types, including ericoid, arbutoid, monotropoid, and orchid, involve plants from even younger angiosperm families and reflect even more recent origins. The most recent development of all appears to be the evolution of the non-mycotrophic condition, as consistently non-mycorrhizal species represent a large majority only in the youngest angiosperm families such as the Brassicaceae (mustards) and Cyperaceae (sedges). Hence, non-mycotrophy represents a derived condition; that is, non-mycotrophic plants evolved from mycotrophic ancestors.
Landscape Distribution of Mycorrhiza Types
From a plant's perspective, the major role of most mycorrhizas is to provide access to water, growth-limiting nutrients, or carbon at critical times in its development. Both the limiting factor(s) and the critical points in development differ from species to species and place to place, so it is not surprising that the patterns of distribution of different types of mycorrhiza seem related to soil factors and climate (see Read 1991).
Arbuscular mycorrhiza is the dominant type in the tropics, and in grasslands and deserts of temperate latitudes. Ectomycorrhizas predominate in temperate and boreal forests. In even higher latitude areas, the ericoid mycorrhizas flourish in heathlands. Although this broad pattern does exist, remember that it masks much underlying complexity and that many areas support mixtures of the different mycorrhiza types. We'll examine the reasons behind these distribution patterns in a future installment.
Thus, the symbioses called mycorrhiza encompass a broad range of diversity. The fungi involved comprise a taxonomically, morphologically, and anatomically diverse group of organisms from different fungus phylums and are similar only in their convergent evolution toward a somewhat similar habit and symbiosis type. However, the pattern of diversity in mycorrhizal fungi differs from that in plants. For example, a north temperate conifer forest such as those near my home in Seattle, Washington might have more than 1000 species of ectomycorrhizal fungi associated with a handful of dominant tree species, whereas a Mexican tropical deciduous forest might have fewer than 25 species of arbuscular mycorrhizal fungi associated with 1000 or more plant species. Such interesting patterns have been noticed only recently and the reasons behind them have yet to be discovered.
In the next installment of this series, we'll look more closely at the physiology of mycorrhizas -- what they do and how they do it.
- Allen, Michael F. 1991. The ecology of mycorrhizae. Cambridge University Press, Cambridge.
- Harley, J.L. and S.E. Smith 1983. Mycorrhizal symbiosis (1st ed.). Academic Press, London.
- Molina, Randy, Hugues Massicote, and James M. Trappe. 1992. Specificity phenomena in mycorrhizal symbioses: Community-ecological consequences and practical implications. Pages 357-423 in: Allen, Michael F. (ed.). Mycorrhizal functioning -- an integrated plant-fungal process. Chapman & Hall, New York.
- Read, D.J. 1991. Mycorrhizas in ecosystems. Experientia 47:376-391.
- A plant that reproduces by means of flowers. Includes most of the plants we see around us every day such as oaks, maples, roses, blueberries, buttercups, clovers, lilies, grasses, and sunflowers.
- The most basic structural and physiologic unit of any organism.
- A thin complex film that surrounds cells and many of their components. Membranes play important functional roles by controlling the movement of substances across them -- for instance into and out of cells.
- Molecular clock
- A means of estimating the ages of groups of organisms based on the number of differences in their DNA and the assumption that differences accumulate through random mutations at a fairly constant rate.
- Describes an individual plant which has formed mycorrhizas.
- Describes a group of plants (species, genus, family, etc.) whose members can or must enter into mycorrhizal relationships
- Plant root (sounds more impressive than would "root" in terms such as periradical). Also used to refer to one who possesses an extreme belief in the importance of mycorrhizas.
- The aboveground portions of a plant; includes stems, leaves, flowers, and fruits.
- An aggregation of cells that forms a structural unit of large organisms. Different tissues together form organs.
This material appeared in slightly modified form in Mushroom: the Journal of Wild Mushrooming, Issue 69, Fall 2000. It can be used freely for not-for-profit personal and educational purposes provided that its source is clearly credited.