| |
|
|
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).
|
| |
|
|
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.
Wrap-up
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.
References
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.
Glossary
Angiosperm
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.
Cell
The most basic structural and physiologic unit of any organism.
Membrane
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.
Mycorrhizal
Describes an individual plant which has formed mycorrhizas.
Mycotrophic
Describes a group of plants (species, genus, family, etc.) whose
members can or must enter into mycorrhizal relationships
Radical
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.
Shoot
The aboveground portions of a plant; includes stems, leaves, flowers,
and fruits.
Tissue
An aggregation of cells that forms a structural unit of large organisms.
Different tissues together form organs.
|
