.jpg)
Many conspicuous fungi such as the fly agaric (upper left) form ectomycorrhiza (upper right) with tree rootlets. Arbuscular mycorrhiza (lower left) are very common in plants, including crop species such as wheat (lower right)
In a mycorrhizal association, the fungus colonizes the host plant's root tissues, either intracellularly as in arbuscular mycorrhizal fungi (AMF or AM), or extracellularly as in ectomycorrhizal fungi. The association is sometimes mutualistic. In particular species or in particular circumstances mycorrhizae may have a parasitic association with host plants.
Definition
A mycorrhiza is a symbiotic association between a green plant and a fungus. The plant makes organic molecules such as sugars by photosynthesis and supplies them to the fungus, and the fungus supplies to the plant water and mineral nutrients, such as phosphorus, taken from the soil. Mycorrhizas are located in the roots of vascular plants, but mycorrhiza-like associations also occur in bryophytes and there is fossil evidence that early land plants that lacked roots formed arbuscular mycorrhizal associations. Most plant species form mycorrhizal associations, though some families like Brassicaceae and Chenopodiaceae
cannot. Different forms for the association are detailed in the next
section. The most common is the arbuscular type that is present in 70%
of plant species, including many crop plants such as wheat and rice.
Types
Mycorrhizas are commonly divided into ectomycorrhizas and endomycorrhizas. The two types are differentiated by the fact that the hyphae of ectomycorrhizal fungi do not penetrate individual cells within the root, while the hyphae of endomycorrhizal fungi penetrate the cell wall and invaginate the cell membrane. Endomycorrhiza includes arbuscular, ericoid, and orchid mycorrhiza, while arbutoid mycorrhizas can be classified as ectoendomycorrhizas. Monotropoid mycorrhizas form a special category.
Ectomycorrhiza
Leccinum aurantiacum, an ectomycorrhizal fungus
Ectomycorrhizas, or EcM, are symbiotic associations between the roots
of around 10% of plant families, mostly woody plants including the birch, dipterocarp, eucalyptus, oak, pine, and rose families, orchids, and fungi belonging to the Basidiomycota, Ascomycota, and Zygomycota. Some EcM fungi, such as many Leccinum and Suillus, are symbiotic with only one particular genus of plant, while other fungi, such as the Amanita, are generalists that form mycorrhizas with many different plants. An individual tree may have 15 or more different fungal EcM partners at one time.
Thousands of ectomycorrhizal fungal species exist, hosted in over 200
genera. A recent study has conservatively estimated global
ectomycorrhizal fungal species richness at approximately 7750 species,
although, on the basis of estimates of knowns and unknowns in
macromycete diversity, a final estimate of ECM species richness would
probably be between 20,000 and 25,000.
Ectomycorrhizas consist of a hyphal sheath, or mantle, covering the root tip and a Hartig net of hyphae surrounding the plant cells within the root cortex.
In some cases the hyphae may also penetrate the plant cells, in which
case the mycorrhiza is called an ectendomycorrhiza. Outside the root, ectomycorrhizal extramatrical mycelium forms an extensive network within the soil and leaf litter.
Nutrients can be shown to move between different plants through the fungal network. Carbon has been shown to move from paper birch trees into Douglas-fir trees thereby promoting succession in ecosystems. The ectomycorrhizal fungus Laccaria bicolor has been found to lure and kill springtails to obtain nitrogen, some of which may then be transferred to the mycorrhizal host plant. In a study by Klironomos and Hart, Eastern White Pine inoculated with L. bicolor was able to derive up to 25% of its nitrogen from springtails.
When compared to non-mycorrhizal fine roots, ectomycorrhizae may
contain very high concentrations of trace elements, including toxic
metals (cadmium, silver) or chlorine.
The first genomic sequence for a representative of symbiotic fungi, the ectomycorrhizal basidiomycete L. bicolor, has been published.
An expansion of several multigene families occurred in this fungus,
suggesting that adaptation to symbiosis proceeded by gene duplication.
Within lineage-specific genes those coding for symbiosis-regulated
secreted proteins showed an up-regulated expression in ectomycorrhizal
root tips suggesting a role in the partner communication. L. bicolor
is lacking enzymes involved in the degradation of plant cell wall
components (cellulose, hemicellulose, pectins and pectates), preventing
the symbiont from degrading host cells during the root colonisation. By
contrast, L. bicolor possesses expanded multigene families
associated with hydrolysis of bacterial and microfauna polysaccharides
and proteins. This genome analysis revealed the dual saprotrophic and biotrophic lifestyle of the mycorrhizal fungus that enables it to grow within both soil and living plant roots.
Arbutoid mycorrhiza
This type of mycorrhiza involves plants of the Ericaceae subfamily Arbutoideae.
It is however different from ericoid mycorrhiza and resembles
ectomycorrhiza, both functionally and in terms of the fungi involved. The difference to ectomycorrhiza is that some hyphae actually penetrate into the root cells, making this type of mycorrhiza an ectendomycorrhiza.
Endomycorrhiza
Arbuscular mycorrhiza
Endomycorrhizas are variable and have been further classified as
arbuscular, ericoid, arbutoid, monotropoid, and orchid mycorrhizas. Arbuscular mycorrhizas,
or AM (formerly known as vesicular-arbuscular mycorrhizas, or VAM), are
mycorrhizas whose hyphae penetrate plant cells, producing structures
that are either balloon-like (vesicles) or dichotomously branching
invaginations (arbuscules) as a means of nutrient exchange. The fungal hyphae do not in fact penetrate the protoplast (i.e. the interior of the cell), but invaginate the cell membrane. The structure of the arbuscules greatly increases the contact surface area between the hypha and the cell cytoplasm to facilitate the transfer of nutrients between them.
Arbuscular mycorrhizas are formed only by fungi in the division Glomeromycota. Fossil evidence and DNA sequence analysis suggest that this mutualism appeared 400-460 million years ago,
when the first plants were colonizing land. Arbuscular mycorrhizas are
found in 85% of all plant families, and occur in many crop species. The hyphae of arbuscular mycorrhizal fungi produce the glycoprotein glomalin,
which may be one of the major stores of carbon in the soil. Arbuscular
mycorrhizal fungi have (possibly) been asexual for many millions of
years and, unusually, individuals can contain many genetically different
nuclei (a phenomenon called heterokaryosis).
Ericoid mycorrhiza
An ericoid mycorrhizal fungus isolated from Woollsia pungens
Ericoid mycorrhizas
are the third of the three more ecologically important types. They have
a simple intraradical (grow in cells) 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.
Ericoid mycorrhizas have also been shown to have considerable saprotrophic
capabilities, which would enable plants to receive nutrients from
not-yet-decomposed materials via the decomposing actions of their ericoid partners.
Orchid mycorrhiza
All orchids are myco-heterotrophic at some stage during their lifecycle and form orchid mycorrhizas with a range of basidiomycete fungi. Their hyphae penetrate into the root cells and form pelotons (coils) for nutrient exchange.
Monotropoid mycorrhiza
This type of mycorrhiza occurs in the subfamily Monotropoideae of the Ericaceae, as well as several genera in the Orchidaceae. These plants are heterotrophic or mixotrophic and derive their carbon from the fungus partner. This is thus a non-mutualistic, parasitic type of mycorrhizal symbiosis.
Mutualist dynamics
Mycorrhizal fungi form a mutualistic
relationship with the roots of most plant species. In such a
relationship, both the plants themselves and those parts of the roots
that host the fungi, are said to be mycorrhizal. Relatively few of the
mycorrhizal relationships between plant species and fungi have been
examined to date, but 95% of the plant families investigated are
predominantly mycorrhizal either in the sense that most of their species
associate beneficially with mycorrhizae, or are absolutely dependent on
mycorrhizae. The Orchidaceae are notorious as a family in which the absence of the correct mycorrhizae is fatal even to germinating seeds.
Recent research into ectomycorrhizal plants in boreal forests
has indicated that mycorrhizal fungi and plants have a relationship
that may be more complex than simply mutualistic. This relationship was
noted when mycorrhizal fungi were unexpectedly found to be hoarding
nitrogen from plant roots in times of nitrogen scarcity. Researchers
argue that some mycorrhizae distribute nutrients based upon the
environment with surrounding plants and other mycorrhizae. They go on to
explain how this updated model could explain why mycorrhizae do not
alleviate plant nitrogen limitation, and why plants can switch abruptly
from a mixed strategy with both mycorrhizal and nonmycorrhizal roots to a
purely mycorrhizal strategy as soil nitrogen availability declines.
It has also been suggested that evolutionary and phylogenetic
relationships can explain much more variation in the strength of
mycorrhizal mutualisms than ecological factors.
Sugar-water/mineral exchange
In
this mutualism, fungal hyphae (E) increase the surface area of the root
and uptake of key nutrients while the plant supplies the fungi with
fixed carbon (A=root cortex, B=root epidermis, C=arbuscle, D=vesicle,
F=root hair, G=nuclei).
The mycorrhizal mutualistic association provides the fungus with relatively constant and direct access to carbohydrates, such as glucose and sucrose.
The carbohydrates are translocated from their source (usually leaves)
to root tissue and on to the plant's fungal partners. In return, the
plant gains the benefits of the mycelium's
higher absorptive capacity for water and mineral nutrients, partly
because of the large surface area of fungal hyphae, which are much
longer and finer than plant root hairs,
and partly because some such fungi can mobilize soil minerals
unavailable to the plants' roots. The effect is thus to improve the
plant's mineral absorption capabilities.
Unaided plant roots may be unable to take up nutrients that are chemically or physically immobilised; examples include phosphate ions and micronutrients such as iron. One form of such immobilization occurs in soil with high clay content, or soils with a strongly basic pH. The mycelium of the mycorrhizal fungus can, however, access many such nutrient sources, and make them available to the plants they colonize.
Thus, many plants are able to obtain phosphate, without using soil as a
source. Another form of immobilisation is when nutrients are locked up
in organic matter that is slow to decay, such as wood, and some
mycorrhizal fungi act directly as decay organisms, mobilising the
nutrients and passing some onto the host plants; for example, in some dystrophic forests, large amounts of phosphate and other nutrients are taken up by mycorrhizal hyphae acting directly on leaf litter, bypassing the need for soil uptake. Inga alley cropping, proposed as an alternative to slash and burn rainforest destruction, relies upon mycorrhiza within the root system of species of Inga to prevent the rain from washing phosphorus out of the soil.
In some more complex relationships, mycorrhizal fungi do not just
collect immobilised soil nutrients, but connect individual plants
together by mycorrhizal networks that transport water, carbon, and other nutrients directly from plant to plant through underground hyphal networks.
Suillus tomentosus, a basidiomycete fungus, produces specialized structures known as tuberculate ectomycorrhizae with its plant host lodgepole pine (Pinus contorta var. latifolia). These structures have been shown to host nitrogen fixing bacteria which contribute a significant amount of nitrogen and allow the pines to colonize nutrient-poor sites.
Mechanisms
The
mechanisms by which mycorrhizae increase absorption include some that
are physical and some that are chemical. Physically, most mycorrhizal
mycelia are much smaller in diameter than the smallest root or root
hair, and thus can explore soil material that roots and root hairs
cannot reach, and provide a larger surface area for absorption.
Chemically, the cell membrane chemistry of fungi differs from that of
plants. For example, they may secrete organic acids that dissolve or chelate many ions, or release them from minerals by ion exchange. Mycorrhizae are especially beneficial for the plant partner in nutrient-poor soils.
Disease, drought and salinity resistance and its correlation to mycorrhizae
Mycorrhizal plants are often more resistant to diseases, such as those caused by microbial soil-borne pathogens.
These associations have been found to assist in plant defense both
above and belowground. Mycorrhizas have been found to excrete enzymes
that are toxic to soil borne organisms such as nematodes.
More recent studies have shown that mycorrhizal associations result in a
priming effect of plants that essentially acts as a primary immune
response. When this association is formed a defense response is
activated similarly to the response that occurs when the plant is under
attack. As a result of this inoculation, defense responses are stronger
in plants with mycorrhizal associations.
AMF was also significantly correlated with soil biological
fertility variables such as soil fungi and soil bacteria, including soil
disease.
Furthermore, AMF was significantly correlated with soil physical
variable, but only with water level and not with aggregate stability. and are also more resistant to the effects of drought.
The significance of arbuscular mycorrhizal fungi includes alleviation of
salt stress and its beneficial effects on plant growth and
productivity. Although salinity can negatively affect arbuscular
mycorrhizal fungi, many reports show improved growth and performance of
mycorrhizal plants under salt stress conditions
Resistance to insects
Recent
research has shown that plants connected by mycorrihzal fungi can use
these underground connections to produce and receive warning signals.
Specifically, when a host plant is attacked by an aphid, the plant
signals surrounding connected plants of its condition. The host plant
releases volatile organic compounds
(VOCs) that attract the insect's predators. The plants connected by
mycorrhizal fungi are also prompted to produce identical VOCs that
protect the uninfected plants from being targeted by the insect.
Additionally, this assists the mycorrhizal fungi by preventing the
plant’s carbon relocation which negatively affects the fungi’s growth
and occurs when the plant is attacked by herbivores.
Colonization of barren soil
Plants grown in sterile soils and growth media often perform poorly without the addition of spores or hyphae of mycorrhizal fungi to colonise the plant roots and aid in the uptake of soil mineral nutrients. The absence of mycorrhizal fungi can also slow plant growth in early succession or on degraded landscapes.
The introduction of alien mycorrhizal plants to nutrient-deficient
ecosystems puts indigenous non-mycorrhizal plants at a competitive
disadvantage. This aptitude to colonize barren soil is defined by the category Oligotroph.
Resistance to toxicity
Fungi have been found to have a protective role for plants rooted in soils with high metal concentrations, such as acidic and contaminated soils. Pine trees inoculated with Pisolithus tinctorius planted in several contaminated sites displayed high tolerance to the prevailing contaminant, survivorship and growth. One study discovered the existence of Suillus luteus strains with varying tolerance of zinc. Another study discovered that zinc-tolerant strains of Suillus bovinus conferred resistance to plants of Pinus sylvestris. This was probably due to binding of the metal to the extramatricial mycelium of the fungus, without affecting the exchange of beneficial substances.
Occurrence of mycorrhizal associations
At around 400 million years old, the Rhynie chert contains an assemblage of fossil plants preserved in sufficient detail that mycorrhizas have been observed in the stems of Aglaophyton major.
Mycorrhizas are present in 92% of plant families studied (80% of species), with arbuscular mycorrhizas being the ancestral and predominant form, and the most prevalent symbiotic association found in the plant kingdom. The structure of arbuscular mycorrhizas has been highly conserved since their first appearance in the fossil record, with both the development of ectomycorrhizas, and the loss of mycorrhizas, evolving convergently on multiple occasions.
Discovery
Associations
of fungi with the roots of plants have been known since at least the
mid-19th century. However early observers simply recorded the fact
without investigating the relationships between the two organisms. This symbiosis was studied and described by Franciszek Kamieński in 1879–1882. Further research was carried out by Albert Bernhard Frank, who introduced the term mycorrhiza in 1885.
