Symbiosis: Mycorrhizae and Lichens

Symbiosis: Mycorrhizae and Lichens

Introduction
In its most common usage, symbiosis is used to describe the intimate association between two distantly, related species that are mutually benefiting from this association. These associations are obligatory ones in which neither organisms can survive in nature if the two organisms are separated.  However, in the strict sense of this term, as it was proposed by de Barry in 1879, symbiotic relationships include a wide range of associations:

• Phoresy: A loose association where a usually, smaller organism is using a larger one as a transport host. Normally used in references to arthropods and fishes. An example of the latter is the remora.

The remora is a one of several species of marine fishes that have sucking disks with which they attach themselves to sharks, whales, sea turtles, or the hulls of ships, from http://blog.discoveroptions.com/wp-content/uploads/2011/02/ shark_remora_close3.jpg

• Commensalism: An association in which one species, usually the smaller, benefits from the association while the other species seems to be unaffected. Such relationships are usually not obligate and neither species will die if the association does not form. A common example here in Hawai‘i is the cattle egret and  grazing cattle. The cattle egrets are birds that feed where cattle or other herbivores may be grazing. The grazing cattle flushes out insects from the vegetation, which benefits the birds, but this relationship does not seem to benefit the cattle nor does it do any harm.
  
  

  Cattle egret usually associated with cattle or with other large herbivores that while foraging for food, will expose insects that the cattle egret will fit on. The cattle egret benefits from this relationship, but the large herbivore does not, nor is it harmed by the relationship. From http://www.bio.miami.edu/dana/pix/cattle_egret.jpg

• Parasitism: A relationship in which one species (parasite) is obligately dependent upon another organism (host) for its food and shelter. We have had several examples of this type of relationship, during the course of the semester.

For our purpose, symbiosis will be used here in its most common sense, where there is mutual benefit in the relationship. The two most common example in fungi are mycorrhizae and lichens, which we will cover, today.
The subject of symbiosis is usually more scholarly than applicable, but in the case of mycorrhizae, you will see that both scholarly as well as applied research have been carried out. We have already mentioned mycorrhizae on several occasions so that you at least know what a mycorrhiza is, but let’s define it one more time. A mycorrhiza is defined as a symbiotic relationship between the roots of plants and fungi. The term mycorrhiza literally means root fungus, but in the broad sense of the term, the interaction does not always occur only with the roots of plants, a mycorrhizal relationship also includes plants that do not have roots, such as Psilotum and bryophytes (mosses and liverworts). Although I have defined this term on several occasions, I don’t believe that I’ve ever mentioned why this relationship is so important.
A common impression, among non-botanist is if plants are in an area with rich soil and have enough water and sunshine that they will grow well. Although this may be true, this is usually not the case. In fact, this is rarely true in nature. Just as there is a lot happening in the recycling of nutrients, in the soil, there is also a lot going on with respect to interaction of plant roots with other microorganisms. In the case of mycorrhizal relationships, we are actually talking about a number of different types of relationships. Another words, there are different categories of mycorrhizae. However, in the most common types, the fungus will usually receive carbohydrates of some sort from the plant and there will be enhancement of mineral transport to the plant. You should recall that in order for plants to grow normally, they require certain essential elements, and I will not review those elements at this time since knowing what they are is really not essential in understanding the concept of mycorrhizae. Generally, in nature, the soil composition is often deficient in one to several essential elements that are required by plants, and it is thought that because the mycelium of the fungus is more extensive than even the roots of the host plant, in the soil, the fungus is able to enhance nutrient uptake for the plant. Ironically, it is in nutrient rich soil, such as agricultural soil, that plant sometimes do not grow better with a mycorrhizal fungus, but instead the plant may even reject the fungus. In addition to the enhanced nutrient uptake, different categories of mycorrhizae may protect roots against pathogens, produce plant hormones and translocate carbohydrates between plants. However, there are some generalizations that can be made, concerning mycorrhizae:

•  Mycorrhiza infection area occurs only on the smallest order of secondary roots. These are the root tips that are still growing, elongating and increasing in girth. So we are talking about just a very small part of the root system of a plant which will be infected by the mycorrhizal fungus. This makes a great deal of sense since this is the only part of the root system that will absorb water and minerals. However, as I just mentioned, the fungus has a much more extensive growth in the soil.

• In all mycorrhizae only the cortical cells of the root are invaded by the fungus. This is the area of the root between the epidermis and the vascular tissue of the root. If we look at the cross section of a young root, it would be here where these large somewhat circular cells are.
  
  

  Cross section of a root: Outer most layer is the mantle layer of mycelium. The round cells are the cortical cells and if you look closely, where the fungus mycelium is growing between the cortical cells, but not penetrating them, is the Hartig net. From http://sciweb.nybg.org/science2/images/larix_amanita.jpg

• Occurs in practically all plants with the exception of the Brassicaceae; The Crucifer Family; Chenopodiaceae, The Goosefoot Family; Cyperaceae; The Sedge Family and in aquatic plants. All other families form mycorrhizae.

•  It is believed that for many plants that usually form mycorrhizae, they would be unable to survive in their natural habitat without this symbiotic relationship. This has been demonstrated to be true for numerous plants.

More than just being relevant to the world’s present flora and its practical applications in agriculture and forestry, it has been claimed by some mycorrhizal researchers that without mycorrhizae, terrestrial plants would never have been able to establish themselves on land. It has been postulated, by mycorrhizal researchers, that long before plants became established in the terrestrial environment, fungi, as mycorrhizal partners, were already associated with plants, in the aquatic environment, and that it was the mycorrhizal fungi that made possible the plant’s conquest of the terrestrial environment.
Types of mycorrhizae recognized (can be divided into three categories):

1. Ectomycorrhizae: characterized by forming an external sheath  of mycelium around the root tips and hyphal cells do not penetrate the cell walls (intercellular) although they may go between cells in the cortex (Hartig Net).
2. Endomycorrhizae: characterized by the lack of an external sheath around root tip and the penetration of cortical cells (intracellular) by the fungus mycelium.
3. Ectendomycorrhizae: mycorrhizal type that seems to be intermediate between ecto and endomycorrhizae. Mycelium sheath around root is reduced, or may even be absent, but Hartig Net is usually well developed as in ectomycorrhizae, but the hyphal cells may penetrate the cortical cells as in endomycorrhizae. However, because of similarities to ectomycorrhizae, they will not specifically be considered here.

Description of mycorrhizae types
Ectomycorrhizae
This category of mycorrhiza is very uniform in appearance, and biologically identical despite having literally thousands of different species fungi, in the Ascomycota and Basidiomycota. For this reason, it is not subdivided into further subcategories as in endomycorrhizae. It is referred to as "ecto-" because the fungal symbiont does not invade the cell protoplasm. However, the fungus does form a thick sheath around the root tip and mycelium also grows between the cells of the cortex forming the so-called Hartig net. The infected roots are very distinctive, forming short, paired, branches.
While there are a large number of fungi that are ectomycorrhizae, plants that have ectomycorrhizae are restricted to only a few families of plants, and these plants are always trees. They are also more common in temperate regions than in the tropics. This is one reason why there are far fewer mushrooms here in Hawai‘i than on the mainland. This type of mycorrhiza is very important in forestry because its association with trees.
In this type of mycorrhiza, the fungal sheath, that forms around the secondary root tips, accumulate minerals from the decomposing litter, before they are able to pass into the deeper mineral layers of the soil where they would be unavailable to the roots. Thus, mycorrhizal fungi are also decomposers as well. Fungus does obtain simple carbohydrates that are produced by the plant, but not used by the plant. So it appears that these carbohydrates may be produced by the plant specifically for the fungus since they are not utilized by the plant. Fungi involved are members of the Basidiomycota and the Ascomycota. Also, they are usually species that form large fruitbodies, such as mushrooms, puffballs, truffles, etc. so that fruitbodies from these groups of fungi that grow in soil are usually ectomycorrhizae rather than being saprobes. From many years of observations, consistent association could be seen of certain species of trees with certain species of fungi that produce fruitbodies. This type of mycorrhiza was discovered first for this reason.
Although we can grow the mycelium of many ectomycorrhizae fungi in an artificial medium, e.g. agar, they often grow slowly and not as well as in soil. It has been demonstrated that unknown growth factors exuded by the roots seems to stimulate mycelial growth. There is undoubtedly many more factors involved, with regards to growth of the fungi, that are yet unknown. Formation of fruiting bodies in artificial media also has never been accomplished. This was the reason why "cultivation" of truffles, e.g. Tuber melanosporum, which form mycorrhizae, requires planting of the host trees that have been inoculated with the fungus in order to obtain fruitbodies.
The ectomycorrhizal root that is formed has a morphology that is distinct from that of uninfected roots. One distinctive characteristic of the infected root tips is that they lack root hairs. This is unusual because root hairs are normally presence, in abundance, in the young root. This morphology is in part due to the fungus secreting auxin, a plant hormone, that acts upon the root development and in the case of gymnosperms, form, thick dichotomous branches. Branching of the root system will differ with different plant families.

Left Image: Ectomycorrhiza of Amanita and Pinus root, from http://mycorrhizas.info/ecm/pine-Amanita.jpg. Right Image: Figure of section through root, showing external mantle of hyphae and Hartig net.

Cross section of arbutoid mycorrhiza, showing external mantle of hyphae and Hartig net, from http://www.mykorhizy.webpark.cz/ArM4.jpg

The ectendomycorrhizae morphology is like that of the ectomycorrhizae, i.e. presence of Hartig Net, same host range, etc. The only real morphological difference is that the host roots cells are penetrated by hyphal cell of fungus. Also, the fungi involved have not been identified.
Economic Relevance
Plants that are involved in ectomycorrhizae are always trees and are found only in a few families. They include the Betulaceae, Beeches and Alders, Casuarinaceae, Ironwood, Fagaceae Oaks, Myrtaceae Eucalyptus and Pinaceae Pines, Douglas Firs, Firs, etc.. Most of these are utilized as a source of lumber, and in the case of the Pine family, millions of trees are used annually, this time of year, as Christmas trees. When planting these trees, it is a routine practice, in forestry, to inoculate the seedling with a mycorrhizal fungus.
This group of mycorrhiza have also been tested as a means of resisting fungal, root pathogens. It was reasoned that if the fungal sheath of the ectomycorrhizal fungus is covering the root tips, fungal root pathogens would be unable to gain entry into the root system of the host.
Endomycorrhizae
Although far less conspicuous because they do not produce large fruiting bodies, such as mushrooms, this category of mycorrhiza is far more common than the ectomycorrhizal type. Generally, it can be said that plants that do not form ectomycorrhizae will be the ones that form endomycorrhizae. However, because of the absence of a macroscopic of macroscopic fruitbodies, the presence of endomycorrhizae is more difficult to demonstrate. Because of the lack of visibility, this group was considered to be rare until a method was devised that could readily detect such fungi in the soil and demonstrate that they are in fact very common.
There are several categories of endomycorrhizae. The only common feature that they all share is that the mycelium of the fungal symbiont will gain entry into the host, root cells by cellulolytic enzymes. Unlike the ectomycorrhizae, roots which are infected with mycorrhizal fungi do not differ morphologically from those that are not infected, i.e. root hairs are present and sheath is not formed around the root tip. However, the type of association that is formed between the host and fungus vary a great deal in the different categories of endomycorrhizae.
Arbuscular Mycorrhizae 
This category of mycorrhiza can be found throughout the world, but more abundant in the tropics than in temperate regions, and is associated with more plants than any of the other categories of mycorrhizae. The name of this type of mycorrhizae comes from the distinct structures called arbuscules that can be seen inside the cells of infected roots. These structures can be recognized by their branched tree-like appearance. Another structure that can be frequently observed are the rounded vesicles. The vesicles and arbuscules contain the stored minerals that are needed by the plant. These structures lyse in the root cells and in this way the minerals become available to the plant. There is also extensive mycelium in the soil, but do not appear to be organized in any fashion. 

Vesicles in roots cells of Sesbania sp. Note some vesicles have been displaced from cells due to preparation of slide. Courtesy of Drs. Richard Koske and Jane Gemma, University of Rhode Island.	Arbuscule in root cell. Arbuscules are characterized by their tree-like appearance. Courtesy of Drs. Richard Koske and Jane Gemma, University of Rhode Island.

The group of fungi involved is always a member of the Zygomycota. If you look at the mycelium, from the infected roots, under the microscope the mycelium can be seen to be coenocytic (=nonseptate), which is as you would expect from fungi in this division.
There are only a few genera of fungi involved, but because of the lack of specificity of these genera to specific host plants, they have been found to have largest host range of any mycorrhizal group.
The VAM fungi normally produce assorted types of spores which can be used in the identification of these fungi, i.e. zygospores, chlamydospores and azygospores. It was once thought that these fungi were nothing more than a rare curiosity. However, this was only because a technique was needed, which could more efficiently find VAM spores, than by simply sifting through the soil. Once this technique was found, this type of mycorrhiza was found to be the most common in nature.
It is because VAM have a broad host range they were once considered to be a future tool in agriculture, i.e. fertilizer substitute. However, because these fungi cannot be grown in the absence of a host plant, individual inoculations would have to be done for each plant. This would be impractical for any grains grown as well as for most crops, but have been utilized in planting of fruit trees which are planted individually. Recently, experiments with VAM fungi have been tried at The National Tropical Botanical Garden (NTBG) in an effort to save endangered species of native Hawaiian plants. There are a number of native plants which are endangered, in which attempts at growing them from seeds and cuttings at NTBG have not been very good. A few years ago, while Drs. Richard Koske and Jane Gemma, two University of Rhode Island mycologists, who are normally given work space at NTBG while they are doing their research on Hawaiian VAM fungi, suggested that perhaps the absence of VAM fungi was the reason why the plants were dying or growing very poorly. While inoculation of VAM fungi did greatly improve the survival of the young plants, it would not be the whole answer to their problems. Some species of native Hawaiian plants that were given inoculated with and without VAM fungi are shown on Figs. 5-7.

Two Chamaesyce plants. Left plant with and right without mycorrhiza.

Two Hibiscus plants. Left plant without and right with mycorrhiza, respectively.	Two Lysimachia plants. Left plant without and right with mycorrhiza, respectively.

Orchid Mycorrhizae
Orchid mycorrhiza is endomycorrhizal and have fungal partners that are saprotrophic or pathogenic species of Basidiomycota, but a some are ectomycorrhizae, e.g. Russula. All orchids must form mycorrhizae. In most plants, the seed contains a food supply that will feed the embryo, until germination occurs, at which time the plant becomes photosynthetic and can produce its own food. However, orchid seeds are very minute and contain a very small food reserve for the embryo. This food supply is usually depleted by the time that the first few cell divisions of the embryo has occurred. During this critical period, the fungal symbiont colonizes the plant shortly after seed germination and form characteristic, coiled hyphae within the cortical cells of the root. The hyphae in the host cells collapse or are digested by the host that will supply the embryo with its carbon source and vitamins until it is able to photosynthesize. Unlike other mycorrhizal fungi, orchid mycorrhizal fungi can also digest organic materials, from the surrounding environment of the orchid, into glucose, ribose and other simple carbohydrate and these nutrients are translocated into the orchid to support their growth.
The relationships that orchid species have with the mycorrhizal fungi are variable and is dependent on their nutritional needs. Those orchids that are photosynthetic still retain their fungal partners, but it is not clear as to what role it is playing. However, the achlorophyllous orchids will require it even as adult plants. In these species the associate fungus forms a tripartate relationship, where the fungus also forms a relationship with a photosynthetic plant and channel its nutrient to the orchid. The fungus will also supply both plants with inorganic nutrients. 
Ericaceous Mycorrhizae
The mycorrhiza formed in this group is between fungi in the Ascomycota, and more rarely in the Deuteromycota, and species in the families Epacridaceae, Ericaceae and Pyrolaceae. Three subcategories are recognized, arbutoid, ericoid and monotropoid. We will briefly cover the latter two groups.

Arbutoid Mycorrhiza
This group forms associations with plants that are trees and shrubs that belong to the genera Arbutus (madrone), Arctostaphylos (manzanita) and Arctous alpinus (mountain bearberry). They have characteristics that are both ecto- and endo-mycorrhizae: There is a formation of an external mantle of mycelium that forms a hartig's net, as in ectomycorrhiza, but intracelllar penetration of cortical cells occurs as in endomycorrhiza. Fungi forming this association are members of the Basidiomycota.

Ericoid Mycorrhizae
Plants having this group of mycorrhiza are commonly found in acidic, peatland soils and include members of genera Calluna (heather), Rhododendron, Azaleas and Vaccinium (blueberries), of the family Ericaceae. Ericoid mycorrhizae have evolved in association with plants that are continually stressed by factors within the soil. The soil is typically extremely acid, peatland soil, low in available minerals because mineralization is inhibited. Plants with ericoid mycorrhizae seem to have a high tolerance to these stresses and there is good reason to believe that this is related to the presence of the mycorrhizal fungus and that the survival of the host is dependent upon the fungus.
The mycorrhizal association is most similar to that of an endomycorrhiza because fungus growth is extensive in the root cortex. The fungus penetrates the cell wall and invaginates plasmalemma and is filled with coiled hyphae, like those in orchid mycorrhizae. No mantle is formed. Infected cells are fully packed with fungal hyphae.  Fungus species are mostly members of the Ascomycota, in the genus Hymenoscyphus.

Cross section of ericoid root, showing coiled hyphae. From http://www.mykorhizy.webpark.cz/ErM5.jpg (c) M. Vohnik.

The host cell dies as the association disintegrates, thereby restricting the functional life, i.e., nutrient absorption of these epidermal cells to the period prior to breakdown of the infected cell.  
Monotropoid Mycorrhizae
One of the characteristics that we normally attribute to plants is that they have chlorophyll and can produce their own food through the process of photosynthesis. However, this is not true of all plants. The Monotropaceae and Pyrolaceae are two families of plants that are achlorophyllous. Thus, plants in these families are more dependent upon their mycorrhizal partners than plants which can carry out photosynthesis.

Monotropoid plants: Monotropa uniflora (left) from http://mycorrhizas.info/intro/Monotropa1.jpg and Sarcodes sanguinea (right).

The means by which food is obtained by these plants is the same as in achlorophyllous orchids. However, morphologically, they are very different. The achlorophyllous host has mycorrhizae roots that appear to be formed by an ectomycorrhizal fungus, but the epidermal and outer cortical cells are penetrated by the fungus, as in endomycorrhizal plants. The fungus also forms an ectomycorrhizal relationship with a tree which is capable of photosynthesis. So, as in the case of the epiphytic orchids, the photosynthetic tree indirectly provides carbohydrates to these achlorophyllous plants, as well as to the fungus. Both hosts probably obtain their mineral requirements through the fungus.

Lichens
The most well known example of a symbiosis between fungi and plants is the lichen, if you will allow me to include algae as plants.  The concept of what constitutes a lichen has broaden significantly in the last 25 years to include some species of mushrooms, slime molds, and some members of the Zygomycota. However, we will discuss lichens in the traditional sense, as an association between a fungus and an alga that develops into a unique morphological form that is distinct from either partner. The fungus component of the lichen is referred to as the mycobiont and the alga is the phycobiont. Because the morphology of lichen species was so distinct, they were once thought to be genetically autonomous until the Swiss Botanist Simon Schwendener described their dual nature in 1868. Prior to that time, because of the morphology of many of the "leafy" species of lichens, they were considered to be related to bryophytes, i.e., mosses and liverworts. Although, lichens are now known to be composite organisms, they are still named for the fungus part of the association since that is the prominent part of the lichen thallus. A thallus is an old botanical term used to describe "plants" that do not have leaves, stems and roots, and its origin goes back to a time when only two kingdoms were recognized in classifying organisms, i.e., organisms were either plants or animals. Prior to 1969, organisms such as algae, bacteria and fungi, were included in the plant kingdom. In 1969, Whitaker, proposed a five kingdom system that was used for many years, but may soon also become outdated. Although, this term is antiquated, it is still used to describe the "bodies" of algae, fungi and of course lichens. The only group of plants, in which we still use the term thallus, to refer to the plant body, are the bryophytes.
Although the lichen thallus is composed of an algal and fungal component, lichens are not studied in mycology or phycology (that part of botany that studies algae). Instead, they are studied in their own discipline, lichenology. There are relatively few lichen researchers. Of these most are systematists. As a result, there are still some basic questions concerning this symbiosis that are unanswered or at least up for debate. One of the most basic questions, that has been asked since the discovery of the lichen symbiosis, concerns whether lichens represent a true mutualistic symbiosis or nothing more than a variation of a host-parasite relationship. There is evidence supporting both sides. That it represented a mutualistic symbiosis, in which the alga was believed to contribute the food supply through photosynthesis, and the fungus protected the alga from desiccation, harmful solar radiation and provided the alga with water and inorganic nutrients, was postulated by Beatrix Potter, the writer and illustrator of Peter Rabbit, soon after Schwendener had determined the true nature of the lichen thallus. In order to understand both sides of the issue, lets look at the morphology and anatomy of lichens.
The Lichen Thallus
In the traditional sense of lichens, their thallus can be artificially divided into four forms: foliose, crustose and fruticose.
Foliose Lichens
Lichen thallus which is generally "leaf-like", in appearance and attached to the substrate at various points by root-like structures called rhizines. Because of their loose attachment, they can easily be removed. These are the lichens which can generally be mistaken for bryophytes, specifically liverworts. It is possible, or even probable, that herbaria still contain lichens that have been mistakenly identified as liverworts. If we look at these a foliose lichen in longitudinal section, from top to bottom, we would be able to distinguished the following layers:

• Upper Cortex: Often composed of tightly interwoven mycelium, which gives it a cellular appearance. This cellular appearance is referred to as pseudoparenchymatous.

•  Algal Layer: Composed of interwoven hyphae with the host algal cells. This is the ideal location for the algal cells. Beneath the upper cortex so that it receives the optimal amount of solar radiation, for photosynthesis, but not direct solar radiation which would be harmful.

•  Medullary Layer: Composed of loosely interwoven mycelium. Layer is entirely fungal.

• Lower Cortex: Usually same composition as the upper cortex and attached to the substrate by root-like structures called rhizines. The rhizines are entirely fungal, in origin, and serve to anchor it to the substrate. Thus, the foliose lichens also have what is referred to as a dorsiventral thallus, i.e. a distinct upper and lower surface.
  
  

  Sectional views, illustrating how the three thallus types of lichens differ. From http://www.earthlife.net/lichens/lichen.html

Foliose lichens are typically leafy in appearance and is attached to their substrate by rhizines, on their lower surface. From http://www.fs.fed.us/wildflowers/interesting/lichens/gallery/foliose/images /lobaria_pulmonaria_dry.jpg

Crustose Lichens
Lichen thallus which is very thin and flattened against the substrate. The entire lower surface is attached to the substrate. These lichens are so thin that they often appear to be part of the substrate on which they are growing. The following link shows an image of several lichen thalli. Crustose species that are brightly colored often give the substrate a "spray-painted" appearance. The thallus has the upper cortex, algal and medullary layers in common with the foliose lichens, but does not have a lower cortex. The medullary layer attached directly to the substrate and the margins are attached by the upper cortex.

Crustose lichen thalli. This type of lichen is tightly flattened to its substrate and the entire lower surface (medulla) is attached, making it impossible to remove the thallus from its substrate.

Fruticose Lichens
The thallus is often composed of pendulous ("hair-like) or less commonly upright branches (finger-like). The thallus is attached at a single point by a holdfast. In cross section, the thallus can usually be seen to be radially symmetrical, i.e. does not have a top and bottom. The layers that can be recognized are the cortex, algal layer, medullary layer, and in some species the center has a "cord" which is composed of tightly interwoven mycelium. Other species have a hollow center that lack this central cord.

Fructicose lichen thallus is attached to its substrate at a single point, but finding that point is not that easy!

Biology of Lichens
In looking at the anatomy of the lichen, it is obvious that there is interaction between the phycobiont and mycobiont, but what kind of interaction is occurring. One school of thou0ght is that the alga produces the food material and that the fungus protects alga from desiccation, high light intensities, mechanical injuries and provides it with water and minerals. This is the reasoning that many introductory text books have adopted and they define a lichen as a mutualistic symbiosis. However, in studies that have been done that examines the alga-fungus interface, it can be clearly seen that haustoria, specialized feeding structures present in parasitic fungi, penetrate the alga cells. Thus, many lichenologist have defined this relationship as a controlled form of parasitism. Obviously, the story doesn’t end there. There is more evidence and I would like to go over some of these.

Illustration of haustoria penetrating algal cells give evidence that the lichen symbiosis is really a controlled form of parasitism. From http://www.yosemite.ca.us/library/yosemite_nature_notes/47/3/images/lichen_2.png

If we think about fungi and algae in general, we know that they are normally going to be found in a moist to wet environment where they are not receiving direct solar radiation. Conditions outside these parameters will usually be fatal for most species of fungi and algae. However, lichens occur all over the world. They even occur in arctic and hot, dry desert areas where few organisms can live or even survive. Thus, the lichen is able to exploit habitats that few other organisms are able to utilize that seem likely to be the result of their mutualistic, symbiotic relationship. 
Another experiment that demonstrates that lichens represent a mutualistic symbiotic relationship was carried out in the laboratory by Vernon Ahmadjian. Although, it is not difficult to separate the myco- and phycobiont components of the lichen, and grow them separately in the laboratory, putting the component back together is another story. For many years it was not possible to put the two together to reform the lichen thallus. The reason for this was the method that was used in attempting to reform the lichen thallus. The reformation of the lichen thallus was, for many years, attempted in a growth medium that would contain nutrients that were favorable for growth by both of the myco- and/or phycobiont. These types of media did not work. Ahmadjian reasoned that if the lichen represents a symbiosis, the reason that the relationship formed was because, in nature, neither one could obtain all the nutrients necessary for survival and that only after the two organisms interacted was it possible. Thus, Ahmadjian created a minimal medium, which would not support the growth of either the myco- or phycobiont, and inoculated them into that medium. This method successfully reformed the lichen thallus, in the laboratory, for the first time.
Although, it would appear that there is a great deal more evidence supporting the lichen thallus as a product of mutualistic symbiosis, there are still many who believe that the relationship is that of a balance parasitism that favors the mycobiont.
 A Few Words on The Lichen Component
 Although there are approximately 13,500 species of lichens recognized, the number of taxonomic groups of fungi and algae that produce the lichen thallus are few.
Mycobionts
In the traditional sense of lichens, which is how we are defining lichens, the fungal components are always in the Ascomycota, specifically in those groups that form their asci and ascospores in fruiting bodies. The fungi involved in the lichen symbiosis are never found to be free-living in nature.
Phycobiont
Regardless of whether we are using the traditional or expanded definition of lichens, the algae involved in the association are the same. Of all the different species of algae that are known, only the divisions Chlorophyta ("green" algae) and Cyanophyta ("blue-green" algae or Cyanobacteria ) are involved in lichen formation. The latter are actually bacteria rather than algae although they were classified as such once upon a time. Furthermore, within these divisions, only a few genera are involved in the lichen symbiosis. Some genera, such as Trebouxia, are known to only occur in lichens and are not free-living, but there are also examples that are free-living.
Economic Relevance
Economically, lichens have little significance. Perhaps this is why there is so little interest in this group of organisms. One way that they have been utilized is in the extraction of blue, red, brown or yellow dyes in the garment industry. Also, the indicator pigments used in litmus paper was also derived from lichens. Previously, we briefly mentioned lichens as a source of pharmaceutical compounds. You can include some "folk" remedies in this category as well. They are also used in the cosmetic industry, in the making of perfumes and essential. Finally, some species have been used as food. One species, Lecanora esculenta, is a species that grows in the mountains near Israel and are typically blown free from their substrate. Desert tribes grind up the lichen, dry it and mix it with dry meal to form a flour. It is postulated that this is the species lichen that is referred to as "Manna from Heaven" when Moses led the Hebrews across the desert during biblical time. One species, Cladonia rangiferina (reindeer moss), is fed upon by reindeers and cattle. This has led to the discovery that lichens readily absorb radioactive elements. After open-air, atomic testing, both Alaskan Eskimos and Scandinavian Laplanders were found to have high levels of radioactive contamination, which they had absorbed from eating reindeer, which in turn ate lichens.
Other Significant Uses for Lichens
Lichens are conspicuously absent in and surrounding cities because many species are sensitive to pollution, especially to sulfur dioxide and flourine, which are common pollutants. For this reason, they have been commonly used as indicators of pollutants. In urban areas, where lichen surveys have been carried out, the absence of certain indicator species is used as early warnings of decrease in air quality.
Lichens also play a very significant role in nature. They are the pioneers in rocky substrates, where there is no soil. Lichens break down the rocky substrate into soil and their decomposing thallus fertilize the newly produced soil, making it possible for the plant habitation.
Reproduction
Reproduction of the lichen is entirely asexual. It may occur by soredia (sing.: soredium), spore-like structures, composed of alga cells and hyphae that are formed from the algal layer and become exposed when the cortex ruptures. This is best seen in a sectioned lichen. The other means of asexual reproduction is by isidia (sing.: isidium), columnar to swollen structures that are part of the lichen thallus that are likely to break off to form new lichens.  Ascospores and conidia also form, but these will only reproduce the fungus. It is assumed that these structures will come in contact with a suitable algal host and resynthesis the lichen thallus. However, the latter are not thought to be significant in lichen reproduction.

From left to right: Clusters of soralia, two soredia, as seen through the microscope, isidia and section through soredium. From http://waynesword.palomar.edu/

Terms for Symbiosis:

 Algal Layer: The part of the lichen that is composed of interwoven hyphae with the host algal cells. This is the ideal location for the algal cells. Beneath the upper cortex so that it receives the optimal amount of solar radiation, for photosynthesis, but not direct solar radiation which would be harmful.

Arbuscular Mycorrhizae: A category of Endomycorrhizae characterized by the production of globose structures, called vesicles, and branched, tree-like structures called arbuscules, in the cortex of the root cells. The root cells lyse these structures and receive the minerals from the fungus, in this matter.

Commensalism: An association in which one species, usually the smaller, benefits from the association while the other species seems to be unaffected. Such relationships are usually not obligate, and neither species will be adversely affected if the relationship does not occur.

Crustose Lichens: Lichen that is very thin and flattened against the substrate. This type of lichen lacks a lower cortex and is attached to its substrate by the medullary layer. Thus, these lichens are very thin and often appear to be part of the substrate on which they are growing.

Ectomycorrhizae: characterized by forming an external sheath of mycelium around the root tips and between the cells of the cortex, i.e., they do not penetrate the root cells.

Endomycorrhizae: characterized by the lack of an external sheath around root tip and the penetration of cortical cells by the fungus mycelium.

Foliose Lichens: Lichens that have a leafy appearance and are attached to their substrate by structures called rhizines.

Fruticose Lichens: Lichens that are often composed of pendulous ("hair-like) or less commonly upright branches (finger-like) and attached at a single point. In cross section, the thallus can usually be seen to be rounded, i.e. does not have a top and bottom. Thus, there is a single cortex layer.

Haustoria: specialized feeding structures present in parasitic fungi by which they penetrate the host cells and obtain nutrient.

Isidia: Asexual reproductive structures found on lichens that are upright, cylindrical to swollen in appearance. Structures break off and can form another lichen.

Lichen: The symbiotic relationship between a fungus and an alga that develops into a unique morphological form that is distinct from either partner.

Mycobiont: The fungal component of the lichen. In the traditional sense, the fungus is a member of the Ascomycota.

Mycorrhiza (pl.: mycorrhizae): The symbiotic relationship between the roots of plants and fungi. The term mycorrhiza literally means root fungus, but in the broad sense of the term, the interaction does not always occur only with the roots of plants, a mycorrhizal relationship also includes plants that do not have roots, such as and bryophytes (mosses and liverworts).

Parasitism: A relationship in which one species (parasite) is obligately dependent upon another organism (host) for its food and shelter.

Phoresy: A loose association where a usually, smaller organism is using a larger one as a transport host. Normally used in references to arthropods and fishes.

Phycobiont: The algal component of the lichen. The alga is usually a member of the Chlorophyta or Cyanobacteria.

Rhizines: Structures found on the lower cortex of foliose lichens and functions in anchoring the lichen to the substrate.

Soredia: Asexual reproductive structures found on lichens that form as a result of the rupture of the cortex, exposing the algal layer, which break into spore-like structures composed of a few algal cells and hyphae that are dispersed by wind.

Upper Cortex: The upper surface of the lichen, often composed of tightly interwoven mycelium, which gives it a cellular appearance.

Questions of Interest:

1. What are the plants that are involved in ectomycorrhizae formation?
2. What groups of fungi would you expect to find in ectomycorrhizae formation?
3. Name and describe the different categories of endomycorrhizae.
4. Generally, how does an ectomycorrhiza differ from one that is an endomycorrhiza?
5. Lichens can be divided into artificial groups, based on the type of thallus that they produce, name these different groups and describe the characteristic of each.
6. What evidence is there that lichens actually represent a parasitic relationship between a parasitic fungus and its algal host?
7. What evidence is there that demonstrates that lichens are indeed the result of a mutualistic symbiotic relationship?
8. What phylum, of fungi, does the mycobiont of lichens typically belong to?
9. What groups, of algae, does the phycobiont of lichens belong?
10. Describe how lichens reproduce.