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Plants, Fungi and the Underground Internet

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A photographic montage of different types of fungus.

Just as no man is an island, no organism in this world lives alone. Even as the environment makes an impact upon each living thing, so do all living organisms interact with their environment and with one another? The sharing of information is what keeps nature's gene pool from stagnating - organisms trading DNA, exchanging traits that allow them to survive better in a world that may or may not be meant for them. And yet there are also organisms whose trade is not limited to information but also food; not only to members of its own species, but also to members of other families, or other kingdoms even. Mankind may have created telecommunication and the Internet, but it is the humble plants and fungi that are the true inventors of networking.

A Brief History

The great potato blight of 1845 is an historic event, not only because of the tragedy that it caused - the death of a million Irish peasants by starvation in the wake of the destruction of Ireland's entire potato crops - but because it paved the way for the discovery of an amazing phenomenon in nature.

Throughout the course of this disaster, scientists sought an explanation for the devastation of potato crops, and yet met dead ends at every turning - until eight years later when a young German biologist named Anton de Bary established how fungal spores penetrated plant leaves and propagated in their tissues, ultimately causing death to their host.

Anton de Bary had, as a child, been driven to blaze his own path in the study of plants and their diseases by the horrors of the devastating potato blight. His intense studies and experimentation would later lay the foundation for mycology1, back then a relatively new area of research. With his publication of Understanding Plant Disease in 1853 and his growing reputation as an expert in the field, the hard-pressed English government and the Royal Agricultural Society of England brought de Bary in to shed light upon the role of fungi in the potato blight.

The traditional farmers had, for a long time, believed that the common barberry plant harboured whatever agent it was that caused blight. Unlike his peers, who had dismissed this knowledge as unfounded, de Bary took the claim seriously and, through a series of elegant explanations, demonstrated how the blight agent, which he named Phytophthora infestans, was in fact harboured by the plant.

Had he stopped there, de Bary would have become renowned simply as an expert of plant pathology. However, he took mycology a step further and went on to demonstrate that the relationship between plants and fungi did not stop at parasitism, but that they were also able to live in a cohabitating relationship that benefited both partners2. With this new insight, scientists came to the realisation that many of the phenomena they had dismissed as quirks of nature might be this unusual plant-fungi liaison that de Bary had described.

Today, science has unravelled the mysteries behind the delicate relationship between plants and fungi, and we now know what only a hundred years ago was considered improbable - that far from being simply greedy parasites, a fungus can also be a plant's best friend.

First Of All, What Are Fungi?

Fungi are a diverse group of eukaryotic microorganisms - organisms who's DNA are encapsulated by nuclei - that comprises moulds, yeasts and mushrooms3. Their habitats are varied - there are fungi that live in aquatic environments, be it freshwater or marine, and then there are also those that have terrestrial habitats. All fungi are chemoorganotrophs, which is to say that they lack the necessary equipment (namely chlorophyll and the photosynthesis system) to synthesise their own food, and must therefore derive their nutrition from organic matter around them. A fair number of fungi are parasites of plants, and are in fact the cause of many economically significant diseases of crops. There are also those that are parasites of animals including humans, although their role as animal pathogens is vastly overshadowed by bacteria and viruses.

Mycorrhizae

It concerns the fact that certain species of trees do not regularly feed in the soil, but that they are everywhere in their whole root system in symbiosis with a fungus mycelium that serves them like a foster-mother and takes charge for the whole feeding of the tree from the soil...
- Albert Bernhard Frank, 1885.

If you take a stroll through the park one day and happen to see a mushroom growing near a pine tree, chances are that the two are not merely neighbours; they are partners in life.

Most plants are associated or bonded to fungi in some way. Unlike parasitism, however, this unlikely marriage between plants and fungi is a happy one that benefits both partners. Many of these interactions occur at the root, beneath the soil and hidden from the eyes of the observer, and yet these fungi hold the key to the dominion of plants on the land surface of earth.

The relationship between plant roots and fungi is called mycorrhiza, involving up to 95% of the terrestrial plant population, about 400 species of which lack chlorophyll, and about 5,000 species of fungi from various orders (Zygomycota, Basidiomycota, Ascomycota).

Types of Mycorrhizal Relationships

Ectomycorrhiza is the relationship between plant root and fungi whereby the fungus partner forms a sheath around the outside of the root; its hyphae4 only extend into the root's cortex tissue, but not into the cells. This type of relationship is common among a number of species of trees and shrubs that are commonly found in cold and temperate countries (including pines, beeches and oaks), or tropical regions that are nutrient-deficient, and commonly involves mushrooms and higher fungi.

Conversely, in an endomycorrhiza relationship, part of the fungal partner actually dwells within the cells of the plant root, while the other part spreads out into the soil. The plants are considered obligatory mycotrophs5, but are usually able to survive without their fungal partners on organic substrates. Vesicular-arbuscular mycorrhiza (VAM), which closely resembles ectomycorrhiza in that the fungal partner penetrates no further than the root cortex, is perhaps the most common, and there is not a single plant family in which this relationship has not been detected - all members, be it fungi or plant, are obligate symbionts. It is more distinct in plants inhabiting dry places or eroded soil, and involves aseptate6 fungi. Of all mycorrhizae, VAM is symbiosis in its most primitive form.

Ectendo-, arbutoid- and monotropoid mycorrhiza are variants of ectomycorrhiza. The hyphae of the fungal partner typically penetrate the epidermal layer of the plant root. Ectendomycorrhiza are in fact cases where an ectomycorrhizal relationship becomes endomycorrhizal, and is a common phenomenon among flowering plants and woody plants lacking true vascular systems.

Orchid mycorrhizas belong to a class of their own, consisting of coils of hyphae within the root or stems of orchids. Because an orchid seed is little more than an embryo in a shell, partnership with the right fungal partner is crucial to its germination. Young seedlings and chlorophyll-lacking mature plants are entirely dependent on their fungal partners for survival.

Ericoid mycorrhizas are relationships between fungi and plants of the order Ericales and Australian members of Epacridaceae. The hyphae of the fungal partners penetrate the outer cells of the plants narrow 'hair roots'.

Finding the Right Match Through a Matchmaker

For a mycorrhizal relationship to work out, both the plant and fungus partner must first find each other via signal exchange. A third party - Mycorrhization Helper Bacteria (MHB), often mediates the meeting of these partners. Germinating fungi first interact with bacterial populations in the soil, and the outcome of this interaction may or may not lead to the formation of the mycorrhiza partnership. Indeed, experiments with the fungus Laccaria laccata and MHB has shown that these helper bacteria can be somewhat picky, allowing only mycorrhizal fungi of certain species to form fruitful partnerships with the Douglas fir tree.

If there is a positive relationship between the helper bacteria and the fungus, the plant-fungus interaction tentatively begins. Chemical signals in the form of iso/flavonoids and phenolics issued by the plant root stimulate germination of fungal spores and activation of their hyphae. In return the fungus will respond with its own chemical signals. When the two organisms have recognized one another, the fungus will proceed to penetrate the root - an action that causes injury and provokes a defence response in the plant in the form of chemicals that are inhibitory or injurious to the fungus. If the fungus is compatible however, the response will be weak7, and a mycorrhizal relationship will be established.

With this acceptance, the fungus is now free to colonise and develop extensively inside and around the root, and the partnership is sealed.

How a Mycorrhizal Relationship Profits Both Partners

  1. Acquisition of Nutrients and Growth Enhancement

    The importance of mycorrhizal relationships is the acquisition of raw material. For example, phosphate, which is the key component in the energy-storing ATP8 molecule as well as a component of the cell membrane, is largely found bound to soil particles in the ground and are therefore inaccessible to plants. Because it is insoluble, phosphate from fertilizers will remain on the topsoil indefinitely unless mechanically removed. It is therefore the duty of the fungal partner, whose hyphae are able to spread further and penetrate places inaccessible to the plant root, to complement and enhance ability of the plant root to uptake these crucial compounds and nutrients as well as water (which would be an energy-exhaustive process for the plant if it were to go it alone by developing its own adequately complex root system9). These fungal partners are able not to only forage for food, but even dissolve soil minerals and break down recalcitrant organic compounds into substrate that the plant can use. In addition, phytohormones secreted by fungal partners have also been found to enhance plant growth. The plant, on its part, nourishes the fungal partner with food synthesized through photosynthesis.

    In the strange case of endomycorrhiza, the plant partners are able to survive quite well without their fungal counterparts on inorganic media; however, they are unable to utilize organic compounds on their own, and their growth are in fact impeded by addition of organic matter because chemicals secreted by the root combine with them to form toxins; utilization of organic substances is made possible by the fungal partner. In fact, these fungal partners have been found to enhance plant growth - the plant Calluna's primary vegetative point is destroyed by its fungal partner, which causes activation of secondary vegetative zones, and therefore, increased branching of the root which enables better penetration of the soil.

  2. Protection from Intruders

    Aside from obtaining food, the fungus also confers protection to its plant partner. The rhizosphere (the region immediately adjacent to the plant root) is a gold mine of nutrients, flooded with leakage from plant roots as well as active secretions of rich jelly-like substances called mucilage. The free food attracts many microbial guests - many of which help break down nutrients into substances that the plant can use - not least parasites lurking in the soil. Phenolic compounds exuded by the fungal partners help control the activity of potentially friendly microbes in check, so that their part in the grand scheme is to help increase the turnover rate of nutrients in the soil and not wreaking havoc for the plant; the downright unfriendly ones, include Phytophthora and Fusarium, are staved off. This protection extends to seedlings as well - for example, it has been demonstrated that the ectomycorrhizae colonizing black spruce seedlings keep the root rot fungus at bay.

  3. Tolerance of Harsh Environments

    The partnership between plant and fungus has also enabled the partners to endure harsh environments that would otherwise be lethal to each individual. Mycorrhizal fungi have also been shown to protect their plant partners from heavy metal toxicity, as well as enable them to grow in inhospitable environments, such as salt marshes and soil heavily polluted with heavy metals or industrial wastelands. Furthermore, the partnership between plant and fungi seems to confer thermotolerance to both parties. Researchers were astounded when, in 2002, they discovered the hot-spring panic grass (Dichanthelium lanuginosum) and its fungal partner, Curvularia, flourishing around hot springs (with temperatures exceeding 50°C) in the Lassen Volcanic and Yellowstone National Parks. When they conducted experiments in the laboratory, they found that neither plant nor fungus could withstand high temperatures on their own; when coupled, however, these symbionts were able to withstand temperatures up to 65°C for short periods. The exact mechanism of this thermotolerance is unknown; however it has been speculated that the cell wall melanin produced by the fungus might serve to dissipate heat along its hyphae; it is also hypothesized that the fungus may serve as a 'biological trigger' allowing the plant to activate its stress-response systems more quickly and strongly than plants without symbionts. Whatever the mechanism, it is another excellent example of what plants and fungi are able to achieve together.

The Happy Marriage Between Orchids and Fungi

Perhaps the happiest odd couple in this world of mixed marriages is the orchid and its fungal symbiont. Orchid seeds are tiny, frail, delicate things that contain virtually nothing except an embryo; even when fully grown, the root systems of the orchid are tragically undeveloped. On its own, it could never survive in the world, let alone achieve maturity. But introduce it to the right mould partner, and incredible things happen. The sudden spurt of growth is nothing short of an explosion; both partners mate and flourish in a way that would have been otherwise impossible.

The key to this happy relationship is this: the orchid's root system, incapable of scraping enough nutrients to get by, are aided by the fungus' powers for foraging; in turn the orchid shares the food it manufactures from photosynthesis with the fungus. To keep the fungus from overstaying its welcome, however, the orchid also manufactures natural fungicides lest the fungus becomes too intimate and tries to take over. Eventually, as the plant matures, the fungal partner dies, its job completed, and its remains are absorbed to become part of the orchid.

Because the relationship between orchid and fungus is so intimate, divorce of these partners is often lethal to the orchid - which is why orchid conservationists have so hard a time trying to grow orchids in an artificial environment. Many scientists have tried germinating orchid seeds in a laboratory environment, without success; even when supplied with complex concoctions10 that mimic the cocktail of nutrients that the orchid normally gets from its fungal partner, these orchids barely make it past their infancy, and even then life is a struggle in isolation. This is also the reason why certain species of orchids are becoming endangered, thanks to the black market trade established by collectors and their mercenary suppliers - because they have blatantly ignored the role of fungi in the life-cycle of these plants. For, should the fungal symbiont die in the course of transportation, no amount of watering or fertilizing could restore a dependent orchid.

Getting Connected

But the relationship between plants and fungi do not stop at individuals. Just as no man is an island, no plant is isolated that lives side-by-side with fungi. Because a fungus is able to grow faster and penetrate grounds inaccessible to plants, it is only to be expected that the partnership is not just one plant-one fungus, but can be what would be the plant and fungi worlds' equivalent of a polyamorous relationship11. In other words, plants and fungi are all interconnected in an insane tangle of an underground Internet.

Although we who live above ground are unable to see the intricate connections in the soil, we are nevertheless able to observe the manifestations of this relationship. One of the most common phenomenon is the appearance of fairy rings in a field of grass12. Before the relationship between plants and fungi was established, scientists and the general populace alike puzzled over the mysterious appearances of progressively enlarging circles of dark fertile grass in fields and meadows. Even more mysterious was the occasional appearance of mushrooms at the centre of these circles. The superstitious attributed them to strange or metaphysical force: UFOs landings, fairies linking hands and dancing in the moonlight.

Unfortunately, for wishful thinkers, it is the power of fungi and not Daoine Sidhe at work.

A fungus that connects a host of trees to one another isn't simply a chain; it serves as a relay channel through which nutrients flow in all directions. It doesn't just find food for one tree; it finds food for many, and distributes it evenly to all its subscribers. Extra nutrients may be channelled from one to another. In a forest where tall trees form a canopy and shrubs form the undergrowth in relative darkness, the trees that get the lion's share of sunlight subsidise those that remain in the dark with nutrients via the fungal network. In some instances, germinating seedlings may even be supported by the pre-existing fungal partners of the parent plant. By sharing resources through a community support network, the fungi and its plant partners help maintain ecological stability.

This plant-fungus networking not only gives its plant members an enhanced, equal opportunity to flourish, it even in some cases gives the plants a vast advantage over other plants that are not subscribed. The tall fescue grass dominates the landscapes of prairies in many parts of the world. One variety in particular has been especially successful and far hardier in drought conditions than its uninfected counterparts - and to the dismay of farmers, surprisingly unpalatable to cattle. The secret to its success was discovered in the 1960s when scientists found a fungus growing in the space between the cells of the grass, which they named Acremonium for all the bitter farmers. This fungal partner not only increased the plant's resistance to drought and the number of seeds the grass produced in comparison to its neighbours13 but also causes the grass to become highly unpalatable to a wide variety of animals including cattle, plant-eating insect and worms. Attempts to replace them with fungus-free fescue grass are futile, and usually result in only more acrimony.

As a man who saves for a rainy day is cushioned when stock markets crash, so do mycorrhizal guild members recover quickly from natural disasters. Hurricanes, erosions and fires are the sledgehammer of nature, striking with blind force and devastating forest ecosystems. Ground-level fires may raze deciduous trees but will usually spare the hardier conifers; if the fire spreads from branch to branch, the ground-level plants will fare better. Either way, when such changes take place, the fungal partners will change their strategy to aid the plant partners who survive the devastation, quickly altering their foraging activities and growth patterns to cater to the needs of the survivors.

And to explain the mysterious fairy-ring phenomenon: the spread of the ring of darker grass and mushrooms in the centre is caused by the spreading of fungal hyphae around their plant partner/s. As the fungal partner grows outwards to find and decompose more organic matter for the plant, nutrients leak out from the fungi to the roots of these new tufts of grass, nourishing the grass and causing them to turn a rich healthy green.

The same phenomenon is observed when one mows a lawn in strips - at the end of the mowing day, the blades of grass are cut to jagged uneven height; and yet in a matter of weeks they somehow, mysteriously grow to be of equal height. Such is the power of fungus partnership.

In Conclusion

Plants and fungi have formed mycorrhizal relationships since the early days of prehistory. The most primitive form - vesicular-arbuscular mycorrhiza - arose in the Devonian era, when multicellular terrestrial plants first came into being. In fact, it was this very relationship between plant and fungi that enabled plants to colonize land over 400 million years ago. This relationship continued with the early vascular plants, and progressed to ectomycorrhiza in the Middle Cretaceous period as plants evolved to become the woodland giants we know today. Indeed, given the intimate relationship between these unlikely partners, the rise of large trees may never have come about had the first plant and fungus never found each other.

References

Clarke, B. 2000. Friendly fungi boost plant growth. Science on your Doorstep, Eastern Daily Press (19th August).

Frank, B. 1885. Über die auf Wurzelsymbiosen beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Ber. Dtsch. Bot. Ges. 3, 128-145.

Madigan, MT, JM Martinko, and J Parker. 1997. Brock Biology of Microorganisms. Prentice Hall International.

Managing Arbuscular Mycorrhizal Fungi for Improving Soil Quality and Plant Health in Agriculture. Proceedings of the Centre National de la Recherche Scientifique Working Group 2 Meeting, 10-11 December 1999.

Morin C, J Samson, and M Dessureault. 1999. Protection of black spruce seedlings against Cylindrocladium root rot with ectomycorrhizal fungi. Canadian Journal of Botany 77: 169-174.

Newsham KK; Fitter AH; Watkinson AR. 1995. Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. Journal of Ecology 83 (6):991-1000.

Redmann, RS, RJ Rodriguez, KB Sheehan, RG Stout, & JM Henson. 2002. Thermotolerance Generated by Plant/Fungal Symbiosis. Science, 298:1581.

Surridge, C. 2002. Fungus and plant stand heat together: Symbiotic relationship helps grass grow round hot springs. Nature Science Update (Nov 22).

Van Tichelen KK, JV Colpaert, and J Vangronsveld. 2001. Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytologist 150: 203-213.

Wakeford, T. 2001. Liaisons of Life. John Wiley & Sons, Inc, USA.

Wilkinson, DM. 2001. At cross purposes. How do we cope with scientific terms that have two different definitions? Nature 412 (2 August).

Resources on the Internet:

1The study or science of fungi.2Note: However, there are certain sources arguing that de Bary actually described symbiosis as a close, long-term associations between different organisms, and that he had included in the definition both parasitism and mutualism.3A mushroom is the fruiting body of higher fungi.4The vegetative part of a fungus, in the form of threadlike tubes. A mycelium is a mass of hyphae.5Which is to say they need fungal partners to survive.6The cells are not separated by cell walls, and so the cytoplasm is free to flow from one to another.7This weak defence response may be due to some plant mechanism that regulates the suppression of such a response to allow symbiosis to occur. It is also possible that mycorrhizal fungi produce very little enzyme that degrades plant cell wall, and so cause little damage and do not induce a strong defence response.8Adenosine triphosphate; energy is stored in its strong triple phosphate bonds.9In fact, the expenditure involved in building root systems comparable to the fungi's hyphal network would be a hundred times greater than the energy cost of fungal hyphae foraging for and extracting the same nutrients.10Svante Malmgren, a Swedish paediatrician and amateur mycologist, came up with a synthetic cocktail of amino acids, potato extract and pineapple extract, which the botanists at Kew Gardens are using to artificially cultivate orchids in the laboratory. However, this has brought limited success as very few orchids have survived beyond the seedling stage without their fungal partners.11One fungus can be connected to many plants of different species; one plant can be connected to fungi of different species; every plant and fungus has more than one symbiont partner. For example the Western Australian underground orchid Rhizanthella gardneri forms mycorrhizal relationship with a fungus that also partners the Australian Tea Tree, Melaleuca. These relationships are not static, but may change over time, and with change of environment.12Such fairy circles can reach diameters of up to nine hundred feet, weigh an average of one metric tonne, and may endure for several hundred years.13All of which come packaged with their own fungal partner, which will ensure they grow to become healthy, vigorous plants.

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