What lies beneath

12 July 2013 by Malcolm Campbell, posted in Biology

Nature alone is antique, and the oldest art a mushroom." by Thomas Carlyle (1795-1881)

Nature is a master of understatement, if not outright sly deception.

The proverbial “tip of the iceberg” is the most frequently invoked illustration of Nature’s understatement.  The iceberg’s tip belies the massive body that lies beneath the water’s surface. The tip only hints at the vastness of the underlying ice, and the role that ice plays in the subsurface environment. That which we see above the water’s edge doesn’t directly inform us of the mass of ice necessary to keep it buoyant – that enables it to be visible to passers-by.

As examples of deceptive understatement go, the tip of the iceberg is, well, the tip of the iceberg. Other examples of deceptive simplicity in Nature are plentiful.

Of all of the examples of deceptive simplicity in Nature, there are few better than the humble mushroom.

Where I live, mushroom season has kicked into high gear. Warm, humid weather has created ideal conditions for mushrooms to emerge – seemingly erected overnight – prominently dotting field and forest alike.

Mushrooms, sometimes referred to as toadstools, are the so-called “fruiting bodies” – the reproductive part – of fungi. Standing above the soil, variously shaped like umbrellas, buttons, balls, or stalks with caps, these fleshy bodies will produce spores that complete the fungal life cycle – spores that will enable the fungus to spread far and wide. As such, mushrooms are the prominent, visible feature of the fungus. But, like the tip of the iceberg, the mushroom provides a remarkably incomplete picture of what the fungus is really up to.

Like the plants that surround them, mushrooms have an extensive existence beneath the soil. Where plants have roots, mushrooms have mycelium. In fact, the majority of a fungus consists of mycelium, with the mushroom only poking into existence under specific conditions to enable spore production, sporulation, to occur. For most of its life, a fungus will consist of a network of soil-bound mycelium. Mycelium consists of thread-like hyphae, the growing cells of the fungus. Hyphae spread through the soil as long, branching filamentous strands. They spread by elongating at their tips. When an elongating hypha reaches a critical length, a dividing plate, or septa, will be made behind the growing tip, so as to divide the hypha into two cells. This process repeats iteratively, with periodic branching occurring, so that eventually the fungal mycelium completely insinuates itself into the soil.

The mycelium functions as an effective network to collect resources from the environment. Crucially, for many fungi, the acquisition, or, to be more accurate, the sharing of resources is something they do in partnership. While it is hidden beneath the soil, this is one of the most prominent, and important, partnerships in nature – the mycorrhizal symbiosis.

Mycorrhizal symbioses involve almost all plant species. As the name implies, mycorrhizal relationships involve fungi (myco-) and plant roots (-rhiza). There are two major types of mycorrhizal symbioses.

Approximately 10% of plant families can participate in what are known as ectomycorrhizal symbioses. With ectomycorrhiza, or ectomycorrhizae, fungal hyphae intercalate between the cells of the roots, forming a structure known as the Hartig net. The fungus has invaded the root, but has not actually entered the cells of the root, hence the name “ecto”, for outside. The Hartig net hyphae embedded within the root extend outside the root and, together with other hyphae, form a dense mycelium sheath around the root. This sheath is then connected to the larger mycelium, extending well out into the soil. Many forest trees, particularly conifers, form ectomycorrhizal symbioses.

The majority of plants, approximately 85% of all plant families, are able to form endomycorrhizal symbioses. In contrast to ectomycorrhizal symbioses, in endomycorrhizae, the fungal hyphae actually enter inside the root cells. It is this feature that gives ectomycorrhizae their name, as “ecto” means inside. In the most prominent type of endomycorrhizae, known as arbuscular mycorrhizae (formerly vesicular-arbuscular mycorrhizae), the fungal hyphae penetrates the cell wall of root cells, and forms a vesicle-like structure embedded within the plant cell. The hyphae embedded within the root connect with the mycelium network on the root’s exterior, thereby providing a continuum that extends from within the root well out into the soil.

Generally speaking, mycorrhizae are mutualistic symbioses. That is, both partners benefit from the relationship. In the case of the fungus, it is the beneficiary of carbohydrates, sugars, that the plant has produced through photosynthesis. The fungus may also obtain other nutrients, including amino acids, from the plant. On the other hand, the plant acquires soil-bound nutrients and minerals, notably phosphorous, sulfur, and nitrogen, from the fungus. It can also acquire water through the fungus. In fact, one can think of the plant’s root system as being dramatically extended by the mycorrhizal mycelium, as if through a fungal prosthetic, into the surrounding soil. By virtue of its connection with the fungal network, plants have a means by which to expand the range of their foraging for essential nutrients and water.

The mycorrhizal relationship is a longstanding one, extending back into the Devonian, some 400-450 million years ago. Like many long-standing relationships, the establishment and maintenance of mycorrhizal symbioses requires good communication between the partners. This communication is based on the exchange of chemical signals. For example, plant roots produce and release specific molecules, such as flavonoids and strigolactones, that can function to attract fungal hyphae and induce hyphal branching. Hyphae in the proximity of plant roots release complex molecules known as lipopolysaccharides that function to inform the plant of their presence. Plant perception of specific lipopolysaccharides from mycorrhizal fungi invokes a suite of responses that ready the plant for the partnership. The back-and-forth discourse involving chemical signals and developmental responses ultimately leads to the establishment of the mutualistic relationship – a relationship that is reinforced by the sharing of resources over the mycelium network.

The extent to which the mycorrhiza-associated mycelium can extend a plant’s reach is astonishing. The mycelium network may cover not merely square meters, but literally square kilometers. This provides an opportunity for any plant that is embedded in this network to access resources that may be quite distant from its roots. In fact, the mycelium network can function as a conduit for exchange of nutrients between plants. This nutrient exchange is thought to be very important for the establishment of young plants, as they can acquire resources from established individuals within the network.

Beautiful research undertaken by Kevin Beiler and colleagues examined the extent of interconnectivity between plants in a mycorrhizal network. Examining plots that were 30m by 30m, containing mixed-aged Douglas fir trees and two different fungi of the genus Rhizopogon, they found that individual mycelium networks might connect up to 19 different plants. Crucially, the plants in the network did not need to be related, nor the same age. Thus, the network enabled sharing of resources to the benefit of the species and not just to individuals. Moreover, the network suggests how young plants benefit from older plants, via the resource sharing that is possible over the network.

It turns out that the sharing of resources mightn’t be the only benefit that plants accrue by being connected via the mycorrhizal network. Growing evidence suggests that plants exchange information over the mycorrizhal network - a “wood-wide web” if you will. Most recently, this information exchange has been shown to function as an early warning system for herbivore attack.

In elegant experiments, David Johnson and his colleagues found that plants could preemptively prepare themselves for an aphid attack if they were connected to a mycorrhizal network. These experiments focused on the ability of broad bean plants to produce volatile molecules, particularly methyl salicylate. Methyl salicylate plays two important roles in defending broad beans against aphid herbivores. In the first instance, it repels aphids, making the plants unattractive as a food source. Methyl salicylate also attracts parasitoid wasps – mortal enemies of aphids. With these two roles, methyl salicylate is a pretty effective defence against aphids making a meal of broad beans.

Aphid-infested broad beans will make methyl salicylate as a defence against the herbivore. Bu contrast, normally, plants that are not under attack from aphids will not mount this defence. However, plants that are not aphid infested will launch a methyl salicylate defence, if they are connected via a mycorrhizal network to plants that are infested. Johnson and his colleagues made sure that the communication was not merely via the volatile signals being released by the infested plant, by completely enveloping the plant in an airtight sealed bag so that the uninfested plant was not exposed to the volatiles. Taken together, the findings point to a subterranean signal travelling via the mycelium from the infested plant to the uninfested plant. This underground information flow invokes an anticipatory defence response in the uninfested plant. Amazing!

To date, we don’t know the nature of the signal that is transmitted via the underground network. You can be sure that this is topic of intense interest. It is only a matter of time before this new aspect of the remarkable mycorrhizal partnership is fleshed out.

Mycorrhizae underscore how the deceptive simplicity of the humble mushroom doesn’t do justice to the astonishing relationship that lies beneath the soil. How often are we similarly tricked by the apparent simple nature of things, such that we miss the layers of remarkable complexity that hold that object in place? Alternatively, how often are we deceived by that which is visible, only to miss the important relationships, the support networks, that lay hidden from our view? We are quick to highlight, praise, or otherwise champion the mushrooms – those  that stand centre stage, or take the microphone, or sit in positions of power – without acknowledging the incredible network that has secured that position for them. If mushrooms and mycorrhizae tell us anything, it is that networking, with strong communication, sharing of resources, and watching each others' backs that enables us to periodically stand above the dirt.


Babikova Z et al. (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters 16: 835-843

Barto EK et al. (2012) Fungal superhighways: do common mycorrhizal networks enhance below ground communication? Trends in Plant Science 17: 633-637

Beiler KJ et al. (2010) Architecture of the wood‐wide web: Rhizopogon spp. genets link multiple Douglas‐fir cohorts. New Phytologist, 185: 543-553

Bonfante P & Requena N (2011) Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 14: 451-457

Jung SC et al. (2012) Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology 38: 651-664

Simard SW et al. (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biology Reviews 26: 39-60

Images: All photographs by Malcolm M. Campbell.


3 Responses to “What lies beneath”

  1. Susi Batstone Reply | Permalink

    Thank you for this article, which was also beautifully illustrated. The more I learn about fungi, the more I want to learn and understand. Awesome life forms.

    • Malcolm Campbell Reply | Permalink

      Thank you for the kind feedback, Susi! I'm glad you liked the post. Fungi are awesome indeed!

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