Can trees nurse their young? Do plants send out signals underground to warn each other of the arrival of ravenous insects? Can they go on the attack themselves and cripple competing plants with noxious chemicals they deliver through fungal connections? Lately, researchers investigating subterranean fungal networks have come up with surprising answers to questions like these. Their intriguing findings also have game-changing implications for ecology and conservation, forestry and agriculture—even evolutionary theory.
Some 90% of terrestrial plant species around the world engage in symbioses called mycorrhizae—from Greek mykos (fungus) and rhiza (root). Mycorrhizal plants come from all corners of the plant kingdom and include trees, forbs, grasses, ferns, clubmosses, and liverworts. Their symbiotic partners (symbionts) are fungi whose threadlike hyphae radiate out into the soil, bringing water and nutrients—including phosphorus, nitrogen, zinc, and copper—back to the plant’s roots in exchange for a share of the carbohydrates plants produce through photosynthesis. Though mycorrhizal symbioses range along a continuum from parasitic (on the part of the plant) to mutualistic types, most are mutually beneficial. By themselves, plants can only access nutrients in the immediate vicinity of their feeder roots, and soon exhaust the supply. By associating with fungi, they conserve resources that would have been spent on growing ever larger root systems. In fact, as Smith and Read state categorically in their compendium of all things mycorrhizal, “Mycorrhizas, not roots, are the chief organs of nutrient uptake by land plants” (Smith and Read 2008).
Subway Lines
When compatible mycorrhizal fungi and plants recognize each other and create an interface in the plants’ roots for the exchange of nutrients, they can form a variety of structures in and around the roots, depending on the species involved. Broadly speaking, there are two main types: arbuscular mycorrhizae and ectomycorrhizae.
Arbuscular mycorrhizae get their name from the classic shape that the fungi take inside root cells, a profusely branching form called an arbuscule. As its name suggests, an arbuscule has a miniscule tree- or shrub-like shape. The creation of an arbuscular mycorrhiza begins when chemicals exuded by a plant’s roots stimulate a nearby arbuscular mycorrhizal fungus to branch and grow, allowing it to quickly find the roots. Once in contact, the fungus adheres to the root surface and, within a few days, penetrates the root and begins the formation of a mycorrhiza.
Inside the root, different arbuscular mycorrhizal structures may develop, depending on the particular species involved. In 1905, the botanist Ernest-Isidore Gallaud named arbuscular mycorrhizal structures after plant genera he found them in. Arum-type mycorrhizae resemble maps of bus or subway lines: hyphae grow into the space between rows of cells, extending alongside them, like avenues running past city blocks, and making “stops” along the way to enter cells and form arbuscules. Though it penetrates a root cell’s wall, the fungus remains in what amounts to an antechamber; it never passes through the cell’s plasma membrane. Instead, this membrane envelops the invading hypha and all of its branches, maximizing the area of mutual contact. At this interface, plant and fungus establish a sort of marketplace where each partner deposits nutrients and trades them for nutrients deposited by the other.
Gallaud named the other main form of arbuscular mycorrhiza the Paris type, after a Eurasian plant genus (a relative of Trillium). In the Paris type, the fungus forms coils that look like chaotic loops of strewn intestines. An occasional small arbuscule may branch off from a coil, but the Paris-type mycorrhiza lacks a straight “subway line” traveling alongside the cells. Instead, a coiling hypha exits from one cell only to enter the adjacent one, where it forms another mass of coils before moving on to the next cell—definitely not the express train!
Arbuscular mycorrhizae have been around for a long time. Researchers have found arbuscules in fossils of Aglaophyton,an extinct genus of pre-vascular plant, dating from around 410 million years ago, in the Devonian Period. In fact, most scientists agree that the first plants to colonize the land were symbiotic organisms containing structures very similar to arbuscular mycorrhizae (Smith and Read 2008). Given their lengthy tenure on the planet, it’s not surprising that arbuscular mycorrhizae occur in nearly all species of herbaceous plants and in most trees and shrubs. But the other main mycorrhizal type—the ectomycorrhiza (going back a mere 50 million years)—is also extremely important. While only about 3% of seed plants are ectomycorrhizal, they occupy large expanses of the earth’s terrestrial surface. Almost all are woody plants, and they include forest trees that are the world’s main sources of timber, such as pines. Starting alphabetically, Abies, Acer, Alnus, Betula, Carpinus, and Corylus are a few of the eastern North American genera containing at least one ectomycorrhizal species.
Ectomycorrhizae differ from arbuscular mycorrhizae in several other ways. Unlike arbuscular mycorrhizal fungi, ectomycorrhizal fungi mostly do not penetrate root cells, hence their designation as “ecto-” meaning “outer” or “external.” The hallmarks of an ectomycorrhiza are the fungal sheath, which encloses the root tip in a dense mass of hyphae, and the Hartig net, a labyrinthine hyphal network that grows between the outer layers of the root’s cells. Another difference involves the relative numbers of associated fungus species. Despite the vast numbers of arbuscular mycorrhizal plant species, their fungal symbionts consist of only about 150 species, all in the division Glomeromycota. Inversely, a more diverse group of about 5,000 to 6,000 fungus species form ectomycorrhizal associations. And while all arbuscular mycorrhizal fungi are microscopic and subterranean, many ectomycorrhizal fungi develop large fruiting bodies that occur either above or below ground. Those that appear above ground include many common woodland mushrooms, while the most notable of the underground-fruiting ectomycorrhizal fungi belong to the genus Tuber, best known for its fruiting bodies, truffles.
Sharing Food
We can visualize a mycorrhiza as a simple one-to-one relationship between an individual plant and an individual fungus. But in nature the picture is more complex. As the threadlike hypha of a mycorrhizal fungus extends outward from a plant’s roots, it frequently encounters the roots of other plants of the same or different species. It may form mycorrhizae with these new partners, while still maintaining its connection with the first plant. As it proliferates in new directions, the hypha branches and fuses repeatedly, weaving a fungal net through the surrounding soil. Meanwhile, additional fungi of the same or different species may approach the first plant. If they’re compatible, the plant is apt to form mycorrhizae with them, too. Soon a diverse association appears, composed of various fungi and various plant species, big and small, all connected into a sizeable mycorrhizal network that may span hundreds of hectares of forest (Gorzelak et al. 2015). The promiscuous nature of these associations of multiple plant and fungus species has prompted scientists to give their papers playful titles like: “Changing partners in the dark,” “Mycorrhizal networks: des liaisons dangereuses,” and “Architecture of the wood-wide web.”
Mycorrhizal networks are highly efficient at procuring essential plant nutrients from the soil while the plant partner provides the carbon that fungi require. But the carbon doesn’t stop there. It’s long been known that certain nonphotosynthetic, parasitic plants, called mycoheterotrophs, depend on carbon shuttled from photosynthesizing plants via mycorrhizal fungi (see next page). The seeds of most mycoheterotrophs are tiny “dust seeds,” consisting of only a few cells and little or no endosperm to supply the germinating plant with food. Thus, these species depend upon mycorrhizal fungi for their survival. The orchids, perhaps the largest family in the plant kingdom, depend entirely on carbon received via mycorrhizal fungi for successful seed germination and early development. Experiments have shown that certain green orchids can convey carbon back to their associated fungi once they reach maturity. Thus, they partake in mutualisms that are offset in time, like borrowers repaying a loan. But “full mycoheterotrophs” (including some orchids) depend, throughout their lives, on carbon received through mycorrhizal networks, apparently without benefit to the fungus.
In recent years investigators have discovered that mycorrhizal networks can distribute resources in much more flexible ways than previously thought, sending them in the direction of greatest need in response to changing conditions, in a seasonal tide-like flux. Researchers at Laval University in Quebec found evidence that carbon moved via mycorrhizal networks from yellow trout lilies (Erythronium americanum) to young sugar maples (Acer saccharum) as the maples’ leaves unfurled in spring, and then back to the trout lilies in the fall during rapid trout lily root growth (Lerat et al. 2002). The direction of carbon flow can reverse even more frequently. University of British Columbia researchers reported that the flow of carbon changed direction not once but twice in the course of a growing season. In the spring, carbon traveled from Douglas-fir (Pseudotsuga menziesii) to paper birch (Betula papyrifera) as its buds resumed growth. In the summer, carbon flowed from heavily photosynthesizing paper birch into stressed Douglas-fir in the understory. And in the fall, it flowed from still-photosynthesizing Douglas-fir into paper birch as it shed its leaves (Simard et al. 2012).
Other resources besides carbon can change direction too. Though water typically flows from mycorrhizal fungi into the roots of their plant symbionts, under extreme conditions it can go the other way. In a greenhouse experiment, investigators using dye tracers found that when soil became extremely dry, oaks that were able to access water through their deep taproots transferred water to their mycorrhizal fungi, thus keeping them alive (Querejeta et al. 2003). Plants can even defend their fungal partners from fungivores. A recent study found evidence that when springtails (tiny insect-like hexapods) browse on mycorrhizal fungi, plants can help by sending protective chemicals into the hyphae (Duhamel et al. 2013).
What about the extraordinary idea that plants might be subsidizing their progeny—essentially nursing them—using mycorrhizal networks? Though there is no clear evidence that plants can detect their kin through mycorrhizal networks and shuttle nutrients preferentially to offspring, there are hints in that direction. Ferns reproduce in a life cycle that passes through two distinct generations. Spores from the familiar, leafy sporophyte generation germinate and grow into the tiny, rarely seen gametophyte generation, which, through sexual reproduction, gives rise to the next generation of sporophytes. Researchers working with two species of the fern genus Botrychium found that strains of Glomus (a genus of arbuscular mycorrhizal fungi) maintained mycorrhizae with individuals of both generation types simultaneously, demonstrating the potential for sporophytes to subsidize the achlorophyllous gametophytes (Winther and Friedman 2007). Since then, a number of studies have shown that tree seedlings do indeed benefit from resources received from mature trees of the same species via mycorrhizal networks, though not necessarily to a greater degree than other plants in the network.
Notes from the Underground
The hustle and bustle of mycorrhizal networks becomes even more intriguing as we look beyond resource sharing to the remarkable communication functions of mycorrhizal networks. What do plants need to talk about? Like many animal species, plants have a language of danger. In the early 1980s, David Rhoades, a zoologist interested in the interactions between insect herbivores and plants, proposed a novel idea. In the course of his research with Salix sitchensis, he had noticed that defensive changes in the leaf chemistry of willows being chewed on by tent caterpillars also showed up in the leaves of nearby plants, even though they had not yet been attacked. He speculated that the neighboring plants must have detected airborne molecules emanating from either the attacked plants or the tent caterpillars, prompting them to deploy protective chemicals preemptively (Rhoades 1983). Subsequent research confirmed Rhoades’ suspicion—plants being attacked by herbivores can release volatile organic compounds into the air that induce defensive responses in nearby plants. And recent experiments have shown that such “stress signals” can also be transmitted through mycorrhizal networks. Researchers at South China Agricultural University inoculated tomato plants with the fungal pathogenAlternaria solani, the cause of early blight disease in tomatoes and potatoes, and became the first to demonstrate that mycorrhizal networks can act as plant-to-plant communication conduits. They found that the uninfected tomato plants (stress-signal receivers) in the mycorrhizal network showed an increase in disease resistance and putative defense-related enzyme activity. They also found that the receiver plants had activated several defense genes. These changes in the receiver plants began within 18 hours of inoculating the donor plants (Song et al. 2010).
In 2013, a group of scientists working in the United Kingdom decided to follow up on the fungal pathogen study and see what would happen with insect herbivores. They produced the first experimental evidence that signal molecules from plants infested with aphids travel through mycorrhizal networks to uninfested neighboring plants. Within 24 hours of the arrival of pea aphids (Acyrthosiphon pisum) on broad bean plants (Vicia faba), signals traveling through mycorrhizal networks caused uninfested broad beans to give off volatile compounds. Not only did these compounds repel the aphids, they actually attracted the aphids’ natural enemy, the parasitoid wasp Aphidius ervi (Babikova et al. 2013). This interaction apparently benefits all three parties to the network. Being quickly alerted to the threat allows the uninfested beans to deploy their protective volatiles preemptively, thus evading aphid attack. The fungi thereby avoid a potentially catastrophic reduction in the plants’ capacity to supply them with carbon. And even the infested beans may benefit: some investigators suggest that stress-signal transmission ensures that signal-donor plants will become engulfed in a large plume of protective volatiles created collectively by the surrounding plants in the network (Barto et al. 2012).
In some cases, attacks on plants can simultaneously stimulate both stress signals and nutrient transfers. A recent collaboration between Chinese and Canadian researchers investigated the flow of carbon and stress signals in a mycorrhizal network involving a four-month-old interior Douglas-fir (Pseudotsuga menziesii var. glauca), a ponderosa pine (Pinus ponderosae), and the ectomycorrhizal fungus, Wilcoxina rehmii. They found that manual defoliation of the young Douglas-fir resulted in a transfer of both defense signals and carbon via mycorrhizal network to the ponderosa pine (Song et al. 2015). Some mycorrhizologists ascribe this result to the fungus throwing in its lot with the healthy pine rather than throwing good money after bad by propping up the struggling Douglas-fir. Postulating that the transfers were initiated by the fungus, they write: “Here, the networking fungus may have acted to protect its net carbon source, by allocating carbon and signals to the healthy, more reliable ponderosa pine” (Gorzelak et al. 2015).
Weapons of Plant Destruction
Besides tranferring resources and signals, mycorrhizal networks can extend the reach of the allelochemicals that certain plants produce—toxic substances that inhibit the development of nearby competitors. Thus, “mycorrhizal networks can serve as couriers for biochemical warfare” (Gorzelak et al. 2015). A study of the effect of mycorrhizal networks in the transport of the allelochemical juglone, which is exuded by the roots of Juglans species (walnuts) and negatively affects the growth of many plants including rhododendrons, tomatoes, and apples, unequivocally implicated mycorrhizal networks in the dispersal of juglone into the soil (Achatz et al. 2014).
In at least one case, instead of helping to spread noxious allelochemicals, mycorrhizal fungi themselves become the victims. Garlic mustard (Alliaria petiolata), a European plant well known as an invasive in eastern North America, is a non-mycorrhizal plant that produces fungicidal allelochemicals. Researchers found that garlic mustard drastically reduced the ability of North American arbuscular mycorrhizal fungal spores to germinate and form mycorrhizae. As a result, American mycorrhizal plants had reduced seed-germination and increased mortality, while non-mycorrhizal plants were unaffected. European arbuscular mycorrhizal fungi and plants were also relatively unaffected, presumably due to their long evolutionary exposure to garlic mustard’s allelochemicals (Callaway et al. 2008).
Another peculiar relationship between invasives and mycorrhizal networks involves spotted knapweed (Centaurea stoebe, formerly C. maculosa), which is invasive in many areas and covers over seven million acres in the United States. It’s of particular concern in the West, where Idaho fescue (Festuca idahoensis) is a common native grass. University of Montana researchers estimated that as much as 15% of the above-ground carbon in spotted knapweed plants came from nearby fescue by way of mycorrhizal fungi (Carey et al. 2004). Thus, invasives may exploit mycorrhizal networks to thrive at the expense of neighboring native plants.
Networking for the Future
Understanding mycorrhizal networks is evidently important for effective conservation of many species. This is particularly true of mycoheterotrophs, which cannot survive apart from mycorrhizal networks. According to Martin Bidartondo of the Royal Botanic Gardens at Kew, “myco-heterotrophic plants are excellent indicators of undisturbed forests and forests with old-growth characteristics” (Bidartondo 2005). It follows that mycoheterotrophs are among the species at greatest risk of extirpation from the clearcutting of forest lands (Moola and Vasseur 2004). Mycoheterotrophs are extremely host-specific, so their conservation must involve both their particular fungal host species and the green plants that supply carbohydrates as essential habitat components.
With the increased resistance to diseases and pests and the better access to water and nutrients that mycorrhizal networks offer, there is increasing recognition of the potential for a new “Green Revolution” based on using mycorrhizae in crop fields and forests. Much of the world’s agriculture depends upon fertilizer derived from mined rock phosphate, a non-renewable resource that is steadily dwindling. Phosphorus is a crucial plant nutrient that mycorrhizal fungi are particularly good at locating in ordinary soil and funneling back to their plant symbionts. We can lessen our dependence on rock phosphate by finding ways to work with mycorrhizae. Proposed techniques include sowing fallow fields with appropriate mycorrhizal plants to maintain the level of fungal inoculum in the soil between crop rotations, using tilling patterns that minimize disturbance of mycorrhizal fungi, and avoiding the indiscriminate use of fungicides in the soil. Many tree nurseries are finding that inoculating tree seedlings with appropriate mycorrhizal fungi increases survival both in the nursery and after planting out.
In perusing the reports mentioned in this article, I was struck by the various ways investigators conceptualized what they saw happening in mycorrhizal networks. There are large gaps in what is understood about how mycorrhizae operate, and scientists must often use human metaphors as stand-ins to bridge the gaps. One implicit question that kept surfacing was: Who were the doers of the actions taking place in mycorrhizal networks, and what were their “motives”? Were plants “nursing” their progeny to keep their species going, or were fungi redistributing resources to the young plants with an eye to their own future wellbeing? Were Douglas-firs helping paper birches so as to later receive reciprocal benefits in their hour of need, or were fungi orchestrating the flux of resources, minimizing their risk by diversifying across multiple partner species? Were stress-signal donors “warning” receiver plants, or were the receivers “eavesdropping” on donors, on the alert for potential trouble? Or were mycorrhizal fungi acting like savvy farmers, apportioning fertilizer and coordinating pest management to maximize long-term yield? Perhaps the answer is “all of the above,” because ultimately all the organisms involved tend to strengthen and perpetuate their mutually beneficial networks. Indeed, when all the participants’ roles are considered, the network as a whole emerges as a kind of higher-order organism in its own right, fitter than the sum of its parts, a well-ordered social entity capable of surviving the death of any of its individual members.
Citation: Yih, David. 2017. Food, Poison, and Espionage: Mycorrhizal Networks in Action. Arnoldia 75(2): 2–11.
Some scientists argue that the groupings of species involved in mycorrhizal networks are examples of natural selection at the level of the group (Gorzelak et al. 2015). For others, the interesting question is: which is the true driver of evolution—competition or cooperation? The ground-breaking evolutionary theorist Lynn Margulis passionately insisted on the predominant role of symbiosis in evolution. And for evolutionary biologist and author Frank Ryan, the discovery of mycorrhizae was a missed opportunity. He wrote, “The intimate cooperation between wholly different life forms—plants and fungi—is not only an amazing biological phenomenon but also a vitally important factor in the diversity of plant life on earth. It should have been of enormous interest to evolutionary theorists, but … at the end of the nineteenth century, as the fundamental principles of biology were being hammered into place in laboratories around the world, Darwinian evolution took center stage. And as Darwinism, with its emphasis on competitive struggle, thrived, [mutualistic] symbiosis, its cooperative alter ego, languished in the shadows, derided or dismissed as a novelty” (Ryan 2002). Perhaps its time is still to come. In the meantime, plants and their mycorrhizal networks offer a fascinating and fruitful field of inquiry on many different levels.
References
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Babikova, Z., L. Gilbert, T. J. A. Bruce, M. Birkett, J. C. Caulfield, C. Woodcock, J. A. Pickett, D. Johnson, and N. van Dam. 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters 16: 835–843.
Barto, E. K., J. D. Weidenhamer, D. Cipollini, and M. C. Rillig. 2012. Fungal superhighways: Do common mycorrhizal networks enhance below ground communication? Trends in Plant Science 17: 633–637.
Bidartondo, M. I. 2005. The evolutionary ecology of myco-heterotrophy. New Phytologist 167: 335–352.
Callaway, R. M., D. Cipollini, K. Barto, G. C. Thelen, S. G. Hallett, D. Prati, K. Stinson, and J. Klironomos. 2008. Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89: 1043–1055.
Carey, E. V., M. J. Marler, and R. M. Callaway. 2004. Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecology 172: 133–141.
Duhamel, M., R. Pel, A. Ooms, H. Bücking, J. Jansa, J. Ellers, N. M. van Straalen, T. Wouda, P. Vandenkoornhuyse, and E. T. Kiers. 2013. Do fungivores trigger the transfer of protective metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology 94: 2019–2029.
Gorzelak, M. A., A. K. Asay, B. J. Pickles, and S. W. Simard. 2015. Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7.
Lerat, S., R. Gauci, J. G. Catford, H. Vierheilig, Y. Piché, and L. Lapointe. 2002. C14 transfer between the spring ephemeral Erythronium americanum and sugar maple saplings via arbuscular mycorrhizal fungi in natural stands. Oecologia 132: 181–187.
Moola, F. M. and L. Vasseur. 2004. Recovery of late-seral vascular plants in a chronosequence of post-clearcut forest stands in coastal Nova Scotia, Canada. Plant Ecology 172: 183–197.
Querejeta, J. F., L.M. Egerton-Warburton, and M.F. Allen. 2003. Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134: 55–64.
Rhoades, D. F. 1983. Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In: Plant Resistance to Insects: Based on a symposium sponsored by the ACS Division of Pesticide Chemistry at the 183rd Meeting of the American Chemical Society, Las Vegas, Nevada, March 28–April 2, 1982, ed. Paul Hedin. ACS Symposium Series number 208. pp. 55–68. American Chemical Society.
Ryan, F. 2002. Darwin’s Blind Spot: Evolution Beyond Natural Selection. Boston: Houghton Mifflin Harcourt.
Simard, S. W., K. J. Beiler, M. A. Bingham, J. R. Deslippe, L. J. Philip, and F. P. Teste. 2012. Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biology Reviews 26: 39–60.
Smith, S. E. and D. J. Read. 2008. Mycorrhizal Symbiosis, third edition. Cambridge, Massachusetts: Academic Press.
Song, Y. Y., R. S. Zeng, J. F. Xu, J. Li , X. Shen, and W. G. Yihdego. 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS ONE 5(10): e13324.
Song, Y. Y., S. W. Simard, A. Carroll, W. W. Mohn, and R. S. Zeng. 2015. Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Scientific Reports 5, Article no. 8495.
Winther, J. L. and W. E. Friedman. 2007. Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). American Journal of Botany 94: 1248–1255.
David Yih is president of the Connecticut Botanical Society.
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