It’s every plant’s worst nightmare. In the fall of 2009, in a Victorian greenhouse at the Cruickshank Botanic Garden at the University of Aberdeen in Scotland, Zdenka Babikova sprinkled vegetation-devouring aphids on eight broad bean plants and sealed each plant’s leaves and stems inside a clear plastic bag. This was no act of malice, though; it was all in the name of science. Babikova, a PhD student at the University of Aberdeen, knew that aphid-infested bean plants release odorous chemicals known as volatile organic compounds (VOCs) into the air to warn their neighbors, which respond by emitting different VOCs that repel aphids and attract aphid-hunting wasps. What she didn’t know was whether the plants were also sounding the alarm beneath the soil surface.
Five weeks earlier, Babikova filled eight 30 cm–diameter pots with soil containing Glomus intraradices, a mycorrhizal fungus that connects the roots of plants with its hyphae, the branching filaments that make up the fungal mycelium. Like a subterranean swap meet, these hyphal networks facilitate the trade of nutrients between fungi and plants. In each pot, Babikova planted five broad bean plants: a “donor” plant surrounded by four “receiver” plants. One of the receivers was allowed to form root and mycorrhizal contact with the donor; another formed mycorrhizal contact only, and two more had neither root nor mycorrhizal contact. Once the mycorrhizal networks were well established, Babikova infested the donor plants with aphids and sealed each plant in a separate plastic bag that allowed for the passage of carbon dioxide, water, and water vapor but blocked larger molecules, such as the VOCs used for airborne communication.
Four days later, Babikova placed individual aphids or parasitoid wasps in spherical choice chambers to see how they reacted to the VOC bouquets collected from receiver plants. Sure enough, only plants that had mycorrhizal connections to the infested plant were repellent to aphids and attractive to wasps, an indication that the plants were in fact using their fungal symbionts to send warnings.1
In last 15 years the idea that plants are communicating has become much more accepted. It’s exciting to unravel all these different realms of plant communication.—Richard Karban, University of California, Davis
“When Zdenka first showed us those results it was quite a eureka moment,” says David Johnson, a soil ecologist at Aberdeen who co-led the research. “There was a really striking difference between the insects’ responses to plants with and without hyphal connections. We had more samples to test, but even at that point, it was pretty clear that this is an effective signaling system.”
The remarkable conclusions from this study, published last May, are the latest shoots in a growing thicket of data revealing the unexpectedly complex ways that plants exchange information with one another. Researchers are unearthing evidence that, far from being unresponsive and uncommunicative organisms, plants engage in regular conversation. In addition to warning neighbors of herbivore attacks, they alert each other to threatening pathogens and impending droughts, and even recognize kin, continually adapting to the information they receive from plants growing around them. Moreover, plants can “talk” in several different ways: via airborne chemicals, soluble compounds exchanged by roots and networks of threadlike fungi, and perhaps even ultrasonic sounds. Plants, it seems, have a social life that scientists are just beginning to understand.
“In the last 15 years the idea that plants are communicating has become much more accepted,” says Richard Karban, an evolutionary ecologist at the University of California, Davis. “The evidence for that is now substantial, and it’s exciting to unravel all these different realms of plant communication.”
Whispers on the wind
© EERIK/ISTOCKPHOTO.COMIn 1983, plant scientists Jack Schultz and Ian Baldwin reported that intact maple tree saplings ramped up their defense systems when exposed to herbivore-damaged maples. The injured trees, they suggested, were alerting neighbors to the presence of a predator by releasing chemical signals into the air. But the plant research community didn’t buy it. The results were difficult to replicate, critics pointed out, and many questioned how a trait that benefits neighboring plants but not the emitter could be evolutionarily stable. By the late 1980s, “most ecologists felt these ideas had been debunked and that it was time to move on,” says Karban.
A decade later, however, a trickle of more carefully designed experiments began to yield convincing evidence to the contrary. In 2000, Karban showed that wild tobacco plants grown in close proximity to sagebrush plants whose leaves had been clipped became resistant to herbivores, ostensibly in response to VOCs released by the sagebrush.2 Other researchers soon reported similar VOC-induced defense responses—both intra- and interspecies—in several other plants, including lima bean, broad bean, barley, and corn. And in 2006, Karban showed that VOCs released by damaged sagebrush induce herbivore resistance in plants growing at distances of up to 60 cm, well within the range of sagebrush neighbors in nature.3
By now the phenomenon of VOC-based plant communication is well described. In several cases, it has also been demonstrated that volatile cues increase fitness in receiver plants. In one study, lima bean plants exposed to herbivore-induced VOCs lost less leaf mass to herbivores and produced more new leaves than controls, for example.4 But no experiment has yet demonstrated that volatile signaling between neighboring plants can benefit the emitting plant, prompting some researchers to suggest that “eavesdropping” is a more accurate description of what has been observed than “intentional” communication.
Either way, researchers who doubt that plants would have evolved to be altruistic have ruminated on the old question of the evolutionary origins of the phenomenon. Perhaps the ability to synthesize and emit VOCs could simply be an unavoidable consequence of non-communicative functions, such as repelling herbivorous insects and attracting insects that parasitize those herbivores. Another possibility is that external communication channels are merely an extension of within-plant signaling. In sagebrush, lima bean, and poplar, VOCs released from damaged parts of a plant induce resistance in intact sections of the same plant, suggesting that each individual plant uses the signals to coordinate its own physiological responses. “The interplant signaling we see may be a result of plants co-opting that process,” explains Karban.
Alternatively, VOC-based signaling between plants may have been favored because it enhances the “extended fitness” of the emitter by benefitting its related conspecifics: a strategy known as kin selection. This idea gained support from a study published last February, in which Karban and colleagues found that airborne communication was more effective among sagebrush plants that were closely genetically matched than among those that were more distantly related.5 “If communication is more effective among kin, it is less likely that plants are giving away information to potential competitors and more likely that it will benefit close relatives,” says Karban. (See sidebar: “Foliage Family Values.”)
While the evolutionary explanation for volatile communication among plants remains open to debate, researchers have been working to identify and chemically characterize VOCs and to figure out how they encode messages. Gas chromatography–mass spectroscopy has unveiled various compounds that function as plant-to-plant signals, and such work has made it increasingly clear that specific blends of those compounds dictate the content of the messages. In 2011, for example, Japanese researchers found that in herbivore-damaged daisies, eliminating any one compound from a mixture of five VOCs, which induces insecticide production in neighbors, significantly reduced the expression of genes associated with insecticide biosynthesis in those plants.6
“Individual compounds are the words,” says Jarmo Holopainen, an ecologist at the University of Eastern Finland, “and these words are combined to make specific sentences.” Unfortunately, he adds, researchers know little about what these volatile signals mean to a plant and how they are perceived. “We’ve made very little progress in deciphering this chemical code.”
© LOGAN PARSONSPlant gossip is not only spread on the breeze; the rhizosphere crackles with chatter, too. Over the past few years, a team led by Ariel Novoplansky of Ben-Gurion University of the Negev in Israel has produced compelling evidence that plants eavesdrop on hints of their neighbors’ distress through their root systems.
Novoplansky’s team planted six garden pea plants so that each pot contained the roots of two different plants. The researchers then subjected the first plant in each row to drought-like conditions and evaluated the response of its neighbors by measuring the width of the microscopic pores, called stomata, on leaf surfaces, which close in response to drought stress.
Fifteen minutes after drought was initiated, the stressed plant closed its stomata—as did its nearest unstressed neighbor, suggesting some sort of drought warning sign had been passed between the two. After an hour, all five neighbors, each more distant from the stressed plant—the only one that actually experienced drought-like conditions—had also shuttered their stomata, indicating that they, too, received the message to prepare for drought.7 Importantly, in a control setup where root contact between neighboring plants was blocked, pores stayed open, indicating that the message was somehow being passed between roots.
“The finding that plants communicate stress cues via roots was itself novel,” says Novoplansky. “But for me another aspect was more interesting and important: that unstressed neighbors not only responded as if exposed to drought themselves, but also released more of the same cue, which was in turn perceived by further, more remote, unstressed plants.”
Novoplansky’s team has since observed the same phenomenon in garden peas under more realistic, field-like conditions and in three wild plant species, and he suspects that root-based stress cuing could be common in nature.8 The mechanisms underlying this ability are still under investigation, but the cue is almost certainly chemical, says Novoplanksy: when researchers extract soluble chemicals released into the soil by drought-stressed roots and apply them to unstressed plants, they see the same response. His team is currently doing metabolomic studies of root exudates to pinpoint the compound or combination of compounds that carry the message. “The hottest candidate for the vector is abscisic acid (ABA), a hormone involved in plant responses to drought and osmotic stress,” he says. “But I wouldn’t be surprised if it was something else.”
Meanwhile, other researchers are starting to explore another underground plant communication system, one in which messages are sent through the labyrinth of hairlike fungal filaments that festoon the roots of the vast majority of plants on the planet—including important crops such as wheat, rice, maize, and barley. These mycorrhizal fungi are involved in an important mutualistic relationship: in exchange for sugars, they provide plants with much-needed phosphorus and nitrogen. In many cases, the fungi connect the roots of neighboring plants to form common mycelial networks (CMNs), which play a major role in recycling soil nutrients and water. And as Aberdeen’s Johnson revealed last summer, CMNs are also a means of communication. The stringy white hyphae act like fiber-optic cables, carrying information between plants of the same or even of different species. (See “Fighting Microbes with Microbes,” The Scientist, January 2013.)
This idea first gained credence in 2010, when a team at South China Agricultural University in Guangzhou showed that interplant connections via CMNs led to increased disease resistance in healthy tomato plants connected to tomato plants that had previously been infected with the fungal pathogen that causes leaf blight.9 The work of Johnson and Babikova, published last year, provided the first evidence that signals warning of herbivore damage can also be transmitted via CMNs.
“Most research into mycorrhizal networks has focused on their role as biological marketplaces,” says Johnson, “but we’ve now shown that they could have an additional role as a really effective way to transmit messages.”
Subsequent work by Johnson’s group found that CMN-mediated signals elicit behavioral changes within 24 hours of an aphid infestation.10 “That’s important because the signaling has to be quick to be ecologically relevant,” says Johnson.
CMNs may also carry signals over far greater distances than airborne volatiles can. One 2009 study documented a fungal network that wove its way through an entire forest, with each tree connected to dozens of others over distances as great as 20 meters.11 Still, Johnson notes, communication within extensive mycelial networks such as these has yet to be demonstrated in the field.
For Johnson and his colleagues, the next step is to use transcriptomics to see which plant genes are expressed in response to aphid attacks. He says he may also compare proteomic analyses of CMN-connected roots with unconnected roots to identify any compounds that differ between the two systems. But it won’t be easy, he says. “Pinning down the molecules involved is going to be a slog.”
Monica Gagliano’s first attempt to publish evidence suggesting that plants might communicate with each other using sounds was met with rank disbelief. Her manuscript was rejected by six different journals in 2010 and 2011. “It was dismissed as something that is not possible,” says Gagliano, an evolutionary ecologist at the University of Western Australia in Perth.
Undeterred, Gagliano kept plugging away. In April 2012, after she had repeated her experiments and addressed comments from seven different reviewers, PLOS ONE accepted the paper. The study showed that chili plant seedlings grown next to fennel germinated more quickly than seedlings grown with conspecifics. Gagliano and her colleagues suspect the chili plants are compensating for the presence of the fennel, which is known to release chemicals that inhibit the growth of other plants. Remarkably, however, all known interplant communication pathways—airborne volatiles, root contact, and common fungal networks—were blocked. The results begged for an alternative explanation.
In an article reviewing the evidence suggestive of plants’ use of sound as a communication medium, Gagliano and colleagues cited a study showing that the roots of young corn plants grown in water make clicking sounds, and that when sounds in the same frequency range were played back to the roots, they responded by bending toward the source.13
“We’ve shown that plants can recognize when they’re growing next to a ‘bad neighbor’ and change their growth behavior accordingly, even when we remove all the channels of communication we know about,” says Gagliano. “We also have some evidence that there is an emission [of sound] and a response of some sort. We are not ruling out other possibilities, of course, but we think this other channel of communication might be acoustic.”
Theoretically, she says, sound has several advantages over chemical signaling: it propagates faster and over greater distances, and it can be generated with fewer energy costs.14 But behavioral ecologist Carel ten Cate of the University of Leiden in the Netherlands points out that taking advantage of such putative benefits would require sensory mechanisms yet to be described in plants.15 Plants do generate sounds at frequencies outside the range of human hearing, but it’s not clear how they are produced or whether plants can detect sounds at all. “There are many outstanding questions,” Gagliano admits.
Despite widespread skepticism in the plant research field, Gagliano has received some encouragement. UC Davis’s Karban, for example, is cautiously enthusiastic. “She’s presenting results that don’t fit conventional wisdom . . . but she is repeatedly getting results that are very difficult to explain based on the mechanisms we’re currently aware of,” says Karban, noting the parallels between Gagliano’s struggles and his own situation in the 1990s, when the field was reluctant to entertain the idea that plants can communicate with airborne volatiles. “Whether or not the explanation she favors is the right one,” he adds, “I think that she’s gotten results that, as a field, we need to come to grips with.”
Applications for agriculture?
© URSULA ALTER/ISTOCKPHOTO.COMWhether they’re studying volatiles drifting on the breeze or phytochemicals zipping through subterranean fungi, researchers are now bent on elucidating the relevant receptors and deciphering the molecular lingua franca of plant communication. They could then begin to clarify the ecological significance of the phenomenon and, potentially, help farmers grow hardier crops.
Understanding how plants perceive airborne volatile signals, for instance, could inform the genetic engineering of crops that are hypersensitive to cues from sacrificial “beacon” plants that are deliberately damaged to emit signals that trigger neighboring plants to activate their antipredator and/or antipathogen defenses. And if researchers could pinpoint the compounds that act as vectors for stress cues passed between roots, they could potentially “train” crop seedlings to better cope with drought and other stresses.
“I think it can [be a successful strategy], but we have to put in the work to make it happen,” says Novoplansky. “You’re dealing with farmers’ livelihoods, so you have to be certain it will work in realistic agricultural settings,” agrees Johnson, who collaborates with scientists at the UK’s James Hutton Institute and Rothamsted Research, both of which are dedicated to increasing agricultural productivity. “Applying our limited knowledge [of plant-communication mechanisms] to agriculture is a big jump,” he says, “but it is definitely on the horizon.”
Regardless, one message has emerged loud and clear from those studying this new realm of botanical interaction: despite not possessing eyes, ears, or a nervous system, plants are anything but uncommunicative. Rather, the latest findings speak of a plant kingdom brimming with chatter. “When I did my PhD [in the late 1980s], all this stuff was considered very weird,” recalls Novoplansky. “Today, there is no doubt. We now recognize that plants are capable of some very sophisticated exchanges of information with other plants. This idea is not strange anymore.”
In 2007, Susan Dudley of McMaster University in Ontario, Canada, and graduate student Amanda File showed that a beach weed called sea rocket, which is common on the shores of the Great Lakes, senses whether it’s growing among siblings or unrelated plants of the same species. When sea rocket detects strangers, it allocates more resources toward sprouting nutrient-grabbing roots, but when it recognizes kin, it graciously restrains itself.1
Since then, researchers have demonstrated kin recognition in several other plant species. The common model organism Arabidopsis thaliana, for example, reins in root development when growing among brethren. Pale jewelweed (Impatiens pallida), on the other hand, reduces leaf growth and elongates and branches its stems in the presence of kin—likely to reduce shading of siblings in the woody areas where it grows, in which light acquisition is a priority.2
Together with Harsh Bais of the University of Delaware, Dudley has also demonstrated that Arabidoposis’s ability to recognize kin depends on the secretion of soluble chemicals from roots.3 The problem is, the researchers have no idea which compounds are important. “Roots put out a lot of chemicals,” says Dudley, “and we don’t know which matter; which are serving as name tags.”
Nevertheless, researchers have been thinking about the evolutionary dynamics underlying such adaptations. “If plants can recognize their siblings and agree not to waste resources competing against them, then the group as a whole benefits,” Dudley explains. But, she adds, precious few studies have measured whether family groups actually do benefit from kin-dependent behavioral changes. “If we want to test our predictions, we have to see whether differential responses have fitness consequences.”
In 2012, Dudley and File documented some of the first evidence along those lines. They showed that ragweed grown among kin develop larger common mycelial networks—through which plants and fungi trade nutrients—than those grown among non-kin, and that ragweed plants with increased root colonization were better protected against pathogens. Greater fungal abundance was also associated with higher leaf-nitrogen levels, indicative of healthy plants.4 “We have more evidence [that plants benefit from kin recognition] in the pipeline,” says Dudley. “Now we need to see what happens out in the field.”
- Z. Babikova et al., “Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack,” Ecol Lett, 16:835-43, 2013.
- R. Karban et al., “Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush,” Oecologia, 125:66-71, 2000.
- R. Karban et al., “Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication,” Oecologia, 87:922-30, 2006.
- C. Kost, M. Heil, “Herbivore-induced plant volatiles induce an indirect defense in neighboring plants,” J Ecol, 94:619-28, 2006.
- R. Karban et al., “Kin recognition affects plant communication and defence,” Proc R Soc B, 280:20123062, 2013.
- Y. Kikuta et al., “Specific regulation of pyrethrin biosynthesis in Chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants,” Plant Cell Physiol, 52:588-96, 2012.
- O. Falik et al., “Rumor has it . . . : relay communication of stress cues in plants,” PLOS ONE, 6:e23625, 2011.
- O. Falik et al., “Plant responsiveness to root-root communication of stress cues,” Ann Bot, doi:10.1093/aob/mcs045, 2012.
- Y.Y. Song et al., “Interplant communication of tomato plants through underground common mycelial networks,” PLOS ONE, 5:e13324, 2010.
- Z. Babikova et al., “How rapid is aphid-induced signal transfer between plants via common mycelial networks?” Commun Integr Biol, 6:e25904, 2013.
- K.J. Beiler et al., “Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts,” New Phytol, 185:543-53, 2010.
- M. Gagliano et al., “Out of sight but not out of mind: alternative means of communication in plants,” PLOS ONE, 7:e37382, 2012.
- M. Gagliano et al., “Toward understanding plant bioacoustics,” Trends Plant Sci, 17:323-25, 2012.
- M. Gagliano, “Green symphonies: a call for studies on acoustic communication in plants,” Behav Ecol, doi:10.1093/beheco/ars206, 2012.
- C. ten Cate, “Acoustic communication in plants: Do the woods really sing?” Behav Ecol, doi:10.1093/beheco/ars218, 2012.