Plant communication

For almost two decades, researchers into plant biology have been continually observing surprising capabilities that were thought to be reserved for the animal kingdom. Indeed, plants communicate with each other, develop strategies to combat attackers, warn their neighbors in the event of danger and produce mysterious electrical signals.

Chemical signals as a means of communication and cooperation between plants

It was during the 1980s that a biologist and a chemist, Jack Schultz and Ian Baldwin, opened the way through their work published in the scientific journal “Science” [Baldwin 1983]. The two authors observed that young poplar and maple plants where the foliage was partially damaged increased their concentration of phenolic compounds over 36-52 hours, and so did healthy neighboring plants.

Thus it was demonstrated for the first time that an airborne signal from the tissues of a damaged plant could stimulate biochemical changes in neighboring individuals, and in this way influence, for example, the feeding and growth of phytophagous insects.

The work of South African biologist Wouter van Hoven in the 1990s highlighted a surprising mutualistic defense mechanism in acacias (Acacia drepanolobium Harms ex Y. Sjöstedt) in the South African Transvaal reserve in the face of excessive grazing from kudu antelopes. Following the unexplained death of more than 2,000 of these ruminants, the researcher from Pretoria conducted a scientific investigation which initially showed that the death of the antelopes was due to the presence of abnormally high concentrations of tannins compared to those usually found in association with a significant consumption of foliage. Some tannins ingested at high doses can give rise to acute digestive toxicity in ruminants [Robbins, 1987]. The establishment of induced chemical defenses in plants (production of alkaloids, tannins and other constituents that are harmful to animals) is a well-known mechanism, but the next part was less so.

Full understanding came later when it was observed that branches damaged by the passing of ruminants emitted a volatile organic compound, ethylene. This has the effect of triggering the production of tannins in the neighboring acacias before the kudus even arrive. Thus the acacias warn their neighbors of the danger, and in response they activate their defense system [Van Hoven 1985, Van Hoven 1991].

Communication between plants can also take place underground. This is the case of the tomato with the help of a root fungus with which it forms mycorrhizas. During one study, after planting tomato plants in pairs, the foliage of one of the two plants was infected with a pathogenic fungus. It was found that the neighboring healthy plant begins to produce defense enzymes usually produced during a fungal attack. In contrast, if the root fungi network is absent or a wall prevents it from connecting the two plants, the defenses of the healthy tomato are not triggered [Song 2010].

Thus, defense mechanisms against parasites or predators can be implemented in response to signals emitted by neighboring plants that have been attacked, before they themselves are victims of an attack. Good examples of mutual assistance and cooperative relationships between plants!

Several studies show that many plants are capable of recognizing whether their neighbors are of the same species and, moreover, if a “kinship” tie exists (kin recognition). During the first study of the genus, conducted in 2007, it was found that Cakile edentula (Bigelow) Hook seedlings growing next to seedlings originating from seeds of the same individual, after 40 days produced fewer roots than pairs of seedlings that do not originate from seeds of the same individual, thus preferring to invest their energy in the development of their reproductive system [Dudley 2007].

A final good example that can be given of cooperation is that of the Douglas fir (Pseudotsuga menziesii (Mirb.) Franco). Canadian ecologist Suzanne Simard and her team wrapped pine branches in plastic bags containing carbon-14-labeled CO₂ She found that part of the radioactivity was transferred to many of the surrounding trees, but in particular that the most significant transfer was between the old, largest trees and the young ones growing at their feet, most often originating from their seeds. The nourishment is transported by fungi in the ground which connect the roots of the trees to each other (mycorrhizas).

The old trees thus play the role of hubs, interconnecting all the individuals and distributing the flow of nutrients, in particular to the young ones [Simard, 2012].

Electrical signals as a means of communication within plants 

Although we have known that plants have electrical activity, we have long underestimated its significance. The team led by Edward Farmer from Lausanne University asked “if these electrical signals generated when the plant is damaged can trigger defense mechanisms” as the defense proteins are produced not only in the attacked parts but also in the healthy parts of the plant. Using thale cress (Arabidopsis thaliana (L.) Heynh.) as a model, the team was able to identify the genes that trigger the electrical signal and to verify the link with the activation of defense proteins away from the injury. The results, published in 2013 in the famous journal Nature, show that three GLR (glutamate receptor-like) genes, similar to those in animals, are involved in this electrophysiological process [Moussavi 2013].

Farmer explains that “what is surprising, is that these genes are very similar to the genes activated in the fast synapses of the human brain, whereas a plant does not have any neurons. This is very intriguing and exciting.”

The hypotheses focus on the plant’s vascular system, composed of phloem (tissue that transports sap from the leaves to the rest of the plant) and xylem (tissue that transports sap—water and mineral salts—from the roots to the rest of the plant). According to Farmer, “many researchers think it is one or the other that is involved in electrical transmission: at my laboratory we believe that these two types of cells work together to send the signal. But we still don’t know which does what.”

According to Francis Bouteau from the membrane electrophysiology laboratory (Sorbonne Paris Cité) “electrical communication among plants and the circulation of messages via membrane depolarization waves were demonstrated years ago. And we now know that the phenomena of exocytosis and endocytosis exist among plants, namely the expulsion and absorption of molecules by membranes, which very much resemble nerve synapses in animals. Obviously, plants do not have neurons, synapses, or any organ that can be called a brain; with them, everything goes much more slowly... but we can definitely talk about plant neurobiology.”

Furthermore, the presence of classical neurotransmitters in the animal kingdom, involved in numerous functions in both the central and peripheral nervous systems—serotonin (or “phytoserotonin”) [Ramakrishna 2011], dopamine and glutamate—has been described in plants. Their role is becoming better understood [Roshchina 2010].

Auxin, a particularly important plant hormone, has even been compared to a neurotransmitter.

Didier Guédon, Expert on the French Pharmacopoeia Committee

Bibliography:

Baldwin IT, Schultz JC. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 1983;221:277-9.
Dudley SA, File AL. Kin recognition in an annual plant. Biol Lett 2007;3:435–8.
Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature 2013;500(7463):422-6.
Ramakrishna A, Giridhar P, Ravishankar GA. Phytoserotonin, a review. Plant Signal Behav 2011;6:800–9.
Robbins CT. Role of tannins in defending plants against ruminants: reduction in dry matter digestion? Ecology 1987;68:1606-15.
Roshchina VV. Evolutionary considerations of neurotransmitters in microbial, plant, and animal cells. In Microbial endocrinology. Lyte M et al. (Eds), p. 17-52, Springer 2010.
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Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 2010; 5: e13324.
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Van Hoven W. The tree’s secret weapon. South African panorama 1985;30:34-7.