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Plant biology

Electric defence

Nature volume 500, pages 404405 (22 August 2013) | Download Citation

Herbivory and mechanical wounding in plants have been shown to elicit electrical signals — mediated by two glutamate-receptor-like proteins — that induce defence responses at local and distant sites. See Article p.422

The mammalian nervous system can relay electrical signals at speeds approaching 100 metres per second. Plants live at a slower pace. Although they lack a nervous system, some plants, such as the mimosa (Mimosa pudica) and the Venus flytrap (Dionaea muscipula), use electrical signals to trigger rapid leaf movements. Signal propagation in these plants occurs at a rate of 3 centimetres per second — comparable to that observed in the nervous system of mussels. On page 422 of this issue, Mousavi et al.1 address the fascinating yet elusive issue of how plants generate and propagate electrical signals. The authors identify two glutamate-receptor-like proteins as crucial components in the induction of an electrical wave that is initiated by leaf wounding and that spreads to neighbouring organs, prompting them to mount defence responses to a potential herbivore attack.

As sessile organisms, plants have evolved diverse strategies to combat herbivores. These include mechanical defences, such as the thorns found on rose bushes, and chemical deterrents, such as the insect-neurotoxic pyrethrins of the genus Chrysanthemum. However, some plants do not invest in continuous defensive structures or metabolites, relying instead on the initiation of defence responses on demand2. This strategy requires an appropriate surveillance system and rapid communication between plant organs. A key player in orchestrating these reactions is the lipid-derived plant hormone jasmonate, which rapidly accumulates in organs remote from the site of herbivore feeding3.

“Electrical signals evoked near the site of attack spread to neighbouring leaves at a maximum speed of 9 centimetres per minute.”

Mousavi et al. used thale cress (Arabidopsis thaliana) plants and Egyptian cotton leafworm (Spodoptera littoralis) larvae as a model of plant–herbivore interactions. The researchers placed the larvae on individual leaves and recorded changes in electrical potentials using electrodes grounded in the soil and on the surface of different leaves. The leaf-surface potential did not change when a larva walked on a leaf, but as soon as it started to feed, electrical signals were evoked near the site of attack and subsequently spread to neighbouring leaves at a maximum speed of 9 centimetres per minute. The relay of the electrical signal was most efficient for leaves directly above or below the wounded leaf. These leaves are well connected by the plant vasculature, which conducts water and organic compounds, and is a good candidate for the transmission of signals over long distances.

At all sites that received the electrical signals, jasmonate-mediated gene expression was turned on and initiated defence-responsive gene expression. In a mutant A. thaliana plant lacking the receptor for jasmonate, an electrical signal was propagated but no defence response was elicited. Defence responses also failed to occur at remote sites when the transmission of the electrical signal was prevented by ablation of the damaged leaf before the signal had passed the leaf stalk. These fascinating observations clearly demonstrate that electrical signal generation and propagation have a crucial role in the initiation of defence responses at remote sites upon herbivore attack.

The salivary secretions of herbivores contain elicitor molecules that are recognized by the host plant4,5 and that induce jasmonate-mediated defence responses. However, Mousavi and colleagues found that extensive mechanical wounding (in the absence of herbivory) also initiated electrical signal transmission and jasmonate biosynthesis. In addition, a herbivore-response gene-expression pattern could be artificially induced by applying electric pulses that mimicked the plant's electrical signals. Thus, it remains unclear how the electrical signals are interpreted to stimulate jasmonate biosynthesis.

The authors next investigated which cellular components are involved in generating the electrical signals, by screening A. thaliana plants defective in candidate ion pumps and channels. They found that loss of function of certain members of the glutamate-receptor-like (GLR) family of ion-channel proteins — some of which form calcium-ion-permeable channels that can be activated by agonists such as glutamate and serine6,7 — affected wound-induced signal generation. Indeed, combined disruption of the genes encoding two of these channels, glr3.3 and glr3.6, resulted in the electrical wave no longer propagating after wounding.

Thus, it seems that herbivory and mechanical wounding trigger the local generation of an electrical signal through the activity of GLRs; this signal then spreads to neighbouring organs where the biosynthesis of jasmonate is induced, in turn triggering jasmonate-dependent defence responses (Fig. 1). Several questions emerging from this study will foster future research efforts. For example, how do feeding and mechanical wounding activate the GLRs? Might calcium ions be involved in the generation and maintenance of the electrical wave? It will also be intriguing to elucidate whether GLRs relay the faster electrical signalling that triggers movement in mimosa and the Venus flytrap.

Figure 1: Protective responses induced by electrical signalling.
Figure 1

On herbivore attack, levels of the plant hormone jasmonate increase, triggering defence responses. Mousavi et al.1 show that leaf injury, caused by herbivory or mechanical wounding, induces the transmission of electrical signals that are generated by the activity of glutamate-receptor-like (GLR) ion channels. These signals induce the formation of jasmonate at local and distant sites in the plant.

Plant wounding is also known to evoke an extracellular wave of reactive oxygen species (ROS), which propagates at a speed8 comparable to that recorded by Mousavi et al. for the electric signals. But the authors found that inhibiting wound-induced ROS generation did not substantially disrupt electric signalling, so it remains to be determined whether there is an interaction between wound-induced ROS signalling and electric signalling.

It is interesting to note that plant GLRs are structurally related to vertebrate ionotropic glutamate receptors, which are important for rapid excitatory synaptic transmission in the nervous system. Insect feeding on leaves has also been shown to generate an electric wave by a continuous relay of cell-membrane depolarizations4 that is reminiscent of excitatory signal propagation in animals. Together, these findings imply that ionotropic glutamate-receptor-type proteins must have existed before animals and plants diverged. These ancestral proteins might already have functioned in the generation of long-distance warning signals to elicit the timely initiation of protective responses.

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  1. Alexander Christmann and Erwin Grill are in the Department of Plant Sciences, Life Science Centre Weihenstephan, Technische Universität München, D-85354 Weihenstephan, Germany.

    • Alexander Christmann
    •  & Erwin Grill

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Correspondence to Alexander Christmann or Erwin Grill.

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