A L E X A N D E R C H R I S T M A N N & E R W I N G R I L L
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 sig-nals 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 mus-sels. 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 chemi-cal deterrents, such as the insect-neurotoxic pyrethrins of the genus Chrysanthemum. However, some plants do not invest in con-tinuous 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.
Mousavi et al. used thale cress (Arabi-dopsis 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 candi-date for the transmission of signals over long distances.
At all sites that received the electrical sig-nals, 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 elec-trical signal was propagated but no defence response was elicited. Defence responses also failed to occur at remote sites when the trans-mission of the electrical signal was prevented by ablation of the damaged leaf before the signal had passed the leaf stalk. These fasci-nating 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 con-tain 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 her-bivory) also initiated electrical signal transmis-sion and jasmonate biosynthesis. In addition, a herbivore-response gene-expression pattern could be artificially induced by applying elec-tric pulses that mimicked the plant’s electri-cal signals. Thus, it remains unclear how the electrical signals are interpreted to stimulate jasmonate biosynthesis.
The authors next investigated which cell-ular components are involved in generating the electrical signals, by screening A. thaliana plants defective in candidate ion pumps and
P L A N T B I O L O G Y
Electric defence 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 Letter p.422
Jasmonate
Electricalsignalling
GLRchannel
Defence
Figure 1 | Protective responses induced by electrical signalling. 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.
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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 gen-erat ion. Indeed, combined disruption of the genes encoding two of these channels, glr3.3 and glr3.6, resulted in the elec-trical wave no longer propagating after wounding.
Thus, it seems that herbivory and mechanical wounding trig-ger the local generation of an electrical sig-nal 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 emerg-ing 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 genera-tion 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.
Plant wounding is also known to evoke an extracellular wave of reactive oxygen species (ROS), which propagates at a speed8 compa-rable to that recorded by Mousavi et al. for the electric signals. But the authors found that inhibiting wound-induced ROS gen-eration 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. ■
Alexander Christmann and Erwin Grill are in the Department of Plant Sciences, Life Science Centre Weihenstephan, Technische Universität München, D-85354 Weihenstephan, Germany. e-mails: [email protected]; [email protected]
1. Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellenberger, S. & Farmer, E. E. Nature 500, 422–426 (2013).
2. Meldau, S., Erb, M. & Baldwin, I. T. Ann. Bot. 110, 1503–1514 (2012).
3. Howe, G. A. & Jander, G. Annu. Rev. Plant Biol. 59, 41–66 (2008).
4. Maffei, M., Bossi, S., Spiteller, D., Mithöfer, A. & Boland, W. Plant Physiol. 134, 1752–1762 (2004).
5. Dinh, S. T., Baldwin, I. T. & Galis, I. Plant Physiol. 162, 2106–2124 (2013).
6. Vincill, E. D., Bieck, A. M. & Spalding, E. P. Plant Physiol. 159, 40–46 (2012).
7. Michard, E. et al. Science 332, 434–437 (2011).8. Miller, G. et al. Sci. Signal. 2, ra45 (2009).
A S T R O P H Y S I C S
Twinkling starsA correlation between stellar brightness variations and the gravitational acceleration at a star’s surface has been observed that allows this acceleration to be measured with a precision of better than 25%. See Letter p.427
J Ø R G E N C H R I S T E N S E N - D A L S G A A R D
“Twinkle, twinkle little star, how I wonder what you are.” Given the wording of this old nursery
rhyme, it is highly satisfying that Bastien et al.1 (page 427 of this issue) find that a star’s twinkle may hold the key to deter-mining its properties. The authors used data from NASA’s Kepler space mission to show that accurate measurements of variations in a star’s light reveal informa-tion about the acceleration of gravity at the star’s surface. This result is significant for the characterization of stars, and in par-ticular for the determination of radii of stars hosting planetary systems.
Essentially all knowledge about distant stars derives from observation of the light emitted by their outer layers. Therefore, the properties of these layers are central to the study of stars. These properties have conventionally been obtained from ana-lysis of stellar spectra, but the gravitational acceleration (g) has proved notoriously difficult to nail down, and the resulting
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uncertainty about this quantity has substantial effects on the measurement of other proper-ties, such as temperature and chemical com-position.
Analyses of variations in stellar brightness caused by stellar oscillations (asteroseismol-ogy), particularly those based on the spectac-ular data from the Kepler mission2, provide precise determinations of g but require exten-sive observations and complex analysis, which
are available for only a limited number of stars. However, stellar oscillations are not the only factor that contributes to variations in brightness. Bastien and col-leagues show that g is also reflected in these variations.
One of the properties of a star’s bright-ness variations measured by Bastien et al. is the total range of the variations. This includes variations on timescales of days that may have a number of causes, such as the rotation of large starspots across the disc of the star. In addition to this total range, the authors characterize the vari-ations in terms of what they call ‘flicker’ — variations that occur on timescales shorter than eight hours (Fig. 1). In the Kepler data, they identify a substantial fraction of Sun-like stars that have a low range, defining what they dub ‘flicker floor’ (see Fig. 3 in the paper). Bastien et al. find that, for a subset of these flicker-floor stars whose precise values of g are known from asteroseismology2, there is a close correlation between flicker and g, with the amplitude of the flicker increas-ing with decreasing g. For other stars on
Figure 1 | Stellar variability. Bastien et al.1 describe the brightness variations of Sun-like stars in terms of variations on timescales of days (total range; here about 1 part per thousand) and of variations on timescales shorter than 8 hours (flicker; here roughly 0.03 p.p.t.). The red curve shows the result of smoothing the blue curve with an 8-hour running mean.
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. 1
“Electrical signals evoked near the site of attack spread to neighbouring leaves at a maximum speed of 9 centimetres per minute.”
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