Plant Communication and Signaling

Plant signaling operates on at least four nested scales, each with distinct carriers. At the intracellular/intercellular scale, wounding triggers calcium waves, reactive oxygen species (ROS) bursts, and changes in membrane potential that propagate cell-to-cell through plasmodesmata and the apoplast. At the whole-plant (systemic) scale, a damaged leaf sends a signal through the phloem and xylem — part electrical, part chemical — that reaches distant, undamaged leaves within 1–30 minutes and induces defenses there before the herbivore ever arrives. At the plant-to-plant scale, volatile organic compounds released from damaged tissue diffuse through air and can be perceived by neighboring plants (or even other branches of the same individual not connected by direct vascular signaling), which then prime or activate their own defenses. At the plant-to-third-organism scale, the same volatile blends serve as foraging cues for natural enemies of herbivores — parasitoid wasps, predatory mites, predatory bugs — recruiting an "enemy of my enemy" bodyguard service known as indirect defense (contrasted with direct defense, such as toxins or protease inhibitors that the plant itself deploys). Two conceptual traps must be avoided from the outset. First, "communication" in the strict evolutionary sense requires that a signal benefits the sender by influencing a receiver — this is well established between plants and their insect bodyguards, but for plant-to-plant volatile signaling the evolutionary framing is contested: is the emitting plant "warning" kin (a sender-benefit trait, favored by kin selection) or is the receiving plant simply eavesdropping on cues that primarily serve the emitter's own systemic signaling (a "public information" or incidental view)? Both mechanisms are compatible with the same molecules; the field distinguishes cue (informational value evolved for the receiver, i.e., true communication) from eavesdropping (informational value not selected for by the sender) carefully, and for plant volatiles the evidence supports mostly the latter, with kin-selected true signaling remaining a live but harder-to-prove hypothesis. Second, none of this implies plant "intelligence" or intention in the cognitive sense; all of it is explicable by ordinary stress-signal transduction, hormone action, and inducible defense biochemistry operating at a distance and across organisms.

Step 1 — Local wound perception. Herbivore chewing or mechanical damage ruptures cells, releasing cell-wall fragments (oligogalacturonides), ATP, and glutamate-like amino acids into the apoplast. These are perceived by plasma-membrane receptors, triggering a rapid influx of Ca²⁺ into the cytosol within seconds. This calcium signal, together with membrane depolarization, is the trigger for the systemic electrical signal.

Step 2 — Systemic electrical signaling. Two types of long-distance electrical signals have been documented. Action potentials (APs), familiar from animal neurons, are also generated in some plants but travel relatively short distances and are self-propagating and independent of the wound's severity. Variation potentials (VPs), first characterized in detail by workers following on from early 20th-century plant electrophysiology and refined in modern clamped-electrode studies, are slower, larger, non-self-propagating signals driven by a hydraulic pressure wave in the xylem: wounding causes a local pressure/tension change in the xylem that propagates as a pressure pulse at roughly the speed of water movement, opening or closing ion channels (notably GLUTAMATE RECEPTOR-LIKE, GLR, channels, and mechanosensitive channels) as it passes, and depolarizing the phloem/xylem-associated cells it reaches. Glutamate-receptor-like channels — homologous in domain architecture to animal ionotropic glutamate receptors — were shown by Toyota, Gilroy and colleagues (2018) to be essential for propagating a Ca²⁺ wave from a wound site through the phloem to distal leaves, visualized directly using the genetically encoded calcium indicator GCaMP3 in living Arabidopsis. This calcium wave moves at roughly 1 mm/s and reaches leaves several nodes away within about two minutes.

Step 3 — Chemical relay: systemin and jasmonate. In tomato and other solanaceous plants, wounding triggers processing of a precursor protein, prosystemin, into an 18-amino-acid peptide, systemin, released into the apoplast. Systemin binds a leucine-rich-repeat receptor kinase (related to the SYR1/SYR2 receptors) on nearby cells, activating a MAP kinase cascade that stimulates the octadecanoid pathway: linolenic acid released from chloroplast membranes is converted via lipoxygenase (LOX), allene oxide synthase (AOS), and allene oxide cyclase (AOC) into 12-oxo-phytodienoic acid (OPDA) and ultimately jasmonic acid (JA) in the peroxisome. JA (and its active conjugate, JA-isoleucine) is the near-universal systemic wound hormone across land plants, playing the role analogous to salicylic acid in pathogen defense (see Plant-Pathogen Interactions and Immunity). JA-Ile promotes degradation of JAZ repressor proteins via the SCF^COI1 ubiquitin ligase complex, releasing MYC2 and other transcription factors to activate wound- and herbivory-responsive genes — most famously, proteinase inhibitor (PI) genes, whose protein products block insect digestive proteases and stunt herbivore growth.

Step 4 — Long-distance transport. Systemin itself may act largely locally to amplify JA synthesis rather than travel far in the phloem; the mobile long-distance signal is now understood to be a combination of the electrical/hydraulic/Ca²⁺ wave (which travels fast, in minutes) and JA or its precursors moving through the phloem (slower, over tens of minutes to hours), reinforcing each other so that distal, undamaged leaves accumulate JA and express PI genes within roughly 30–120 minutes of a single wounding event.

Step 5 — Volatile biosynthesis and release. JA signaling also switches on biosynthesis of volatile organic compounds. Two major classes are released from herbivore-damaged tissue:

• Green leaf volatiles (GLVs) — six-carbon aldehydes, alcohols, and esters (e.g., (Z)-3-hexenal, (Z)-3-hexenol, (Z)-3-hexenyl acetate) produced within seconds to minutes directly from membrane lipids via the same lipoxygenase pathway that feeds into jasmonate synthesis. GLVs are released almost immediately upon any tissue damage — mechanical or herbivore — and are the "fresh-cut-grass smell."
• Herbivore-induced plant volatiles (HIPVs) — terpenoids (mono- and sesquiterpenes), aromatic compounds (methyl salicylate, indole), and homoterpenes, synthesized over hours and requiring not just wounding but chemical elicitors in herbivore oral secretions — most famously volicitin (N-(17-hydroxylinolenoyl)-L-glutamine), identified from beet armyworm caterpillar regurgitant by Alborn, Turlings, and Tumlinson (1997). Volicitin applied to a mechanically wounded maize leaf induces the same volatile blend as real caterpillar feeding, while mechanical wounding alone does not — direct proof that the plant chemically distinguishes "cut" from "eaten."

Step 6 — Perception by receivers. Airborne GLVs and terpenoids are perceived by (a) undamaged parts of the same plant, (b) neighboring plants of the same or different species, and (c) foraging natural enemies. Reception in plant tissue appears to work by the volatile itself (or a derivative) re-entering leaf tissue and being metabolized/perceived in ways that feed into the same JA-signaling machinery, effectively priming (lowering the threshold for) or directly inducing defense gene expression — without requiring vascular connection to the damaged tissue. In parasitoid wasps and predatory mites, volatile blends are detected by antennal olfactory receptors and used for directed flight/walking orientation (odor-plume tracking), a behavior quantified in wind-tunnel and olfactometer assays.

Step 7 — Indirect defense in action. In the classic maize–Cotesia system, corn seedlings damaged by beet armyworm caterpillars release a volatile blend dominated by terpenoids such as (E)-β-caryophyllene and the homoterpene DMNT/TMTT, plus methyl salicylate and indole. Parasitoid wasps of the genus Cotesia use this blend, tracked in a wind tunnel, to locate the caterpillar-infested plant from a distance, then use close-range cues (including the caterpillar's own frass) to pinpoint the host and lay eggs in it. In lima bean attacked by two-spotted spider mites, an analogous volatile blend attracts the predatory mite Phytoseiulus persimilis. This chain — herbivore damage → oral-secretion elicitor → JA-mediated volatile biosynthesis → volatile blend → predator attraction → reduced herbivore load — is now one of the best-characterized multitrophic signaling pathways in ecology.

Step 8 — Root-zone and microbial signaling. Roots continuously exude a cocktail of sugars, organic acids, amino acids, flavonoids, and strigolactones into the rhizosphere. Strigolactones, originally identified as a class of hormones controlling shoot branching, are also potent signals that stimulate hyphal branching in arbuscular mycorrhizal fungi, initiating the symbiosis; in a signaling arms race, some parasitic plants (e.g., Striga) and pathogenic fungi have evolved to eavesdrop on strigolactones to detect a host root. Legume roots exude flavonoids that are perceived by rhizobial bacteria, inducing bacterial nod gene expression and production of Nod factors that the plant, in turn, perceives via LysM-domain receptor kinases to initiate nodule organogenesis (detailed under root-microbe symbiosis, closely related to Plant-Pathogen Interactions and Immunity receptor logic, since both use structurally similar pattern-recognition machinery to distinguish friend from foe). Below-ground volatiles also matter: maize roots damaged by the beetle larva Diabrotica virgifera release the sesquiterpene (E)-β-caryophyllene, which attracts entomopathogenic nematodes that kill the larvae — an underground mirror of the aboveground indirect-defense story, demonstrated by Rasmann and colleagues (2005), who also showed that many North American maize varieties have lost this volatile response through breeding, while a European maize line retained it.

1. Ryan and colleagues: the discovery of systemin and proteinase inhibitor induction (1970s–1991). Clarence Ryan's group first showed in the 1970s that wounding a tomato leaf induces accumulation of proteinase inhibitor (PI) proteins not only at the wound site but throughout the plant, in leaves never touched by the herbivore — the first rigorous demonstration of a systemic wound response with a measurable biochemical endpoint. This ruled out the possibility that induction was merely local damage seen everywhere by coincidence, because control (unwounded) plants showed no such induction and the timing (PI accumulation beginning within roughly 30–60 minutes in distal leaves and peaking around 8 hours) tracked a signal moving away from the wound at a definable rate. In 1991, Pearce, Strydom, Johnson, and Ryan purified and sequenced the actual mobile signal candidate from tomato leaves: an 18-amino-acid peptide they named systemin, the first plant peptide hormone identified. Application of nanogram quantities of synthetic systemin to a cut petiole was sufficient to induce PI gene expression in distal leaves, mimicking wounding — a clean gain-of-function proof that this molecule alone could carry the systemic signal.

2. Farmer and Ryan: jasmonate as the universal wound hormone (1990, 1992). Edward Farmer and Clarence Ryan showed that methyl jasmonate, applied to tomato plants merely by exposing them to its vapor in a sealed chamber (with no physical contact or wounding at all), was sufficient to induce PI gene expression at levels comparable to real wounding. This was a striking result for two reasons: it showed jasmonates were potent enough to act at trace airborne concentrations, and it was one of the first clean demonstrations that a plant volatile could switch on defense gene expression in a physically separate plant — an early piece of evidence for airborne plant-to-plant signaling, alongside the pathway work establishing JA/JA-Ile as the central hub of the wound-response transcriptional program, later confirmed genetically by JA-biosynthesis mutants (e.g., tomato def1, Arabidopsis aos, opr3) that fail to accumulate PI proteins or resist herbivores properly unless JA or its precursors are supplied exogenously.

3. Alborn, Turlings, Tumlinson: volicitin and the discovery that plants "taste" herbivore saliva (1997). Working with beet armyworm (Spodoptera exigua) caterpillars feeding on maize seedlings, this group showed that mechanically wounded maize leaves release a modest volatile blend, but leaves damaged by actual caterpillar feeding release a far richer, JA-amplified blend attractive to parasitoids. The key experiment applied caterpillar regurgitant (oral secretion) to mechanically wounded leaves and found this alone reconstituted the full herbivory-induced blend. Fractionating the regurgitant, they isolated and chemically identified the active elicitor: volicitin, a fatty acid–amino acid conjugate the caterpillar makes by combining plant-derived linolenic acid with the caterpillar's own glutamine. This proved that the plant distinguishes mechanical damage from herbivory chemically, at the level of a specific insect-derived molecule, not merely by degree of tissue loss.

4. Turlings, Tumlinson, Lewis: proof that HIPVs function as foraging cues for parasitoids (1990). In a landmark wind-tunnel study, Turlings and colleagues showed that female Cotesia marginiventris wasps, released downwind of maize seedlings, oriented and flew preferentially toward plants damaged by caterpillar feeding over undamaged plants or plants damaged mechanically without caterpillar saliva. Critically, wasps could not distinguish an infested plant from a clean air control when the odor source was masked, but strongly preferred the herbivore-damaged odor plume when given a choice — direct behavioral evidence that HIPVs alone (not visual or other cues) drive host-plant location, establishing the tritrophic (plant–herbivore–natural enemy) signaling concept experimentally rather than anecdotally.

5. Karban and Baldwin: plant-to-plant volatile communication, from controversial claim to replicated phenomenon (1983 onward). Early reports by Baldwin and Schultz (1983) and Rhoades (1983) that undamaged trees near experimentally damaged neighbors showed increased levels of defensive phenolics were met with skepticism — sample sizes were small, and critics worried about pseudoreplication and confounds (e.g., shared root systems, fungal connections, or simple correlation with regional herbivore outbreaks). Richard Karban and colleagues addressed this over subsequent decades with more rigorous, replicated field experiments on sagebrush (Artemisia tridentata), a species that self-evidently lacks root grafts between individuals over the relevant distances. In these studies, sagebrush branches experimentally clipped (simulating herbivory) release volatiles that, when a neighboring unclipped sagebrush (or an unclipped branch of the same plant not vascularly connected to the clipped branch) was downwind and in volatile-only contact (physically isolated by bagging to exclude direct plant contact and exclude root connections), showed reduced subsequent herbivory damage over a growing season compared with plants downwind of unclipped controls. Karban's group extended this to show the effect is concentration- and blend-specific (particular volatile mixtures matter, not any wound odor), that genetic relatedness between the emitting and receiving plant modulates the effect size (a pattern raised as tentative support for a kin-selection/true-signaling interpretation, though this remains actively discussed), and that the phenomenon is best described as "priming" — the receiving plant is not fully induced but has a faster, stronger defense response upon its own subsequent damage — rather than complete pre-emptive activation. This body of work, spanning field seasons and multiple independent research groups replicating the pattern in other species (including lima bean, poplar, and blueberry), is what moved plant-to-plant volatile signaling from an anecdote into a robust, if mechanistically still-maturing, area of plant ecology.

6. Toyota, Gilroy, and colleagues: visualizing the Ca²⁺/electrical wave in real time (2018). Using Arabidopsis engineered to express the calcium indicator GCaMP3 throughout the plant, this group filmed, in real time, a wave of fluorescence (reporting cytosolic Ca²⁺) spreading from a wound site through the phloem to distant leaves within about two minutes, at a propagation speed consistent with earlier electrophysiological estimates of variation potentials. They showed this wave requires glutamate receptor-like (GLR) channel genes: in glr3.3 glr3.6 double mutants, the calcium wave and the associated distal jasmonate accumulation were strongly impaired. This work connected, for the first time with live imaging and clean genetics, the electrical-signal literature (decades of electrode recordings) to the JA-signaling literature (decades of biochemistry), showing they are mechanistically one continuous pathway rather than two separate phenomena.

Example 1 — Timing a systemic response. A researcher wounds leaf 1 of a young tomato plant at time zero and monitors PI-II gene transcript accumulation, using RT-qPCR, in leaf 1 (local) and leaf 5 (systemic, three internodes away, no direct vascular trace to leaf 1 other than the stem). She records:

Reasoning: Local induction is detectable almost immediately (by 15 min) and rises steeply, consistent with direct wound-site JA synthesis triggered by the systemin/octadecanoid loop acting in and near damaged cells. Systemic induction lags by roughly 30–45 minutes and rises more slowly, consistent with a signal (the Ca²⁺/electrical wave arriving in ~2 min, but requiring subsequent JA biosynthesis and transcriptional induction, which takes tens of minutes) having to first propagate the ~15–20 cm distance from leaf 1 to leaf 5 and then trigger local JA synthesis anew in leaf 5's own cells — it is not that JA itself is shipped in bulk from leaf 1, but that leaf 5 mounts its own JA response once triggered. By 4 hours, systemic and local levels converge, showing the whole plant eventually reaches a comparable defended state. If leaf 5 had shown zero induction even at 4 hours, the simplest interpretation would be a break in vascular continuity (e.g., girdling the stem between leaf 1 and leaf 5 is a classic experimental manipulation, and indeed abolishes or greatly delays systemic PI induction, supporting a phloem/xylem-transmitted signal rather than an air-gap signal within the same plant).

Example 2 — Distinguishing "wound-only" from "true herbivory" volatiles in a bioassay. A student sets up four maize treatments and measures the amount of (E)-β-caryophyllene (a terpenoid HIPV) collected from headspace over 6 hours, then offers each odor source to Cotesia wasps in a four-arm olfactometer, recording the number of wasps (out of 20 released) choosing each arm:

Reasoning: Mechanical wounding alone raises volatile output modestly above the undamaged control (3 vs 0.5 ng/g/h) — this is the GLV/basal-terpenoid response to any tissue damage — but wasp attraction barely rises (4 vs 2 of 20), because the blend composition, not just total quantity, matters for parasitoid recognition, and a purely mechanical wound blend does not resemble a genuine herbivory blend closely enough. Adding caterpillar oral secretion to the wound (mimicking real feeding, per the Alborn/Turlings/Tumlinson logic) causes a roughly 16-fold jump in caryophyllene emission (48 vs 3 ng/g/h) and a large, statistically clear shift in wasp preference (15 of 20 choosing that odor, versus near-chance ~3–4 of 20 for the other three treatments, where chance alone across four arms would predict 5 of 20). The buffer-only control matching the mechanical-wounding-only result rules out the possibility that liquid application itself (rather than the biological content of oral secretion) is driving the effect. This experimental logic — separating damage amount from damage identity (elicitor content) — is exactly how volicitin was functionally implicated before it was even chemically identified, and is the standard design for dissecting any putative elicitor's contribution to a plant signaling response.

Clarence A. Ryan (1931–2015) built much of the biochemical foundation for systemic wound signaling at Washington State University, beginning in the 1970s with the deceptively simple observation that tomato leaves accumulate proteinase inhibitors far from a wound site. Where many plant biochemists of his generation focused on primary metabolism, Ryan pursued a defense-signaling question with a chemist's rigor: purify the active molecule, sequence it, synthesize it, and test whether the synthetic version reproduces the biological effect. That approach delivered systemin in 1991 — still, decades later, one of only a handful of well-characterized plant peptide hormones — and, in collaboration with Edward Farmer, connected peptide signaling to the jasmonate pathway that has become the master regulator of induced defense across the plant kingdom. Ryan's insistence on quantitative, dose-responsive, mutant-validated evidence set the methodological bar that the later volatile-signaling and tritrophic-interaction literature (Tumlinson, Turlings, Baldwin, Karban) would follow.

Agriculture and pest management. Understanding HIPVs underlies "attract-and-reward" and push-pull cropping strategies, where border or intercrop plants are chosen or engineered to emit volatiles that recruit natural enemies of pests, reducing insecticide reliance — a direct agricultural translation of the maize–Cotesia and lima bean–Phytoseiulus work. Breeding programs are re-evaluating whether modern crop varieties have inadvertently lost indirect-defense volatile traits (as documented for some North American maize lines relative to wild/European relatives), motivating breeding or gene-editing efforts to restore these signals without sacrificing yield.

Biopesticide and elicitor-based crop protection. Synthetic methyl jasmonate and other jasmonate-pathway elicitors are used experimentally and commercially as "plant defense activators," priming crops to respond faster to real attack while avoiding the yield costs of constitutive defense expression.

Biological control and conservation. Volatile-based lures mimicking HIPV blends are deployed to monitor or enhance populations of parasitoids and predators in integrated pest management, and understanding of below-ground volatile signaling (e.g., (E)-β-caryophyllene recruiting entomopathogenic nematodes against rootworm larvae) has inspired soil-applied biological control products.

Plant-microbe symbiosis engineering. Strigolactone and flavonoid signaling pathways that recruit mycorrhizal fungi and rhizobia are central targets for reducing synthetic nitrogen and phosphorus fertilizer use, by engineering non-legume crops to better recruit beneficial microbes or by breeding for stronger native signaling.

Forestry and ecosystem management. Field-tested priming effects (as in sagebrush) inform silvicultural and conservation strategies that consider stands of genetically related plants as networks with emergent, population-level defense dynamics rather than collections of independent individuals — a bridge to community-level thinking taken up more fully in Plant Ecology and Community Interactions.

Basic neuroscience-adjacent research. The discovery that plant GLR channels, structurally related to animal ionotropic glutamate receptors, drive long-distance Ca²⁺ signaling has become a touchstone in comparative studies of excitable signaling systems across kingdoms, informing broader questions in Plant Responses to Abiotic Stress about how sessile organisms achieve rapid, coordinated, body-wide responses without a nervous system.

Ask the tutor: How do jasmonate and salicylic acid signaling interact when a plant faces both a chewing herbivore and a biotrophic pathogen at the same time?