Synomone

Synomone (from the Greek syn, "together" or "with," and hormōn, "to excite") is an interspecific semiochemical—an information-bearing volatile or water-soluble chemical compound—produced and released by an individual of one species (the emitter) that evokes a behavioral, developmental, or physiological response in an organism of a second species (the receiver) that is adaptively favorable to both the emitter and the receiver (+/+). Introduced in 1977 by the Dutch entomologist Louis M. Schoonhoven and formalized in 1982 by Donald A. Nordlund and W. J. Lewis to complete the classic interspecific allelochemical triad alongside allomones (+/−) and kairomones (−/+), synomones serve as the chemical language of mutualism and tri-trophic indirect defense across terrestrial and marine ecosystems. Their major ecological domains include Herbivore-Induced Plant Volatiles (HIPVs) ("plant cries for help" that recruit parasitic wasps, predatory mites, and entomopathogenic nematodes to kill leaf- and root-feeding herbivores), floral scent bouquets that guide specialist pollinators, mycorrhizal strigolactone root exudates, and coral reef symbiotic recruitment cues.

The most thoroughly characterized class of synomones operates across three trophic levels (First Trophic Level: Host Plant → Second Trophic Level: Herbivorous Arthropod → Third Trophic Level: Carnivorous Predator or Parasitoid; Price et al., 1980; Dicke & Sabelis, 1988; Turlings, Tumlinson & Lewis, 1990).

Why does an injured plant not simply release its volatile SOS signals continuously? Because synthesizing volatile terpenoids and phenylpropanoids consumes substantial photosynthetic carbon and ATP—and worse, broadcasting volatiles when no herbivores are present would attract specialist herbivores (acting as a deleterious kairomone) and cause foraging parasitoids to waste time searching empty leaves, extinguishing their associative learning. Instead, plants keep synomone emission silent until triggered by Herbivore-Associated Molecular Patterns (HAMPs) in the herbivore's oral secretions or oviposition fluids:

1. Oral Kairomone Recognition (Volicitin, Caeliferins, and Inceptins): When a beet armyworm caterpillar (Spodoptera exigua) chews a maize (Zea mays) leaf, or a two-spotted spider mite (Tetranychus urticae) punctures a Lima bean (Phaseolus lunatus) epidermal cell, compounds in the herbivore's regurgitant—most famously volicitin [N-(17-hydroxylinolenoyl)-L-glutamine, isolated by Alborn et al., 1997], inceptins (proteolytic fragments of chloroplastic ATP synthase γ-subunit), or grasshopper caeliferins—bind to pattern-recognition receptors on the wounded plant plasma membrane.
2. Jasmonic Acid (JA) Octadecanoid Cascade and De Novo Terpene Synthesis: Within minutes, membrane depolarization (V_m waves), cytosolic Ca²⁺ spikes, and reactive oxygen species activate lipoxygenases (LOX) that convert α-linolenic acid into jasmonic acid (JA) and its bioactive isoleucine conjugate (JA-Ile). JA-Ile triggers SCF^COI1-mediated degradation of JAZ transcriptional repressors, upregulating terpene synthase (TPS) and lipoxygenase/hydroperoxide lyase genes.
3. Biphasic Emission of Green-Leaf Volatiles and Terpenoid Synomones:
   • Immediate Burst (0–30 minutes after wounding): Damaged cell membranes release Green-Leaf Volatiles (GLVs)—six-carbon aldehydes, alcohols, and esters such as (Z)-3-hexenal, (Z)-3-hexen-1-ol, and (Z)-3-hexenyl acetate.
   • Systemic Induced Blend (2–24 hours after feeding): Both the bitten leaf and undamaged systemic leaves synthesize and emit a species- and herbivore-specific blend of homoterpenes—(E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT)—alongside sesquiterpenes [(E)-β-farnesene, (E)-β-caryophyllene], monoterpenes (linalool, (E)-β-ocimene), methyl salicylate (MeSA), and indole.
4. Recruitment of the "Bodyguard" Third Trophic Level (+/+): Female parasitic wasps (Cotesia marginiventris, Microplitis croceipes) and predatory phytoseiid mites (Phytoseiulus persimilis) use antennal olfactory receptor neurons tuned to DMNT, TMTT, and (E)-β-farnesene to fly or walk upwind directly to the infested leaf, where they parasitize or consume up to 60% to 90% of the herbivore cohort—saving the plant's reproductive seed yield (+ for the plant) while securing a developmental host or meal (+ for the carnivore).

In 2005, Sergio Rasmann, Ted Turlings, Jörg Degenhardt, and colleagues demonstrated that tri-trophic synomone signaling operates belowground in complete darkness. When larvae of the ferocious pest beetle Diabrotica virgifera virgifera (western corn rootworm) feed on the roots of European maize varieties or ancestral wild teosinte (Zea mays ssp. parviglumis), the injured roots transcribe the terpene synthase gene TPS23 and release a heavy plume of the bicyclic sesquiterpene (E)-β-caryophyllene into the rhizosphere. Unlike lighter monoterpenes that adsorb onto soil organic matter, lipophilic yet weakly polar (E)-β-caryophyllene diffuses efficiently through sandy-loam soil pores over distances of 10 to 50 centimeters, guiding infectious juveniles of the entomopathogenic nematode Heterorhabditis bacteriophora directly to the wounded roots, increasing rootworm mortality by 5-fold!

Strikingly, the researchers discovered that most modern North American hybrid maize lines had accidentally lost the ability to transcribe TPS23 during decades of high-input agronomic selective breeding—leaving American cornfields chemically "mute" underground and vulnerable to Diabrotica devastation. When Degenhardt et al. (2009) restored a functional oregano (E)-β-caryophyllene synthase gene into non-emitting American maize in field trials, the engineered plants spontaneously re-recruited native soil nematodes and reduced adult rootworm beetle emergence by > 60%.

Like allomones and kairomones, a synomone's classification depends on the identity of the receiver:

1. Inter-Plant Eavesdropping ("Talking Trees"): When a wounded sagebrush (Artemisia tridentata), poplar, or maize plant releases airborne HIPV synomones—specifically (Z)-3-hexenyl acetate and methyl jasmonate—undamaged neighboring leaves on the same plant and even neighboring intact plants downwind absorb these volatiles through their stomata, convert (Z)-3-hexenol into defense glycosides, and prime their own jasmonic acid defense genes so they react twice as fast if herbivores arrive (Ian T. Baldwin, Richard Karban, Consuelo De Moraes).
2. Hyperparasitoid Eavesdropping: Conversely, fourth-trophic-level hyperparasitoid wasps (such as Baryscapus galactopus, which lays its eggs inside the beneficial third-trophic-level Cotesia parasitoid larvae!) also use the plant's HIPV plume to track down parasitized caterpillars (Poelman et al., 2012)—turning the plant–Cotesia synomone (+/+) into a deleterious kairomone (−/+) for the primary parasitoid.

1. Nordlund, D. A., & Lewis, W. J. (1976). Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. Journal of Chemical Ecology, 2(2), 211–220. https://doi.org/10.1007/BF00987744
2. Dicke, M., & Sabelis, M. W. (1988). Infochemical terminology: Based on cost-benefit analysis rather than origin of compounds? Functional Ecology, 2(2), 131–139. https://doi.org/10.2307/2389687
3. Rasmann, S., Köllner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., ... & Turlings, T. C. J. (2005). Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434(7034), 732–737. https://doi.org/10.1038/nature03451
4. Akiyama, K., Matsuzaki, K., & Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435(7043), 824–827. https://doi.org/10.1038/nature03608