1 Plants release volatiles after herbivore attack in a highly regulated fashion. These compounds attract natural enemies and function as indirect defenses. Whether neighboring plants ‘eavesdrop’ on these volatile signals and tailor their defenses accordingly remains controversial. Recent laboratory studies have identified transcriptional changes that occur in plants in response to certain volatiles. These changes occur under conditions that enhance the probability of signal perception and response. Field studies have demonstrated repeatable increases in the herbivore resistance of plants growing downwind of damaged plants. Addresses Max Planck Institute for Chemical Ecology, Department of Molecular Ecology, Winzerlaer Strasse 10, Jena 07745, Germany *e-mail: baldwin@ice.mpg.de Current Opinion in Plant Biology 2002, 5: 1369-5266/02/$ — see front matter © 2002 Elsevier Science Ltd. All rights reserved. DOI 10.1016/S-1369-5266(02)00263-7 Abbreviations FAC fatty-acid–amino-acid conjugate HI herbivore-induced JA jasmonic acid MeJA jasmonic acid methyl ester PAL phenylalanine ammonia lyase VOC volatile organic compound Introduction Plants are masters of gas exchange, not only literally building forests from gases taken from the air but also releasing complex bouquets of volatile organic compounds (VOCs) back into the air. This remarkable ability fuels the expectation that plants communicate through volatile signals. Although ‘communication’ is a loaded term that means different things to different researchers, most would accept a definition with the minimal requirement that information be exchanged, regardless of ‘intent’ or fitness consequence for either party. Two decades ago, researchers reported that wounding or herbivore attack resulted in changes in the herbivore resistance, or to the secondary metabolites that mediate this resistance, not only of the attacked plants but also of plants growing nearby. In some experiments, aerial transfer of information was the most parsimonious way in which the results could be interpreted [1], causing the phenomena to be dubbed ‘talking trees’ by the popular press. Given that neighboring plants compete for resources and that selection is unlikely to favor plants that provide information to competitors, the phenomena should be more aptly called ‘eavesdropping elms’. Experiments published in the past two years have been highlighted in reviews [2–4] and have rekindled interest in these phenomena. Last year, evidence for inter-plant communication was compiled in a special issue of Biochemical Systematics and Ecology [5 •• ]. Here, we review the evidence concerning how emissions are controlled, the signals involved, and the responses of downwind plants. We also summarize the challenges for future research. Regulation of the composition, and the temporal and spatial patterns, of VOC release After herbivore attack, plants release complex bouquets of volatiles into the air from their vegetative tissues. The release of some constituents is likely a passive consequence of damage to the compartments (e.g. vacuoles or trichomes) in which VOCs (or their precursors) are stored. The release of other constituents has been demonstrated to result from de novo synthesis and is tightly controlled. Even metabo- lites that occur in substantial pools in undamaged leaves may be actively discharged. For example, mechanical damage to Artemesia tridentata leaves causes the release of large amounts of jasmonic acid methyl ester (MeJA) into the air under field conditions. When compared to the pools of MeJA found in the leaves, the epimeric composition of the released MeJA is highly enriched in the thermodynam- ically unstable and biologically active enantiomer (i.e. 3R,7S MeJA) [6 • ], suggesting that the released material is newly synthesized or somehow epimerized during release. Flowers and other reproductive organs are known to discharge complex blends of VOCs with distinct temporal patterns, and evidence is emerging that herbivore-induced (HI) releases from vegetative tissue are similarly regulated. The mechanisms that control floral emissions are only just being examined [7 • ,8], and the molecular and physiological controls over HI releases are not understood. Most HI-VOCs can also be found in the floral headspace of some species and are derived from phenolic, terpenoid and fatty-acid metabolic pathways that utilize both stored reserves and recently fixed carbon. After herbivore attack, HI-VOCs are released both locally from damaged tissues and systemically from undamaged tissues in discrete temporal patterns. Some constituents are emitted at maximum levels during daylight hours and become undetectable at night [9,10 • ], others have nocturnal maxima [11]. With the recent development of instrumenta- tion that allows the real-time analysis of emission patterns [12 •• ], the temporal and spatial complexity of these patterns will be more readily characterized. Wounding plays an important role in eliciting the VOC release. In some plant species, mechanical damage can pro- voke releases of the same VOCs as are elicited by herbivory. In many plant species, however, the HI-VOC release differs from that elicited by mechanical wounding. Exogenous Volatile signaling in plant–plant–herbivore interactions: what is real? Ian T Baldwin*, André Kessler, Rayko Halitschke