Why do distance limitations exist on plant-plant signaling via airborne volatiles?

Abstract

Plant volatiles are known to mediate many important ecological interactions between plants and insects. Plants themselves have also been shown to perceive volatile signals, but the short transmission distances documented thus far in nature raise questions about the ecological significance of plant-to-plant signaling. Recently, we reported that herbivore-induced plant volatiles (HIPVs) can function within an individual plant to overcome vascular constraints on systemic wound signaling. Within-plant signaling is consistent with the limited distances over which HIPVs have been shown to be perceived by plants. However, it remains unclear why these distance limitations should exist. Such limitations cannot be explained by volatile transport distance alone, since parasitoids respond to HIPVs over much greater distances. Thus, we suggest that the apparent distance limitations on plant-to-plant volatile signaling may arise from the mechanisms by which volatile signals are received by plants. These limitations may reflect physiological constraints on plants' ability to perceive volatiles or an adaptive mechanism to avoid responding to signals from other plants. Distinguishing between these possibilities will require additional research into the mechanisms of signal reception, about which little is currently known. Deciphering the ecological significance of HIPVs as phytohormones depends on understanding the mechanisms of HIPV reception.

Many plants respond to insect herbivory by releasing blends of airborne volatile compounds that serve as indirect plant defenses, attracting natural enemies of the herbivores^1,2 and repelling other herbivores.³ The ecological significance of herbivore-induced plant volatiles (HIPVs) in mediating plant-herbivore-parasitoid dynamics is well documented. Such HIPVs may also play a role in signaling between plants, and several studies have reported the initiation of plant defense responses following exposure to HIPVs.^4–11 However, the ecological significance of HIPVs as wound signals between plants has been questioned because of concerns about the effective distances over which HIPVs may be perceived by recipient plants in nature.^12,13

In a recent manuscript, we demonstrated that HIPVs can act as wound signals within a plant and thereby overcome vascular constraints on the dissemination of internally transmitted wound signals.¹⁴ The hypothesis of within-plant, systemic signaling via HIPVs was suggested by Farmer¹⁵ and Orians,¹⁶ and the first experimental test of this hypothesis used wild sagebrush (Artemesia tridentata).¹⁷ Our work with hybrid poplar saplings (Populus deltoides x nigra),¹⁴ and work with wild lima bean plants (Phaseolus lunatus),¹⁸ manipulated herbivore damage to show that systemic within-plant defenses can be primed or induced directly in response to HIPVs. In addition to overcoming vascular constraints on the transmission of internal signaling compounds,¹⁶ within-plant signaling provides clear fitness advantages to the emitting plant, in contrast to between- plant signaling. This observation does not preclude the possibility that plants may still eavesdrop on HIPVs emitted by a damaged neighbor,¹⁹ but deriving benefits from eavesdropping depends on the ability to respond selectively to signals that reliably indicate the presence of an herbivore capable of damaging the recipient.

The efficacy of plant-plant communication via HIPVs has been disputed because plants may routinely be exposed to HIPVs released from nearby plants being fed upon by specialist herbivores that pose no threat to the plant receiving the signal.¹³ For example, green leaf volatiles (GLVs), six carbon compounds that can function as cues to natural enemies of herbivores,²⁰ are released by many plants as a general response to wounding. While GLVs may be reliable indicators of damage, they do not appear to convey context-dependent information. Nonetheless, GLVs have been shown to induce priming or defenses directly in a number of plants spanning a range of eudicots and at least one monocot.^21–23 However, GLVs—even more so than higher molecular weight volatiles such as mono- and sesquiterpenes²⁴—dissipate quickly once released into the air,²⁵ which may limit their effective distance range. Such a limited range suggests that the GLVs may function primarily as within-plant signals, perhaps alleviating the apparent problem that arises when plants with different herbivore communities release the same HIPVs. A generalized HIPV signal transmitted within a plant is presumably adaptive because it will always be associated with feeding damage by an herbivore that poses a direct threat to the plant tissue receiving the signal. Indeed, field tests have demonstrated that some plants in nature respond to wounding-mediated volatile cues only relatively short distances.¹⁰

While within-plant signaling is consistent with the short distances over which plants have been shown definitively to respond to HIPVs under natural conditions, it remains to be determined why such limitations exist. Insect parasitoids and predators detect HIPVs (possibly including GLVs) over distances of tens of meters or more,²⁶ indicating that volatile transport distance may not be the limiting factor on signal reception (Fig. 1).¹² Thus, we hypothesize that the distance limitations on volatile wound signaling are imposed by features of the reception mechanisms employed by plants rather than by any inherent limitations on the distance a volatile can travel. Signal reception may require threshold concentrations that can only be maintained over short distances; and there is some evidence for such a dose response.²⁷ These thresholds might reflect physiological constraints that make it impossible for plants to receive volatile signals as efficiently as do insects. Alternatively, thresholds might serve an adaptive function in preventing the reception of signals originating from distant plants, which may not reliably predict impending herbivory.

Figure 1.

A schematic representing differences in the relative distances over which parasitoids and plants can respond to herbivore-induced volatile (HIPV) emissions. The herbivore-wounded plant (far left) is wounded by herbivores and releases HIPVs (represented by gray arrow). Based on our recent work and work from other systems, systemic regions of the wounded plant can respond () to these HIPVs. Undamaged conspecific and heterospecific neighboring plants close to the wounded plant may also respond (?) to the HIPVs in what has been termed ‘eavesdropping’. However, parasitoids evidently respond to HIPVs from a greater distance than do plants. A better understanding of the mechanisms of HIPV reception in plants is required to understand the basis for such apparent distance limitations on plant-to-plant signaling. See the text for citations.

Plant-to-plant volatile signaling can also occur independently of signaling induced by herbivores or mediated by HIPVs. Parasitic plant seedlings can determine host location by eavesdropping on their host plant's volatile cues,²⁸ though, again, only over very limited distances. But, as with plants responding to HIPVs, short distance reception may be adaptive in this ecological interaction as the parasitic seedlings have limited capacity for growth prior to attachment and must locate potential hosts in their immediate vicinity.

Whether the apparent distance limitations on the reception of volatile signals by plants reflect physiological constraints or adaptation will likely remain unclear until more is known about the mechanisms of signal reception. Unlike reception systems in insects,^29,30 little is known about the mechanisms by which volatiles are perceived by plant cells or the resulting biochemical cascades.^31,32 A single receptor model of recognition—such as has been found in defense responses to herbivore elicitors³³—is possible but may be impractical due to the diversity of possible volatile signals. There is no a priori reason to assume that the mechanism by which some plants respond to terpene volatiles³⁴ is the same mechanism by which other plants perceive and respond to GLVs.^21,23 Indeed, individual compounds elicit specific responses in some cases,³⁵ while a number of compounds elicit similar responses in other cases.²¹ A better understanding of the mechanisms by which HIPVs are perceived is essential to deciphering the patterns of within- and between-plant signaling mediated by volatiles that have long been observed and to understanding the true ecological significance of HIPVs on plant-to-plant signaling.

Addendum to: Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett. 2007;10:490–498. doi: 10.1111/j.1461-0248.2007.01043.x.