How common is within-plant signaling via volatiles?

ABSTRACT

Many plants respond to herbivory by releasing a complex blend of volatiles that may differ from that emitted by intact counterparts. These herbivore-induced plant volatiles (HIPV) mediate many interactions among plants and their community members, including alerting undamaged leaves of the attacked or neighboring plants to impending danger. It has been postulated that HIPVs evolved for within-plant signaling and that other organisms subsequently evolved to use them. However, only 7 studies have reported HIPV-mediated within-plant signaling, most conducted in the laboratory or greenhouse. This leaves open the ecological relevance and evolutionary underpinning of the phenomenon. We recently observed within-plant signaling in hybrid aspen under laboratory and field conditions. Greenhouse experiments showed that HIPVs mediated the process. While our study adds an aspen hybrid to the list of plants in which within-plant signaling has been demonstrated, we lack understanding of how common the process is and whether plants obtain fitness benefits.

Many plants, when attacked by herbivorous insects, release a wide variety of volatile organic compounds (VOCs) that may differ quantitatively and qualitatively from the blend emitted by intact plants. The volatile blends released in response to herbivore feeding are not identical to those elicited by mechanical damage.^1,2 Moreover, the induction of HIPVs is not restricted to the site of damage, but can also be systemic.² The spatial and temporal patterns of HIPV emissions may vary substantially depending on plant species, herbivore species, the developmental stages of both plants and herbivores and the physical environments.^3,4 HIPVs have multiple ecological functions. They can function as defenses against herbivory as means of repelling herbivores and attracting their natural enemies,^3-5 and serve as airborne cues alerting neighboring plants of impending threat.^6,7 In the context of plant-plant communication, the benefit for the emitter plant is controversial, even though a recent study⁷ suggests that plant-plant communication may benefit the remitters by evoking overdispersal of herbivores within the plant population. This leads to the notion that plants do not communicate, but that receiving plants instead eavesdrop on HIPVs, which has stimulated research into within-plant signaling via volatiles among different parts of the same plant.

HIPV-mediated within-plant signaling was first proposed in the 2000s by Farmer⁸ and Orians,⁹ and was first empirically demonstrated in sagebrush (Artemisia tridentata), a woody shrub, by Karban et al.,¹⁰ who reported that only with air contact did branches become more resistant to herbivory when neighboring branches of the same plant were clipped. Interestingly, a follow-up study¹¹ by the same research group found no support in another 2 closely related species, A. canan and A. douglasiana, in which systemic induced resistance did not require volatile cues. Nonetheless, HIPV-mediated within-plant signaling has been demonstrated in several plant species (Fig. 1),^10-18 and has been proposed to be more effective in plant species that have poor vascular connectivity, which prevents effective spread of internal signals generated at the damage site.

Figure 1.

Schematic representation of within-plant signaling via herbivore-induced plant volatiles (HIPV). The dashed arrow depicts possible involvement of internal signals. The simplified diagram illustrates the potential mechanisms underlying this process. The table summarizes evidence accumulated to date. JA: jasmonic acid; EFN: extrafloral nectar.

Recently, we showed that leaves situated on different branches within a hybrid aspen sapling share little if any vascular connectivity.¹⁸ Using volatiles as defense biomarkers, we found under both field and laboratory conditions that local leaf damage by leaf beetles directly induced volatile release in neighboring undamaged branches that lack vascular connection to the damaged branch. This induction in volatile release occurred only when airflow was permitted, confirming that HIPVs are essential for signaling between neighboring branches in hybrid aspen. While our study lends new credence to the notion that plants can use volatile cues to communicate among different organs of the plant, it will remain hard to generalize about how common this process is in nature and whether plants actually benefit from HIPV-mediated self-signaling unless we make significant progress in closing knowledge gaps in the following areas.

First, we know relatively little about the global pattern of HIPV-related within-plant signaling among diverse plant and insect taxa and under different environmental conditions, especially in natural habitats. Compared to studies on HIPV-mediated plant-insect and plant-plant communication, HIPV-mediated within-plant signaling has received little attention.¹⁹ Most studies have been on woody species and conducted in laboratory or semi-natural conditions. Woody plants, especially those growing in arid areas, are thought to have restricted vascular connectivity and thus rely more on volatile signals to communicate among different organs than herbaceous plants.^10,20 Yet, this hypothesis has not been rigorously tested. In addition, it is known that HIPVs can differ dramatically among different herbivore guilds and under different environmental conditions.^3-5 Whether this will impact on the efficacy of within-plant signaling remains to be discovered. For example, does HIPV-mediated signaling differ when plants are confronted with specialist versus generalist herbivores?

Second, systemic induced responses to pathogens and herbivores have been widely investigated,²¹ but most of these studies do not control air-flow and therefore do not disentangle effects of internal signals from those of external volatile signals. Future studies on induced systemic resistance should determine the relative contributions of internal and external signals to systemic responses. It is plausible that even distal parts of a branch that have vascular connection to parts with localized damage may utilize HIPVs to coordinate more effective defense responses. As proposed by Heil,¹⁹ HIPVs acting as a fast signal may prime systemic responses, while internal signals may act in synergy with the HIPVs.

Finally, we lack evidence of whether HIPV-mediated within-plant signaling leads to better performance of the distal parts that perceive and respond to HIPV cues, or the overall fitness of the plant as a whole. To our knowledge, only two studies^10,14 directly measured the amounts of herbivore damage, an integrated component of plant performance, the other studies have measured a very limited number of plant defensive traits, typically release of volatiles. Although the release of volatiles can be a good indicator of plant defense responses, it does not tell us whether enhanced release of volatiles will benefit the plant in terms of reduced herbivory and augmented plant performance and fitness. This concern is especially relevant given that herbivorous insects can also exploit plant volatiles to their own benefit^22,23 and that there is limited evidence for HIPV-mediated indirect defense via attracting natural enemies under natural conditions.^4,5 Furthermore, plants are known to express a wide array of traits, including primary and secondary chemicals, and physiologic and morphological features, all of which relate to plant resistance to herbivores. Indeed, it is increasingly acknowledged that changes to certain traits may not necessarily translate to reduced performance of herbivores and/or increased performance of herbivores’ natural enemies and that plant defense may depend on a suite of these traits acting in concert.^5,24 Therefore, measuring only a few traits may limit our ability to make ecologically relevant inferences regarding volatile-mediated signaling. Moreover, differential expression of any defensive traits caused by HIPV-mediated within-plant signaling will only be ecologically important to the plant if it will eventually translate into differences in plant performance and fitness.⁵ While true plant fitness (i.e., successful offspring in future generations) is extremely challenging to quantify, in particular for slow-growing, long-lived plant species, some better predictors of plant fitness such as plant damage levels and reproductive success (e.g., flower and seed production) as well as insect behavior must be measured in future studies.

In summary, it is becoming increasingly evident that plants use within-plant signaling via volatiles to overcome vascular constraints and/or synergize vascular signaling. However, due to the limited number of studies, along with only a few plant traits measured, we are still in the infancy of our understanding of the ecology and evolution of volatile-mediated within-plant signaling. Future studies should include other plant-insect and plant-pathogen systems, measuring a range of plant resistance and performance-related traits, and combining experiments in the laboratory, field and natural conditions. Only by doing so, can we get a more holistic understanding of whether volatile-mediated signaling is a widespread phenomenon in nature and can improve plant performance and fitness in times of stress.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.