Do Plants Eavesdrop on Floral Scent Signals?

Do Plants Eavesdrop on Floral Scent Signals?

Opinion Do Plants Eavesdrop on Floral Scent Signals? Christina M. Caruso1,* and Amy L. Parachnowitsch2 Plants emit a diverse array of volatile organi...

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Opinion

Do Plants Eavesdrop on Floral Scent Signals? Christina M. Caruso1,* and Amy L. Parachnowitsch2 Plants emit a diverse array of volatile organic compounds that can function as cues to other plants. Plants can use volatiles emitted by neighbors to gain information about their environment, and respond by adjusting their phenotype. Less is known about whether the many different volatile signals that plants emit are all equally likely to function as cues to other plants. We review evidence for the function of floral volatile signals and conclude that plants are as likely to perceive and respond to floral volatiles as to other, better-studied volatiles. We propose that eavesdropping on floral volatile cues is particularly likely to be adaptive because plants can respond to these cues by adjusting traits that directly affect pollination and mating.

Trends Plants emit volatile organic compounds that can function as cues to other plants. Plants may use floral volatiles from their neighbors to sense their mating environment. Plants could respond by adjusting floral traits that affect pollination and mating. Plant responses to floral volatiles cues are particularly likely to be adaptive.

Plants Listen to the Airborne Signals of their Neighbors Plants emit a diverse array of airborne volatile organic compounds (see Glossary) [1]. Plant volatiles can function as signals to mutualists such as seed dispersers [2], pollinators [3], and predators of herbivores [4]. However, these volatiles can also function as cues to other plants [5]. Plants can perceive volatiles emitted by neighbors, and use these volatiles to gain information about their environment, including the presence of herbivores [6] and competitors [7]. In response to this information, plants can adjust their phenotype; for example, in response to volatile cues emitted by herbivore-damaged neighbors, plants can increase their own herbivore defenses [8]. While it is clear that plants can use volatiles to gain information about their environment, less is known about whether the many different volatile signals emitted by plants are all equally likely to function as cues to other plants. In this opinion article we review the evidence that floral volatiles, in the same way as other volatile signals, can function as cues to other plants. First, we describe what is known about how plants perceive and respond to non-floral volatiles emitted by their neighbors. Second, we discuss why plants should also be able to perceive floral volatiles emitted by their neighbors, and use these volatiles to gain information about their mating environment. Third, we predict how plants should respond to this information by adjusting their floral traits. Fourth, we hypothesize the ecological conditions under which plants are likely to perceive and respond to floral volatiles emitted by their neighbors. We conclude (i) that floral volatiles are as likely as other, betterstudied volatile signals to function as cues to other plants, and (ii) that eavesdropping on floral volatile cues is particularly likely to be adaptive because plants can respond to these cues by adjusting traits that directly affect pollination and mating.

The Evidence that Non-Floral Volatiles Function as Cues to Other Plants The first studies on plant–plant communication were controversial, but there are now many examples demonstrating that plants can perceive and respond to volatile cues emitted by their neighbors [5]. Many of these studies have focused on volatiles emitted following herbivore damage (i.e., herbivore-induced plant volatiles) [8]. Plants can use these volatiles to gain information about the presence of herbivores, and respond in at least two different ways. First,

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1 Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada 2 Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden

*Correspondence: [email protected], [email protected] (C.M. Caruso).

http://dx.doi.org/10.1016/j.tplants.2015.09.001 © 2015 Elsevier Ltd. All rights reserved.

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plants can increase their defenses against herbivores. For example, wild tobacco (Nicotiana attenuata) growing next to damaged sagebrush (Artemisia tridentata) had less leaf herbivory than wild tobacco growing next to undamaged sagebrush [9]. Second, plants can change their physiology to more quickly or vigorously respond to future herbivore attack (i.e., priming) [10]. For example, wild tobacco plants growing next to damaged sagebrush plants upregulated the expression of genes that play a role in herbivore defense [11]. Although most studies have focused on volatiles emitted by herbivore-damaged neighbors, plants can also perceive and respond to volatile cues emitted by undamaged neighbors [12]. Plants can use the volatiles from undamaged neighbors to gain information about the presence of conspecifics and heterospecifics, and respond in at least two ways. First, plants can alter their biomass allocation and growth. For example, seedlings of the parasitic species five-angled dodder (Cuscuta pentagona) grew towards volatiles produced by their preferred host species, and away from volatiles produced by non-preferred hosts [13]. Second, plants can suppress [14] or change the composition [15] of their own volatile signals. For example, potato (Solanum tuberosum) plants exposed to volatiles produced by undamaged onion (Allium cepa) plants produced more of two terpenoid compounds [15]. Potato plants that produced more of these terpenoids attracted fewer aphid herbivores [16] and more of the natural enemies of aphids [17]. Overall, these studies suggest that herbivore-induced plant volatiles are not the only plant volatile signals that can function as cues to other plants.

Could Floral Volatiles Function as Cues to Other Plants? Floral volatiles have been shown to function as signals to pollinators and herbivores [18,19], and researchers in disparate fields have speculated that floral volatiles could function as cues to other plants (Box 1). However, only one study [20] that we are aware of has explored whether floral volatiles function as cues to other plants. This study found that floral volatiles produced by snapdragon (Antirrhinum majus) inhibited root growth of Arabidopsis. The response of Arabidopsis to floral volatiles was specific: of the three primary VOCs produced by snapdragon flowers, only methyl benzoate affected root growth, and root growth was not affected by

Box 1. Past Speculation that Plants Can Sense Floral Volatiles With one exception [20], the hypothesis that floral volatiles function as cues to other plants has not been tested using the methods described in Box 2. However, this hypothesis has been invoked by researchers in two disparate fields: chemical ecology and reproductive biology. Chemical ecologists who study communication between undamaged plants have speculated that floral volatiles could function as cues to other plants for two reasons [12]. First, floral volatiles are emitted in a wide range of ecological conditions, including in the absence of herbivore damage and abiotic stress. Consequently, floral volatiles could function as cues to plants growing in a wide range of ecological conditions. Second, floral volatiles and herbivore-induced plant volatiles are chemically similar. This similarity suggests that if plants can perceive herbivore-induced plant volatiles emitted by their neighbors, then they should also be able to perceive floral volatiles emitted by their neighbors. Reproductive biologists who study gynodioecious species have speculated that plants could use floral volatiles emitted by their neighbors as a cue to the mating environment [45]. In gynodioecious species, plants are either female or hermaphroditic, and females cannot produce seeds without receiving pollen from hermaphrodites. Consequently, there should be selection on females to perceive the frequency of hermaphroditic neighbors and respond by adjusting their floral traits. Consistent with this hypothesis, females in the gynodioecious species great blue lobelia (Lobelia siphilitica) adjust their rate of flower opening in response to the frequency of hermaphroditic neighbors; females open more flowers per unit time when they are rare relative to hermaphrodites than when they are common relative to hermaphrodites. Female great blue lobelia plants adjust their rate of flower opening even when hand-pollinated and grown in individual pots, suggesting that they do not use pollen receipt or soil chemicals as cues to the frequency of hermaphroditic neighbors. However, in some gynodioecious species, female and hermaphroditic flowers emit different volatile compounds [46], suggesting that female plants could use floral volatiles as a cue to hermaphroditic neighbors.

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Glossary Adaptive plasticity: phenotypic plasticity that increases fitness (i.e., survival or reproduction). Plasticity is adaptive when genotypes that adjust their phenotype in response to the environment have higher fitness than genotypes that do not adjust their phenotype. Cue: a trait used by a receiver that is not intentionally displayed for that purpose. For example, if herbivores use floral volatiles to find host plants, then floral volatiles are functioning as a cue. Eavesdropping: using a signal intended for other receivers to gain information about the surrounding environment. For example, plants that detect floral volatiles emitted to attract pollinators are eavesdropping. Fine-grained environmental variation: when an individual experiences more than one environment within its lifetime. Floral volatiles: low molecular weight organic molecules emitted by flowers. These compounds are the constituents of floral scent, which can range from simple blends with few compounds to complex bouquets of >50 compounds. Herbivore-induced plant volatiles (HIPVs): low molecular weight organic molecules emitted by plants following consumption by an animal. Green leaf volatiles are common components of HIPVs. Mating environment: environmental factors that affect plant reproduction. The mating environment of a plant can include conspecific plants that act as mates, pollinators that transfer gametes between conspecifics, and heterospecific plants that compete for or facilitate pollination. Phenotypic plasticity: when a genotype produces a different phenotype in response to different environmental conditions. Plant–plant communication: when a plant signal is perceived by another plant. Plant–plant communication can occur via soil or airborne cues, and is often used synonymously with eavesdropping. Priming: a physiological response that prepares a plant to more quickly or vigorously respond to a stressful biotic or abiotic environment in the future. For example, plants exposed to herbivore-induced plant volatiles can upregulate the expression of herbivore defense genes.

snapdragon leaf volatiles. Although this study [20] establishes that floral volatiles can function as cues to other plants in a laboratory environment, it does not ascertain whether floral volatiles also function as cues to other plants in more complex field environments (Box 2). Below we describe the evidence that floral volatiles can be perceived by other plants growing in the field, and that plants can use these volatiles to gain information about the mating environment. Floral Volatiles Are Likely To Be Perceived by Other Plants Volatiles are emitted by all plant organs, including leaves, stems, fruits, and flowers. The likelihood that these volatiles will be perceived by other plants depends on two factors: first, the concentration of the volatiles in the atmosphere; and, second, the amount of time that a plant is exposed to the volatiles [21]. Consequently, volatile compounds that are emitted at a low rate or for a short duration are less likely to function as a cue to other plants than compounds that are emitted at a high rate or for a long duration.

Signal: a trait displayed by an individual with the specific intent of communicating with and changing the behavior of a receiver. For example, floral volatiles can signal the presence of nectar rewards to a pollinator. A signal can be transmitted through the air or the soil. Volatile organic compounds (VOCs): low molecular weight compounds with a low vapor pressure at moderate temperatures. Plants can emit VOCs from all their organs, including leaves, stems, flowers, and fruits.

Floral volatile compounds are likely to be emitted at a sufficiently high rate and/or long duration to be perceived by other plants. Floral volatiles represent a significant proportion of the total flux of VOCs emitted by plants [22], and are emitted at a higher rate than leaf volatiles [23]. Given that leaf volatiles can be perceived by other plants, it is likely that floral volatiles are emitted at a sufficiently high rate to also be perceived by other plants. Plants Can Use Floral Volatiles To Gain Information about the Mating Environment Floral volatiles are likely to convey reliable, ecologically-relevant information about the mating environment for three reasons. First, many of the volatile compounds emitted by flowers are not emitted by other plant organs [3], and floral volatile emission can vary across the phases of floral development; for example, unopened buds emit different volatiles than open flowers [24,25]. Consequently, plants could use floral volatile cues to sense whether their neighbors are in flower. Second, relative to leaves and stems, flowers emit a greater diversity of volatile compounds [26]; over 1700 compounds have been identified from angiosperm flowers [26], and the identity, amount, and ratio of volatile compounds in the floral scent bouquet varies among species [3]. Consequently, plants could use floral volatile cues to sense the identity of their flowering neighbors, such as whether they are conspecifics that could act as mates, or heterospecifics that could compete for or facilitate pollination. Third, pollinated flowers can emit different volatiles than unpollinated flowers [27]. Plants could use the unique volatiles produced by pollinated flowers to sense the presence of pollinators, in the same way as they use herbivore-induced plant volatiles to sense the presence of herbivores.

How Could Plants Respond to Information from Floral Volatile Cues? We can make two general predictions about how plants should adjust their phenotype in response to floral volatile cues. First, because floral volatiles convey information about the mating environment, plants should respond by adjusting their floral traits. Second, because long lagtimes place a limit on the evolution of adaptive plasticity (Box 3), plants should adjust floral traits for which there is a short lag-time between when the volatile cue is perceived and when the new phenotype is produced. If the time between perceiving a floral volatile cue and producing a new floral phenotype is long relative to temporal variation in the mating environment, then eavesdropping on floral volatiles will not be adaptive. Below we describe three traits that plants are particularly likely to adjust in response to floral volatile cues: the rate of flower opening, floral nectar rewards, and floral volatile signals. All these traits affect pollination and mating, change rapidly in response to environmental cues, and can reduce fitness if mismatched to the mating environment. For each trait, we describe how plants could adjust their phenotype in response to information about heterospecific competitors for pollination, as an example of how eavesdropping on floral volatiles could be adaptive.

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Box 2. Methods for Testing Whether Volatiles Function as Cues To test whether plants perceive and respond to floral volatile cues, we need to compare plants that have been experimentally exposed to floral volatiles versus unexposed control plants. However, there are multiple methods for experimentally manipulating the volatile signal that a plant is exposed to (Figure IA), and the choice of method affects how the results are interpreted. We describe these methods and their interpretation below. Three methods can be used to experimentally expose a plant to floral volatiles (Figure IB): (i) expose a plant to a coflowering plant; (ii) expose a plant to floral volatile emissions from a co-flowering plant; and (iii) expose a plant to a synthetic floral volatile compound or compounds. The first method can establish that a plant responds to the presence of a co-flowering plant, but does not isolate floral volatiles as the cue. The second method can establish that a response to a co-flowering plant is elicited by an airborne floral volatile cue. The third method can identify the specific floral volatile compound or compounds that elicit a response. Plants that have been experimentally exposed to floral volatiles can be compared to negative and/or positive controls. In a negative control, a plant is exposed to ambient air to establish plant behavior in the absence of the floral volatile cue. In a positive control, a plant is exposed to volatiles emitted by other portions of the shoot organ system such as leaves; if a plant does not respond to leaf volatiles, but does respond to floral volatiles, then we can conclude that plants can distinguish between different types of volatile cues and respond appropriately. The methods described above can be used to test whether plants respond to floral volatile cues in both laboratory and field environments. Although laboratory experiments are necessary to determine whether plants can respond to floral volatile cues, they are not sufficient to determine whether plants do respond to these cues in the field. In the field, plants are exposed to a wide array of volatiles, as well as weather conditions and pollution that can degrade volatile signals [47]. Consequently, some floral volatiles may function as cues to other plants in the lab but not in the field. Field experiments are thus necessary to determine whether eavesdropping on floral volatile cues is common enough to affect the ecology and evolution of plant populations.

(A) Manipulaon

Control

Flowering plant Lab or

Field

(–) Blank

or

Floral volales

and/or

or

(+) Plant volales

Synthec compounds

(B) (i)

(ii)

(iii)

Figure I. Methods for Testing Whether Plants Respond to Floral Volatile Cues. (A) An overview of the experimental design described in Box 2, including potential experimental floral volatile treatments and control groups. (B) Three methods for experimentally manipulating the floral volatiles that a plant is exposed to. (i) Exposing a plant to a coflowering plant. (ii) Exposing a plant to floral volatile emissions from a co-flowering plant. (iii) Exposing a plant to synthetic floral volatile compound(s).

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Box 3. Plasticity in Response to Temporal Environmental Variation Many organisms live in environments that vary temporally within a single generation (i.e., fine-grained environmental variation). In response to this environmental variation, individuals can adjust their phenotype (phenotypic plasticity). If individuals that adjust their phenotype have higher fitness than non-plastic individuals, then adaptive plasticity can evolve [48]. Given that the mating environment can vary within a flowering season [49,50], and plants can adjust their floral traits [29], adaptive plasticity in floral traits could evolve. However, not all phenotypic plasticity is adaptive [51,52], and there have been no direct tests of whether plants that adjust their floral traits in response to fine-grained variation in the mating environment have higher fitness than non-plastic individuals. To test whether plasticity in floral traits is adaptive, individual plants need to be sequentially exposed to different mating environments – for example, scarce versus abundant pollinators. Plasticity would be estimated as the floral trait value when the plant was in the scarce pollinator treatment minus the floral trait value when the plant was in the abundant pollinator treatment. Fitness for each plant would be estimated at the end of the experiment, after exposure to both pollinator treatments. If individual plants with more plastic floral traits have higher fitness across both mating environments, then we can conclude that plasticity is adaptive. For an example of this experimental design applied to different types of environments and traits, see [53]. The evolution of adaptive plasticity in response to fine-grained environmental variation can be limited by an organism's ability to produce a phenotype that matches its environment [54,55]; an organism that produces a phenotype that matches its environment will have higher fitness than an organism that produces a mismatched phenotype. An organism may produce a mismatched phenotype for two reasons. First, an organism may unable to sense its environment: either the cues to the environment are not reliable or the environment changes too rapidly (i.e., information reliability limit [54]). Second, an organism may produce a mismatched phenotype because too much time elapses between sensing and responding to an environmental cue (i.e., lag-time limit [54]). These limits on the evolution of plasticity suggest that plant responses to floral volatile cues are most likely to be adaptive when volatiles convey reliable information about the mating environment, and when plants can quickly respond by developing a new floral phenotype.

The Rate of Flower Opening The rate at which a plant sequentially opens its flowers can affect pollination and mating by determining the number of flowers that are simultaneously displayed [28,29]. Plants can open flowers within minutes of perceiving temperature and light cues [30], suggesting that they have the physiological ability to rapidly adjust their rate of flower opening. In response to floral volatile cues to the presence a competitor for pollination, a plant could increase its rate of flower opening and thus produce a larger floral display. Large floral displays can increase pollinator visitation in the presence of a competitor [31], suggesting that adjusting the rate of flower opening could be adaptive. Floral Nectar Rewards Floral nectar rewards can affect pollination and mating by manipulating pollinator behavior and by extension the movement of pollen [32,33]. The quantity, quality, and/or chemical composition of floral nectar can change, for example, within minutes of visits by nectar robbers [34] and within hours of simulated visits by pollinators [35], suggesting that plants have the physiological ability to rapidly adjust their nectar rewards. Because pollinators can alter their preference for nectar rewards depending on the availability of alternative resources [36], a plant could respond to floral volatile cues to the presence of a competitor for pollination by producing more nectar. In the presence of a competitor, producing more floral nectar can increase pollinator visitation and fitness [32,37]. Floral Volatile Signals Floral scent bouquets can affect pollination and mating by simultaneously attracting some pollinator taxa while repelling others [38]. The degree of attraction and repellence can be determined by the dosage of particular compounds (e.g. [39]), suggesting that both the identity of the compounds that are emitted and the rate of emission can affect pollination and mating. The chemical composition and emission rate of floral scent bouquets can change within minutes in response to environmental cues such as increased temperature [40], suggesting that plants could rapidly alter their own floral volatile production in response to floral volatile cues from their neighbors. For example, in response to cues to the presence of a competitor for pollination, a

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plant could produce more floral volatiles. This increase in floral volatile emission could attract more pollinators, which could increase plant fitness [41].

Which Ecological Conditions Favor Eavesdropping on Floral Volatiles? Even if floral volatiles commonly function as cues to other plants, not all floral volatile signals will be equally vulnerable to eavesdropping. Instead, the likelihood that a plant will perceive and respond to floral volatiles should vary predictably depending on ecological conditions. Because cue reliability places a limit on the evolution of adaptive plasticity (Box 3), we predict that plants should be more likely to perceive and respond to floral volatiles in ecological conditions where these volatiles provide reliable information about the mating environment. If floral volatile cues provide unreliable information about the mating environment, then eavesdropping on floral volatiles will not be adaptive. Three ecological conditions should increase the likelihood that a plant receives a reliable floral volatile cue: high plant densities, high temperatures, and the presence of plants that produce chemically-unique floral scent bouquets. High plant densities will decrease the distance between a plant and its neighbors, which should increase the reliability of floral volatile cues by decreasing the likelihood that the signal will degrade before it can be perceived by other plants. High temperatures can increase the rate of floral volatile emission [40], and this should increase the reliability of floral volatile cues by increasing the amount of signal that is available to be perceived by other plants. Plants that produce unique floral scent bouquets should be more likely to provide reliable floral volatile cues because they can produce signals that encode very specific information about the mating environment [3]. For example, floral volatiles used in private communication between plants and their pollinators [42] should be more likely to provide reliable cues to the presence of flowering heterospecific plants, whereas floral volatiles produced after pollination [27] should be more likely to provide reliable cues to the presence of pollinators.

Concluding Remarks We conclude that floral volatiles are equally likely as other volatiles to function as cues to other plants. Moreover, eavesdropping on floral volatiles cues is more likely to increase fitness than eavesdropping on other volatile signals because floral volatiles are the only volatile signals emitted by plants that have the potential to convey information about the mating environment. Consequently, plants should respond to floral volatile cues by adjusting floral traits, and floral traits are unique among plant traits in directly affecting pollination, mating, and thus fitness [43]. However, the possibility that plants eavesdrop on floral volatiles has generally been ignored both by researchers studying floral scent signals [44] and by researchers studying plant–plant communication [5]. Therefore, most questions about the nature and extent of eavesdropping on floral volatiles remain unanswered (see Outstanding Questions). Answering these questions will be important because if floral volatiles commonly function as cues to other plants, then we have underestimated the ability of plants to perceive and respond to their environment. Acknowledgments We thank R. Rivkin for discussion and two anonymous reviewers for comments on an earlier version of the manuscript. During the writing of this manuscript C.M.C. was supported by a Discovery Grant from the Natural Science and Engineering Research Council of Canada.

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Outstanding Questions Could floral volatiles function as cues to other plants? Are common or unique floral volatile compounds more likely to be perceived by other plants? Are complex bouquets of volatile compounds or individual compounds emitted by flowers more likely to convey information about the mating environment? How do plants distinguish between their own floral volatiles and those produced by their neighbors? How could plants respond to information from floral volatile cues? How quickly can plants respond to information from floral volatile cues? Are plants more likely to respond to information from floral volatile cues by adjusting floral traits that function as signals or as rewards? Are plant responses to floral volatile cues likely to be adaptive? Is plasticity in response to floral volatile cues more likely to affect male or female fitness in hermaphroditic plant species? What limits the evolution of plasticity in response to floral volatile cues (e.g., information reliability vs lag-time limits; Box 3)? Which ecological conditions favor eavesdropping on floral volatiles? Do plants respond differently to floral volatile cues from competitors for pollination versus species that facilitate pollination? Does eavesdropping only occur between plants that share pollinators or antagonists?

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