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Do Plants Eavesdrop on Floral Scent Signals?

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Do Plants Eavesdrop on Floral Scent Signals? Opinion Do Plants Eavesdrop on Floral Scent Signals? 1, 2 Christina M. Caruso * and Amy L. Parachnowitsch Plants emit a diverse array of volatile organic compounds that can function as Trends cues to other plants. Plants can use volatiles emitted by neighbors to gain Plants emit volatile organic compounds information about their environment, and respond by adjusting their phenotype. that can function as cues to other plants. 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 Plants may use floral volatiles from their neighbors to sense their mating the function of floral volatile signals and conclude that plants are as likely to environment. perceive and respond to floral volatiles as to other, better-studied volatiles. We fl propose that eavesdropping on oral volatile cues is particularly likely to be Plants could respond by adjusting floral traits that affect pollination and mating. adaptive because plants can respond to these cues by adjusting traits that directly 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, better- studied volatile signals to function as cues to other plants, and (ii) that eavesdropping on floral 1 Department of Integrative Biology, volatile cues is particularly likely to be adaptive because plants can respond to these cues by University of Guelph, Guelph, Ontario adjusting traits that directly affect pollination and mating. N1G 2W1, Canada 2 Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala The Evidence that Non-Floral Volatiles Function as Cues to Other Plants University, 75236 Uppsala, Sweden 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 *Correspondence: neighbors [5]. Many of these studies have focused on volatiles emitted following herbivore [email protected], damage (i.e., herbivore-induced plant volatiles) [8]. Plants can use these volatiles to gain [email protected] information about the presence of herbivores, and respond in at least two different ways. First, (C.M. Caruso). Trends in Plant Science, January 2016, Vol. 21, No. 1 http://dx.doi.org/10.1016/j.tplants.2015.09.001 9 © 2015 Elsevier Ltd. All rights reserved. plants can increase their defenses against herbivores. For example, wild tobacco (Nicotiana Glossary attenuata) growing next to damaged sagebrush (Artemisia tridentata) had less leaf herbivory Adaptive plasticity: phenotypic fi than wild tobacco growing next to undamaged sagebrush [9]. Second, plants can change their plasticity that increases tness (i.e., survival or reproduction). Plasticity is physiology to more quickly or vigorously respond to future herbivore attack (i.e., priming) [10]. adaptive when genotypes that adjust For example, wild tobacco plants growing next to damaged sagebrush plants upregulated the their phenotype in response to the expression of genes that play a role in herbivore defense [11]. environment have higher fitness than genotypes that do not adjust their phenotype. Although most studies have focused on volatiles emitted by herbivore-damaged neighbors, Cue: a trait used by a receiver that is plants can also perceive and respond to volatile cues emitted by undamaged neighbors [12]. not intentionally displayed for that Plants can use the volatiles from undamaged neighbors to gain information about purpose. For example, if herbivores fl fi the presence of conspecifics and heterospecifics, and respond in at least two ways. First, use oral volatiles to nd host plants, then floral volatiles are functioning as plants can alter their biomass allocation and growth. For example, seedlings of the parasitic a cue. species five-angled dodder (Cuscuta pentagona) grew towards volatiles produced by their Eavesdropping: using a signal preferred host species, and away from volatiles produced by non-preferred hosts [13]. intended for other receivers to gain information about the surrounding Second, plants can suppress [14] or change the composition [15] of their own volatile environment. For example, plants that signals. For example, potato (Solanum tuberosum) plants exposed to volatiles produced detect floral volatiles emitted to by undamaged onion (Allium cepa) plants produced more of two terpenoid compounds [15]. attract pollinators are eavesdropping. Potato plants that produced more of these terpenoids attracted fewer aphid herbivores Fine-grained environmental variation: when an individual [16] and more of the natural enemies of aphids [17]. Overall, these studies suggest that experiences more than one herbivore-induced plant volatiles are not the only plant volatile signals that can function as environment within its lifetime. cues to other plants. Floral volatiles: low molecular weight organic molecules emitted by flowers. These compounds are the Could Floral Volatiles Function as Cues to Other Plants? constituents of floral scent, which can Floral volatiles have been shown to function as signals to pollinators and herbivores [18,19], and range from simple blends with few fi fl researchers in disparate elds have speculated that oral volatiles could function as cues to other compounds to complex bouquets of plants (Box 1). However, only one study [20] that we are aware of has explored whether floral >50 compounds. Herbivore-induced plant volatiles volatiles function as cues to other plants. This study found that floral volatiles produced by (HIPVs): low molecular weight snapdragon (Antirrhinum majus) inhibited root growth of Arabidopsis. The response of Arabi- organic molecules emitted by plants fl fi dopsis to oral volatiles was speci c: of the three primary VOCs produced by snapdragon following consumption by an animal. flowers, only methyl benzoate affected root growth, and root growth was not affected by Green leaf volatiles are common components of HIPVs. Mating environment: environmental factors that affect plant reproduction. The mating environment of a plant Box 1. Past Speculation that Plants Can Sense Floral Volatiles can include conspecific plants that With one exception [20], the hypothesis that floral volatiles function as cues to other plants has not been tested using the act as mates, pollinators that transfer methods described in Box 2. However, this hypothesis has been invoked by researchers in two disparate fields: chemical gametes between conspecifics, and ecology and reproductive biology. heterospecific plants that compete for or facilitate pollination. Chemical ecologists who study communication between undamaged plants have speculated that floral volatiles could Phenotypic plasticity: when a function as cues to other plants for two reasons [12]. First, floral volatiles are emitted in a wide range of ecological genotype produces a different conditions, including in the absence of herbivore damage and abiotic stress. Consequently, floral volatiles could function phenotype in response to different as cues to plants growing in a wide range of ecological conditions. Second, floral volatiles and herbivore-induced plant environmental conditions. volatiles are chemically similar. This similarity suggests that if plants can perceive herbivore-induced plant volatiles emitted Plant–plant communication: when by their neighbors, then they should also be able to perceive floral volatiles emitted by their neighbors. a plant signal is perceived by another plant. Plant–plant communication can Reproductive biologists who study gynodioecious species have speculated that plants could use floral volatiles emitted occur via soil or airborne cues, and is by their neighbors as a cue to the mating environment [45]. In gynodioecious species, plants are either
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