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1 Synthesis

To decipher the chemical language of plant communication, we firstly need to investigate its effects on the recipients and to try and understand the selective forces that lie behind its evolution. Secondly, we need to translate the language itself, assigning meaning to the chemical compounds and blends that make up its words and sentences. Finally, we must know how the language is produced and received and the mechanisms of plant chemical production and perception. The knowledge and ideas presented in the chapters of this book show that we are making progress on all these points.

Imagine a community consisting of plants, herbivores, predators and parasitoids, pollinators, and a complex network of microorganisms. Chemical-mediated communication may play a role in almost every possible interaction between the members of this community. As well as advances in the understanding of plant–insect communication, communication between plants is now well established. For example, plant–plant volatile communication upon herbivore attack has been observed in more than 30 plant species, and 40 out of 48 studies of plant–plant communication via herbivore-induced plant volatiles (HIPVs) have found evidence of communication that affect herbivory (Li, Chap. 7; Karban et al. 2014a). Evidence is emerging that plant–plant volatiles can carry information not only on attack by antagonists but also about abiotic stress, e.g. salt (Lee and Seo 2014) and UV-C irradiation (Yao et al. 2011), and on potential competition and kin recognition (e.g. Karban et al. 2014b). Conversely, our understanding of the role of plant volatiles for interactions involving microorganisms (and microorganism volatiles for plants) is at a much earlier stage.

In this closing chapter, we attempt to outline common themes emerging from the contributed chapters and suggest some key topics where future research should focus.

1.1 Plant Communication in a Community Context

Great progress has been made in deciphering bipartite communication between plants and other organisms, but this book illustrates clearly the need to take a wider view encompassing the entire community of organisms. Much research on plant volatiles has concentrated on tritrophic interactions, often with plant protection in mind, but plant volatile communication influences community processes and, therefore, community structure. This becomes clear when one considers the myriad interactions that can potentially be mediated by plant volatiles that includes, but is not limited to, pollination, parasitism, predation, intra-guild predation, competition, interference, facilitation, associational resistance, priming and induction of defence and stress tolerance, allelopathy, learning/conditioning and niche partitioning.

In this regard, the impact of the fourth trophic level should not be overlooked, particularly its influence on biocontrol of pests (Poelman and Kos, Chap. 9). This is a relatively new research area that opens up the idea that hyperparasitoids can utilise plant cues and, by doing so, have a top-down impact on beneficial insects. HIPVs can also affect the behaviour of vertebrates, for example appearing to act as kairomones for birds (Mäntylä et al. 2008) and lizards (Stork et al. 2011). The study of HIPVs has been almost exclusively the realm of entomologists, so collaboration with zoologists specialising in other animal groups is needed to fully reveal their ecological roles. Communication between plants and the volatile-receiving community involve either individual chemical compounds or blends of volatiles. These chemicals can have numerous effects on community members, with potentially opposing effects on the emitting plant depending on the organism receiving the signal. In evolutionary terms, the key recipient in some cases could be the emitting plant itself (Guerrieri, Chap. 5).

Changes in plant volatiles are starting to be considered in the context of trait-mediated indirect effects (Pareja and Pinto-Zevallos, Chap. 3; Stam et al. 2014), where herbivore-induced volatiles interfere with another volatile-mediated interaction. Pareja and Pinto-Zevallos (Chap. 3) write that ‘An important avenue of research will be integrating the accumulated behavioural and chemical information with the conceptual framework of indirect effects in ecosystems’, and Meiners (Chap. 6) notes ‘Including chemical diversity in biodiversity research is an emerging issue in ecosystem function research’. Floral scents are diverse and multifunctional, being involved not only in pollinator attraction but also repellence of antagonistic species and regulation of interactions with microorganisms (Junker, Chap. 11).

One should also note that organisms that can both affect and be affected by plant volatiles are not limited to plants, arthropods and vertebrates, but include a whole microbiological world that is so far hardly explored. Knowledge on the importance of plant volatiles below ground lags behind knowledge from the above ground environment. However, in the absence of sunlight, chemical information could have an even greater value belowground. Microorganisms can have a major impact on plant volatile blends (van Dam et al., Chap. 8), for example phyllosphere microbiota can significantly influence plant terpene emissions (Peñuelas et al. 2014). Volatiles released by microorganisms associated with plants can reprogram plant physiology and behaviour, leading to both positive and negative outcomes for the plant (van Dam et al., Chap. 8).

Recent advances have shown, for example, that without physical contact, bacteria can dramatically alter the development of the plant’s root system with effects ranging from death to a sixfold increase in biomass. New roles for known substances are likely to emerge, for example indole, highlighted as a within—and between—plant signal (Erb et al. 2015), is also produced by plant growth promoting rhizobacteria (PGPR) and can promote plant growth. These advances open up the intriguing concept of context in plant communication; if plants respond in different ways to the same chemical cue what is underlying those different responses? In human communication, context is said to be everything; it shapes the meaning of content. While obviously not directly comparable to human communication, observations that plants might not be merely mechanically responding to one chemical in the same way in all instances does lend credence to the possibility that there is a contextual dimension in the plant communication process. Another emerging field is floral microbial ecology, and it is important to understand that the evolution of floral scents has probably been affected by selection not only from mutualists but also from microorganisms (Junker, Chap. 11; Junker and Tholl 2013).

Much of what we know about plant volatile-mediated interactions comes from studies in temperate, agricultural or forest systems. For a fundamental understanding of the importance of plant volatile communication, not least at the community level, more studies on tropical systems are needed. As Pareja and Pinto-Zevallos (Chap. 3) note ‘(tropical) regions are at the forefront of global efforts to stem the loss of biodiversity and ecosystem services, so focus on these systems is long overdue’. Within such ecosystems, it could be postulated that the information provided by chemical signals and cues is more important than for many more homogeneous ecosystems, although the alternative argument could be that the chaotic interplay of chemically diverse plants could render chemical signals largely ineffectual. At this point we simply do not know.

1.2 Signal Versus Noise

Considering the importance of plant chemical-mediated interactions for community processes inevitably leads to the question of specificity of the chemical signal and the ability of receivers to discern the information in a complex and dynamic environment. The biologically relevant cues may consist of single substances, but we now know that, in many cases, specific blends of compounds are important. These cues must be interpreted against a chemical background that is likely to become more complex with increasing organismal diversity. Meiners (Chap. 6) notes that laboratory studies that simulate the field conditions are needed, since most studies on arthropod responses to plant volatile diversity have been done in small scale olfactometer experiments, which are inadequate in this context.

In addition to the chemical background, the nature of the cue itself may be dynamic, changing according to both biotic and abiotic factors. For example, abiotic stresses such as temperature and drought can modify both constitutive and induced volatiles. These effects can then impact on biotic interactions. For example, there is evidence that drought can prime volatile defences upon biotic attacks (Copolovici et al. 2014). Diurnal and seasonal rhythms of volatile release are linked not only to abiotic factors but can be synchronised to biotic interactions in ways that are adaptive for the plant (Schuman, Chap. 1). Recently, evidence that the circadian clock directly regulates floral volatiles has been reported (Yon et al. 2016; Fenske et al. 2015).

Plant communication depends on the fidelity of a signal from an emitting organism to a receiver, which can be complicated immensely when plants are attacked by more than one organism or affected by multiple stress factors (Pareja and Pinto-Zevallos, Chap. 3). There is a great complexity and asymmetry in plant responses to multiple stresses. VOC emission under dual infestation may not merely be a combination of the VOCs induced by individual stressors, but can have its own unique profile that may carry specific information to a receiver (Pierre et al. 2011).

‘Private channels’ do seem to exist (Borges, Chap. 10; Junker, Chap. 11), in which interactions are restricted to particular pairs of species, but even here this communication occurs against a complex chemical background generated by the entire community. The volatile chemicals emitted by flowers and structuring the interactions with pollinators are often emitted by plants in other contexts, which brings into focus the issue of specificity and how it is encoded. The chapter by Borges (Chap. 10) provides a complete update to the brood-site pollination mutualism of figs and fig wasps, which is arguably the best studied mutualism of this type.

This book illustrates the dynamic nature and sensitivity of plant volatile blends, and their responsiveness to abiotic as well as biotic factors. It is therefore not surprising that plant volatile communication may be vulnerable to factors associated with climate change. Copolovici and Niinemets (Chap. 2) report how release of terpenoids and green leaf volatiles, compounds shown to affect multiple trophic interactions, can be affected by factors associated with climate change. It should also be noted that plant volatile emissions can contribute to atmospheric pollution and global climate regulation (Arneth and Niinemets 2010). Reactions between atmospheric pollutants and plant volatiles create new products, which may further increase noise and reduce the efficiency of plant communication (Li, Chap. 7).

Understanding these processes will be critical both to our fundamental understanding of plant chemical communication, but also our possibilities to make use of it in practice, in integrated plant protection for example. New types of collaboration will be needed, for example between biologists and atmospheric chemists and physicists.

It is worth noting that, to successfully study the question of signal versus noise in plant chemical communication, robust and sensitive methods will be needed. Fortunately, methods for volatile collection are advancing all the time, with enhanced sensitivity in the laboratory and an increasing ability to track plant volatile emissions in real time at the community and landscape scale (Misztal, Chap. 4). Within the fields of atmospheric chemistry and environmental science, technology has been developed to measure volatile chemicals over a large area with a high degree of spatial and temporal resolution (Misztal, Chap. 4). Coupling this technology to the most advanced methods for tracking insects and vertebrates opens up new possibilities to overlay maps of volatile plumes and animal orientation. It is clear that coupling these technologies will require a great deal of development, but the basic components are in place to make major inroads into distinguishing signal from noise. One of the most challenging tasks for chemical ecologists has been to extrapolate mechanisms elucidated in the laboratory at a small scale to the situation in the field. Meiners (Chap. 6) and Guerrieri (Chap. 5) both call for efforts to increase experimental scale; collaboration between atmospheric chemists and chemical ecologists could lead to major advances in our understanding of volatile-mediated communication processes.

1.3 Search for the Plant ‘Nose’

The field of chemical ecology has been heavily biased towards studies on plants as a signal provider, emitting volatiles that act as signals or cues for other members of the community, but recent reports that plants can listen-in, or eavesdrop, on insect pheromones (Helms et al. 2013, 2014) as well as neighbouring plants and microorganisms really fuel the need to understand how plants detect and process the information encoded in volatile chemicals. Two chapters in this book focus on how plants may perceive volatile cues (Sugimoto et al., Chap 13) and the early, rapid signalling events that they trigger (Zebelo and Maffei, Chap. 12). The quest for understanding of plant volatile perception has been somewhat of a holy grail for the research field for a number of years, and these authors present cutting edge knowledge on this vital question.

Plant electrophysiology is emerging as a means to examine early plant responses to damage and volatile cues (Zebelo and Maffei, Chap. 12). Change in electrical potential as an early event in plant response to stress may represent a very rapid mode of internal signalling. It is as yet unclear whether it functions as a primary or confirmative signal. A key breakthrough has been development of a system to perform electrophysiology in intact living plants. Using this system, it was shown that VOCs emitted by herbivore-damaged tomato plants trigger a plasma transmembrane potential depolarisation in mesophyll cells of neighbouring, undamaged tomato plants (Zebelo et al. 2012).

An important breakthrough in the search for the plant ‘nose’ is recent understanding of a potential detection/perception mechanism involving conversion of volatiles into defensive metabolites or active signalling molecules by glycosylation (Sugimoto et al., Chap. 13). Plants can incorporate airborne (Z)-3-hexenol and convert it to (Z)-3-hexenyl vicianoside as a form of protection from a future attack by herbivores (Sugimoto et al. 2014). Glycosylation is likely to be commonly used among plants to perceive exogenous volatile compounds. The significance of this process under natural conditions requires further research, but these recent studies promote this mechanism as a foundation for further research. Specific mixtures of volatiles appear critical to plant responses, which will be essential to understand in the future.

Understanding here is in its infancy, but we anticipate a number of key breakthroughs including mapping of the molecular and physiological mechanisms and an explanation of how plants might capture detailed information coded by specific blends of volatile compounds. In recent times, high throughput methods for DNA and RNA sequencing have become more accessible and affordable. The use of these and other developing molecular tools in carefully manipulated experiments involving collaboration between chemical ecologists, plant physiologists and bioinformaticians will open possibilities to understand the molecular mechanisms of plant volatile detection and response.

2 Future Research Directions

To continue the scientific progress reported in the chapters of this book and advance understanding of plant volatile communication to the next level, we will increasingly need to work in a transdisciplinary way, and to think broadly about the importance of this communication at the level of communities, rather than individuals. Below we highlight some of the key points that should guide future research in this field. The list is not exhaustive, and further valuable suggestions can be found in each chapter.

  • Adopt a community approach, since volatiles can affect the entire web of ecological interactions and may influence community composition and function.

  • Integrate functional, evolutionary, physiological and ontogenetic levels.

  • Explore the ecological roles that plant VOCs play in more complicated ecological settings, including those in tropical regions and in non-agricultural systems.

  • Tackle the challenge of exploring volatile interactions involving plants and microorganisms underground, under natural as well as laboratory conditions.

  • Understand how pollution can both influence plant volatile production and impact the efficiency of communication by released compounds.

  • Describe novel mechanisms of plant perception of volatile cues and whether they are transduced by receptor-mediated processes or simply interact with plant membranes and initiate signal transduction pathways.

  • Investigate how plants convert compounds at the cellular level and characterise the molecular mechanisms of volatile perception.

Although the book focuses mostly on ecological interactions, there is great potential to exploit plant volatiles in management of arthropod pests using, for example, attractants, repellents and defence elicitors (Guerrieri, Chap. 5). In this case, there is a need for large scale field studies, which are often avoided due to the time and resources needed. However, practical application of plant chemical communication depends on a thorough fundamental understanding of the interactions. This will only be fully attained when we can deal with the daunting level of complexity found in natural systems. Borges (Chap. 10) concludes ‘The need of the hour is collaboration between various disciplines—ecology, evolution, chemistry, atmospheric science, fluid dynamics, behaviour and neurobiology’. It is time for a broader, community level approach to the study of plant volatile communication, in which these types of collaboration help us decipher the chemical language of plant communication.