Within-plant Signaling Research Articles

No place to run

Plants never had it easy. When their ancestors colonized the land about 460 M years ago during the Ordovician period, they were immediately followed by crustaceans—which eventually developed into insects—that found plants a ready source of food. Ever since plants have been at the bottom of the food chain for pathogens and predators from viruses to mammalian herbivores. Unlike animals, plants cannot run away, having given up motility to maximize their surface exposed to sunlight. In lieu, they became masters in chemical warfare and communication to recognize and fend off pathogens and herbivores. Their “claws and teeth” are a dazzling arsenal of chemicals, metabolic and regulatory pathways, producing sensing and communication molecules that attract increasing interest from chemists and biologists for their potential use in medicine and agriculture. > Humans have also learned to use toxic compounds such as digitalis, atropine, opium or nicotine for medicinal, cosmetic or recreational use. Among these molecules are many spices, including the pungent piperine and capsaicin from peppers, or the glucosinolates from mustard and horseradish, and the bitter polyphenols, flavonoids or terpenes from red grapes, coffee beans, tea or cabbage. Humans have long come to appreciate these tastes—that originally evolved as a warning signal to herbivores—for centuries, spices were the most valuable commodity in global trade. Humans have also learned to use toxic compounds such as digitalis, atropine, opium or nicotine for medicinal, cosmetic or recreational use. The alkaloid taxol from the bark of the Pacific yew is a potent chemotherapeutic drug for cancer treatment; artemisinin, isolated from the plant Artemisia annua, or sweet wormwood, has long been employed in Chinese herbal medicine and been refined into a treatment for malaria. The metabolic pathways of plant compounds with medicinal value are therefore an active field of research with the objective of engineering these into E. coli or …

How common is within-plant signaling via volatiles?

ABSTRACTMany 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.

Volatile-Mediated within-Plant Signaling in Hybrid Aspen: Required for Systemic Responses.

Plant volatiles play crucial roles in signaling between plants and their associated community members, but their role in within-plant signaling remains largely unexplored, particularly under field conditions. Using a system comprising the hybrid aspen (Populus tremula x tremuloides) and the specialized herbivorous leaf beetle (Phratora laticollis) and, combining field, greenhouse and laboratory experiments, we examined whether local damage triggered systemic responses in undamaged branches that lack vascular connection to the damaged branches, and to what extent this was caused by airborne volatile signals versus internal signals. An experiment tracing dye through the vasculature of saplings revealed no downward movement of the dye from upper to lower branches, suggesting a lack of vascular connectivity among branches. However, we found under both field and laboratory conditions that herbivore feeding on upper branches elicited volatile emissions by undamaged lower branches. Greenhouse experiments manipulating air contact between damaged and undamaged branches showed that systemic induction of volatiles was almost eliminated when air contact was interrupted. Our findings clearly demonstrate that herbivore-induced volatiles overcome vascular constraints and mediate within-plant signaling. Further, we found that volatile signaling led to induction of different classes of volatiles under field and environment controlled conditions, with a weaker response observed in the field. This difference not only reflects the dose- and time-dependent nature of volatile signaling, but also points out that future studies should focus more on field observations to better understand the ecological role of volatile-mediated within-plant signaling.

Root-emitted volatile organic compounds: can they mediate belowground plant-plant interactions?

Aboveground, plants release volatile organic compounds (VOCs) that act as chemical signals between neighbouring plants. It is now well documented that VOCs emitted by the roots in the plant rhizosphere also play important ecological roles in the soil ecosystem, notably in plant defence because they are involved in interactions between plants, phytophagous pests and organisms of the third trophic level. The roles played by root-emitted VOCs in between- and within-plant signalling, however, are still poorly documented in the scientific literature. Given that (1) plants release volatile cues mediating plant-plant interactions aboveground, (2) roots can detect the chemical signals originating from their neighbours, and (3) roots release VOCs involved in biotic interactions belowground, the aim of this paper is to discuss the roles of VOCs in between- and within-plant signalling belowground. We also highlight the technical challenges associated with the analysis of root-emitted VOCs and the design of experiments targeting volatile-mediated root-root interactions. We conclude that root-root interactions mediated by volatile cues deserve more research attention and that both the analytical tools and methods developed to study the ecological roles played by VOCs in interplant signalling aboveground can be adapted to focus on the roles played by root-emitted VOCs in between- and within-plant signalling.

Plant communication from an ecological perspective

This book describes recent developments in the evolutionary ecology of plant communication, a relatively recent and rapidly developing topic worthy of synthesis. The book is part of Springer's ‘Signaling and communication in plants’ series, and comprises 13 chapters. Taken together, these contributions admirably cover many aspects of plant communication. However, the book could have benefited from more editorial attention to the integration of the different chapters and the avoidance of repetition. For example, the two chapters, ‘The chemistry of plant signaling’ and ‘Plant volatiles: useful signals to monitor crop health status in green-houses’, present very similar information on techniques of collecting volatile compounds. The first chapter, by Schenk and Seabloom, is an introduction to the conceptual framework. This chapter defines and discusses key terms (communication, information, signal, allelopathy, etc.) and revisits the evolutionary mechanisms involved in plant communication. The chapter on the chemical basis of plant signaling (by Birkett) provides an overview of the classical techniques for the collection and identification of plant chemical signals. However, some recently developed techniques are missing, such as ‘chromatoprobe’ extraction, which is now frequently used in plant chemical ecology. This chapter also develops interesting aspects of the organic chemistry of plant signals; but the genetic basis of variation underpinning the synthesis of chemical signals, and the substantial recent progress in gene expression in signaling, are not developed here or elsewhere in the book. Communication between undamaged plants is covered by four chapters. The different aspects of allelopathy between plant species are examined in the case of the diverse biochemistry of invading species (chapter by Kumar and Bais) and the different effects of allelobiosis in plants are considered in the chapter by Ninkovic. This last chapter also presents the results of different studies concerning the role of plant volatiles (volatile organic compounds, or VOCs) in exchange of information between plants on stress or physiological status. A new aspect in the interactions between undamaged plants mediated by volatile chemicals is the use of these signals as an indicator of host quality by organisms at higher trophic levels. This more recent aspect of the ecology of plant communication is explained in the case of aphids on barley in both the chapter by Glinwood and that by Ahman and Ninkovic. Both emphasize how genetic and inter-specific diversity in VOC profiles influences host recognition by aphids. These chapters have direct implications for future work on integrating allelobiosis in crop management and aphid control in agriculture. Plant defences are then covered by three different chapters spanning above-ground and below-ground defences, the ‘talking trees’ phenomenon, and induced defences. Primed defence responses enhanced by root colonization by microorganisms are developed in detail, and the reciprocal benefits of such associations are examined in the chapter by Van Hulten et al. Priming has been observed in different plant species, mainly under laboratory conditions, and the examples are very well detailed in this chapter, as well as the mechanisms involved in this ‘immunological memory’ in plants. The chapter by Heil, titled ‘Within-plant signaling by volatiles triggers systemic defense’, is an excellent synthesis of recent work on plant responses (direct or indirect) to attack by pathogens and herbivores. The very interesting chapter by Blatrix and Mayer develops a more specialized set of interactions, those involved in ant–plant symbioses. This chapter is a complete review of our current knowledge on plant communication in this context and uses as examples ant-gardens and ant–myrmecophyte mutalisms. The chapter on ‘Photosensory cues in plant–plant interactions’ (by Keuskamp and Pierik) explains in detail our current understanding of the shade avoidance syndrome (SAS) and how plants respond to neighbouring intra- or interspecific individuals using reliable external signals. This chapter ends with a discussion of the complexity of relationships between SAS and defence responses against herbivores, and the trade-offs observed, or expected, between these two functions. The chapter on ‘Global atmospheric change and trophic interactions’ (by Ryan et al.) provides a general overview of the complexity of plant responses to environmental changes such as elevated atmospheric CO2 concentrations and the consequences of these changes on resource allocation to allelochemicals. The chapter also pinpoints the lack of theoretical models to predict responses of the intricate network of trophic interactions in heterogeneous environments. The book ends with two more applied chapters, by Bruce and by Jansen et al., on the current use of plant communication in sustainable agriculture, and plant communication to monitor crop health in greenhouses. These chapters also develop the future prospects (promising!) for biocontrol in preventive approaches incorporating plant health monitoring. In summary, despite some redundancy between certain chapters, this book is written in a pleasant style and gives many up-to-date examples. It will be a useful source of information for graduate students and other researchers looking for a concise overview of current work in the evolutionary ecology of plant communication.

Induced plant defense via volatile production is dependent on rhizobial symbiosis

Nitrogen-fixing rhizobia can substantially influence plant-herbivore interactions by altering plant chemical composition and food quality. However, the effects of rhizobia on plant volatiles, which serve as indirect and direct defenses against arthropod herbivores and as signals in defense-associated plant-plant and within-plant signaling, are still unstudied. We measured the release of jasmonic acid (JA)-induced volatiles of rhizobia-colonized and rhizobia-free lima bean plants (Fabaceae: Phaseolus lunatus L.) and tested effects of their respective bouquets of volatile organic compounds (VOCs) on a specialist insect herbivore (Mexican bean beetle; Coccinellidae: Epilachna varivestis Mulsant) in olfactometer choice trials. In a further experiment, we showed that VOC induction by JA reflects the plant responses to mechanical wounding and insect herbivory. Following induction with JA, rhizobia-colonized plants released significantly higher amounts of the shikimic acid-derived compounds, whereas the emission of compounds produced via the octadecanoid, mevalonate and non-mevalonate pathways was reduced. These changes affected the choice behavior of beetles as the preference of non-induced plants was much more pronounced for plants that were colonized by rhizobia. We showed that indole likely represents the causing agent for the observed repellent effects of jasmonic acid-induced VOCs of rhizobia-colonized lima bean plants. Our study demonstrates a rhizobia-triggered efficacy of induced plant defense via volatiles. Due to these findings, we interpret rhizobia as an integral part of legume defenses against herbivores.

Information networks for disease: commonalities in human management networks and within-host signalling networks

Network models of human epidemics can often be improved by including the effects of behaviour modification in response to information about the approach of epidemics. Similarly, there are opportunities to incorporate the flow of information and its effects in plant disease epidemics in network models at multiple scales. (1) In the case of human management networks for plant disease, each node of a network has four main components: plant communities, microbial communities, human information (among researchers, extension agents, farmers, and other stakeholders), and environmental conditions, along with their interactions. The links between nodes, representing the rate of movement between them, have three parts: the rates for plant materials, the rates for microbes, and the rates for information. Network resilience for information flow is an important goal for such systems. Game theory can provide insights into how human agents decide how to invest their efforts in strengthening information networks, and how policies can support more resilient networks. (2) For the case of within-plant signalling networks, each node has a comparable set of four main components: plant signals (often in the form of phytohormones) and development status, microbial communities and plant disease status, microbial signals (often in the form of quorum sensing molecules), and micro-environmental conditions, along with their interactions. In effect, human information is replaced by plant signals and microbial signals in this second model. The links between nodes have three parts: the rates for microbes, the rates for microbial signals (which may move separately from the microbes, themselves), and the rates for plant signals. Understanding how to enhance adaptive plant signalling networks and microbial signalling networks that support plant productivity, and disrupt microbial signalling networks that contribute to pathogenicity, will be an important step for improved disease management.

Short signalling distances make plant communication a soliloquy

Plants respond to attack by herbivores or pathogens with the release of volatile organic compounds. Neighbouring plants can receive these volatiles and consecutively induce their own defence arsenal. This 'plant communication', however, appears counterintuitive when it benefits independent and genetically unrelated receivers, which may compete with the emitter. As a solution to this problem, a role for volatile compounds in within-plant signalling has been predicted. We used wild-type lima bean (Phaseolus lunatus) to quantify under field conditions the distances over which volatile signals move, and thereby determine whether these cues will mainly trigger resistance in other parts of the same plant or in independent plants. Independent receiver plants exhibited airborne resistance to herbivores or pathogens at maximum distances of 50 cm from a resistance-expressing emitter. In undisturbed clusters of lima bean, over 80 per cent of all leaves that were located around a single leaf at this distance were other leaves of the same plant, whereas this percentage dropped below 50 per cent at larger distances. Under natural conditions, resistance-inducing volatiles of lima bean move over distances at which most leaves that can receive the signal still belong to the same plant.

New evidence for a multi-functional role of herbivore-induced plant volatiles in defense against herbivores

A diverse, often species-specific, array of herbivore-induced plant volatiles (HIPVs) are commonly emitted from plants after herbivore attack. Although research in the last 3 decades indicates a multi-functional role of these HIPVs, the evolutionary rationale underpinning HIPV emissions remains an open question. Many studies have documented that HIPVs can attract natural enemies, and some studies indicate that neighboring plants may eavesdrop their undamaged neighbors and induce or prime their own defenses prior to herbivore attack. Both of these ecological roles for HIPVs are risky strategies for the emitting plant. In a recent paper, we reported that most branches within a blueberry bush share limited vascular connectivity, which restricts the systemic movement of internal signals. Blueberry branches circumvent this limitation by responding to HIPVs emitted from neighboring branches of the same plant: exposure to HIPVs increases levels of defensive signaling hormones, changes their defensive status, and makes undamaged branches more resistant to herbivores. Similar findings have been reported recently for sagebrush, poplar, and lima beans, where intra-plant communication played a role in activating or priming defenses against herbivores. Thus, there is increasing evidence that intra-plant communication occurs in a wide range of taxonomically unrelated plant species. While the degree to which this phenomenon increases a plant’s fitness remains to be determined in most cases, we here argue that within-plant signaling provides more adaptive benefit for HIPV emissions than does between-plant signaling or attraction of predators. That is, the emission of HIPVs might have evolved primarily to protect undamaged parts of the plant against potential enemies, and neighboring plants and predators of herbivores later co-opted such HIPV signals for their own benefit.

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

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.

Within‐plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores

Plant volatiles play important roles in signalling between plants and insects, but their role in communication among plants remains controversial. Previous research on plant-plant communication has focused on interactions between neighbouring plants, largely overlooking the possibility that volatiles function as signals within plants. Here, we show that volatiles released by herbivore-wounded leaves of hybrid poplar (Populus deltoides x nigra) prime defences in adjacent leaves with little or no vascular connection to the wounded leaves. Undamaged leaves exposed to volatiles from wounded leaves on the same stem had elevated defensive responses to feeding by gypsy moth larvae (Lymantria dispar L.) compared with leaves that did not receive volatiles. Volatile signals may facilitate systemic responses to localized herbivory even when the transmission of internal signals is constrained by vascular connectivity. Self-signalling via volatiles is consistent with the short distances over which plant response to airborne cues has been observed to occur and has apparent benefits for emitting plants, suggesting that within-plant signalling may have equal or greater ecological significance than signalling between plants.

A Volatile Response to Injury

Plants defend themselves against herbivores by releasing volatile organic compounds (VOCs) that repel herbivores or attract herbivore predators. This response to herbivore-induced damage is mediated through jasmonic acid (JA). Herbivore-induced VOCs have also been reported to stimulate defenses in neighboring plants, thereby playing a role in plant-plant communication (see Gershenzon). Heil and Bueno found that regions of field-grown lima bean plants exposed to shoots that had been damaged by leaf beetles grew better, showed less herbivore damage, secreted more extrafloral nectar (EFN, which attracts herbivore predators), and attracted more ants than did regions that were unexposed to damaged shoots. When some leaves of field-grown lima bean plants were stimulated through damage and application of JA to produce VOCs, production of EFN was stimulated in nearby undamaged leaves from the same shoot or from a second shoot of the same plant. Enhanced production of EFN in undamaged leaves was inhibited, however, when the damaged leaves were covered with plastic bags. Exposure to VOCs also primed EFN secretion, so that the response to subsequent damage was greater in leaves previously exposed to VOCs. In experiments on potted plants, in which air from damaged leaves was blown toward undamaged leaves or directed away from them, only undamaged leaves exposed to air from damaged leaves responded with increased production of EFN. Thus, VOCs appear not only to function in plant-plant communication but also to act as an intraplant defense signal. M. Heil, J. C. Silva Bueno, Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U.S.A. 104 , 5467-5472 (2007). [Abstract] [Full Text] J. Gershenzon, Plant volatiles carry both public and private messages. Proc. Natl. Acad. Sci. U.S.A. 104 , 5257-5258 (2007). [Full Text]

Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature

Plants respond to herbivore attack with the release of volatile organic compounds (VOCs), which can attract predatory arthropods and/or repel herbivores and thus serve as a means of defense against herbivores. Such VOCs might also be perceived by neighboring plants to adjust their defensive phenotype according to the present risk of attack. We exposed lima bean plants at their natural growing site to volatiles of beetle-damaged conspecific shoots. This reduced herbivore damage and increased the growth rate of the exposed plants. To investigate whether VOCs also can serve in signaling processes within the same individual plant we focused on undamaged "receiver" leaves that were either exposed or not exposed to VOCs released by induced "emitter" leaves. Extrafloral nectar secretion by receiver leaves increased when they were exposed to VOCs of induced emitters of neighboring plants or of the same shoot, yet not when VOCs were removed from the system. Extrafloral nectar attracts predatory arthropods and represents an induced defense mechanism. The volatiles also primed extrafloral nectar secretion to show an augmented response to subsequent damage. Herbivore-induced VOCs elicit a defensive response in undamaged plants (or parts of plants) under natural conditions, and they function as external signal for within-plant communication, thus serving also a physiological role in the systemic response of a plant to local damage.