Specificity and context-dependency of plant–plant communication in response to insect herbivory

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Over three decades of work on airborne plant communication have taught us that plants send, receive, and respond to volatile organic compounds (VOCs) emitted by conspecific as well as heterospecific neighbouring plants. Much of this research has focused on the consequences of plant–plant communication on resistance against herbivory, with studies showing that VOCs emitted by herbivore-damaged plants increase resistance of neighbouring undamaged plants. However, a key aspect that has received less attention concerns the ecological specificity and context-dependency of this phenomenon. Knowledge on this is crucial for assessing the ecological mechanisms that govern plant communication, determining its biological significance under natural conditions, as well as designing effective strategies for its application (e.g. in crop protection). Here we synthesize important advances from incipient work on the ecological specificity of plant communication according to three main aspects: plant-based specificity, herbivore-based specificity, and the influence of the abiotic context. We then provide some ideas for future research to improve our understanding of the specificity of plant communication and its ecological and evolutionary importance.

Introduction

Plants emit complex blends of volatile organic compounds (VOCs), including green leaf volatiles, nitrogen-containing compounds, and aromatic compounds [1,2,3]. These airborne compounds are produced constitutively or can be induced in response to biotic and abiotic stimuli [4,5], and play diverse ecological functions such as: plant protection against extreme abiotic conditions (e.g. thermo-tolerance [4]), attraction of insect pollinators and seed dispersers [6, 7, 8], indirect plant defence by attracting arthropod predators or parasitoids of herbivores [9, 10, 11], and plant-to-plant communication by acting as warning signals of herbivore presence to neighbouring plants [12,13].

Over three decades of work on airborne plant communication have demonstrated that plants emit and respond to VOCs emitted by conspecific [12,14, 15, 16, 17] as well as heterospecific [18,19] neighbouring plants. Most of this work has centered on the consequences of plant–plant communication for resistance against herbivory, with studies showing that VOCs emitted by herbivore-damaged plants (emitter plants) increase resistance of neighbouring undamaged plants (receiver plants) [13]. Responses by receiver plants often involve priming or preparation of defensive responses (rather than full induction), which leads to enhanced defence induction upon subsequent insect attack [13,20]. Plant communication is thought to be widespread and an increasing number of studies have proposed the use of plant VOC-mediated signalling as an alternative for sustainable crop protection against pests and diseases [21, 22, 23]. For example, the exogenous application of VOCs mediating plant communication could be used to prime plants and increase pest resistance [22], representing a complementary (and potentially synergistic) approach to applying plant hormones to enhance direct and indirect plant resistance [24,25].

Despite promising findings, the ecological and evolutionary significance of VOC-mediated plant communication has been questioned primarily on the basis of the ephemeral nature of these compounds and their localized range of action [1]. It has been argued that VOCs serve mainly physiological roles and that their release is an unavoidable consequence of their physiochemical properties (e.g. high volatility [12]). However, the fact that plants have developed biochemical mechanisms to receive and interpret these signals indicates a role of these compounds that is beyond solely a by-product of direct defensive mechanisms [2]. With this in mind, two non-mutually exclusive hypotheses has been posed to explain the ecological and evolutionary role of plant communication. One of these invokes kin selection as a mechanism for the origin and maintenance of plant communication among conspecifics [26••,27], whereas the other argues that this phenomenon functions essentially as a within-plant signalling mechanism that triggers the induction of different plant parts without the need for internal connections between them [28,29]. To date, the relative importance of these two mechanisms remains unresolved, pending on the one hand on future laboratory-based studies that identify the biochemical mechanisms of release and reception of VOCs, and on the other on field-based work measuring concentrations of VOC emissions and consequences for plant fitness under realistic ecological settings [2].

Based on the current state of the field, a key aspect that has received little attention concerns the ecological specificity and context-dependency of plant communication. Identifying the underlying molecular and biochemical mechanisms of plant communication has been considered a top research priority [2], whereas aspects related to the specificity of plant communication in relation to the players involved (i.e. plants and associated insects) and its contingency upon biotic and abiotic factors under natural settings have been seldom discussed. This information is critical for moving beyond describing the presence or magnitude of plant communication, to assessing the ecological mechanisms that govern this phenomenon, its biological significance under natural conditions, and designing effective strategies for its use in crop resistance. Here we synthesize the most important findings from recent work on the ecological specificity of plant communication under three perspectives: plant-based specificity, herbivore-based specificity, and the importance of the abiotic context as a source of variation in strength and specificity of this phenomenon. We end by providing ideas for future research on the specificity of plant communication.

Section snippets

Plant-based specificity

Recent work has demonstrated that communication is contingent on the plant’s genotype identity. Evidence for this plant-based specificity come mostly from research by Karban and collaborators with sagebrush (Artemisia tridentata). Notably, they found that sagebrush receiver plants responded more strongly to volatile cues from mechanically damaged emitter plants that were genetically related to them than to VOCs from unrelated emitter plants (Figure 1a) [26••,27]. Because communication between

Outlook and challenges for future work

An understanding of the biochemical mechanisms of VOC emission and reception as well as the ecological factors influencing plant communication is necessary to explain and predict the specificity and context-dependency of this phenomenon. We next focus on several key challenges and opportunities for the next decade of research, namely: first, identifying key VOCs and understanding their multiplicity in ecological roles, second, achieving a better understanding of communication dictated by

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Katerina Sam for the invitation to write this manuscript, and Kailen A. Mooney, Sergio Rasmann and Colleen S. Nell for helpful discussion on the topic. We also thank three anonymous reviewers for useful comments on a previous version of the article. This research was funded by a Spanish National Research Grant (AGL2015-70748-R), a grant from the Regional Government of Galicia (IN607D 2016/001) and the Ramon y Cajal Research Programme (RYC-2013-13230) to XM.

References (45)

  • N. Dudareva et al.

    Biochemical and molecular genetic aspects of floral scents

    Plant Physiol

    (2000)
  • J. Reinhard et al.

    Scent-triggered navigation in honeybees

    Nature

    (2004)
  • R.A. Raguso

    Wake up and smell the roses: the ecology and evolution of floral scent

    Annu Rev Ecol Evol Syst

    (2008)
  • M. Dicke et al.

    The evolutionary context for herbivore-induced plant volatiles: beyond the cry-for-help

    Trends Plant Sci

    (2010)
  • C.M. De Moraes et al.

    Herbivore-infested plants selectively attract parasitoids

    Nature

    (1998)
  • M. Heil et al.

    Explaining the evolution of plant communication by airborne signals

    Trends Ecol Evol

    (2010)
  • I.T. Baldwin et al.

    Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants

    Science

    (1983)
  • V. Shulaev et al.

    Airborne signalling by methyl salicylate in plant pathogen resistance

    Nature

    (1997)
  • R. Karban et al.

    The specificity of eavesdropping on sagebrush by other plants

    Ecology

    (2004)
  • R. Karban et al.

    Volatile communication between plants that affects herbivory: a meta-analysis

    Ecol Lett

    (2014)
  • R. Karban et al.

    Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush

    Oecologia

    (2000)
  • S.J. Himanen et al.

    Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants – a mechanism for associational herbivore resistance?

    New Phytol

    (2010)
  • Cited by (0)

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