Unclear Intentions: Eavesdropping in Microbial and Plant Systems

Abstract

Eavesdropping, the interception of signals by unintended receivers, is an important component of the ecology and evolution of communication systems. Plants and microbes have complex communication systems with important consequences for agriculture, human health, and ecosystem functioning. Eavesdropping, however, has mostly been studied in animal systems. In this review, we argue that eavesdropping is an important force shaping the ecology and evolution of communication in these non-animal systems. To date, studying eavesdropping in plants and microbes has been limited by the fact that signaler "intention" is often unclear: distinguishing signals that evolved to convey information from unintended cues is particularly difficult in plants and microbes, and the fitness consequences of signaling are rarely measured. We describe some of the main examples of eavesdropping in plant and microbial communication and point out other murkier cases were the molecular and physiological basis of communication are well-understood, but the evolutionary implications have not been addressed. We argue that these systems provide experimental tractability to test some of the predicted ecological and evolutionary consequences of eavesdropping, and that the particularities of these systems can lead to an increased understanding of eavesdropping, and its importance in biological communication.

Plant neighbour-modulated susceptibility to pathogens in intraspecific mixtures

“…This demonstrates that changes in susceptibility in intraspecific plant mixtures does not require inoculation of the neighbour, and thus does not depend on the neighbour's susceptiblity level, and hence expression of immunity can be constitutive. In that respect, NMS does not resemble the many cases of 'eavesdropping' situations reported so far (Rebolleda-Gómez and Wood, 2019). (A) Plants of the wheat genotype Cultur were grown either with itself (CUL-CUL, 'pure' condition) or with the genotype Atoudur (CUL-ATO) and were inoculated with Puccinia triticina.…”

“…This has been shown in both inter-and intra-specific plant-plant interactions, in particular against insects (Karban et al, 2000(Karban et al, , 2006. In the case of intraspecific interactions, such a phenomenon is called 'eavesdropping' (Rebolleda-Gómez and Wood, 2019) where a previously unaffected plant primes its defenses after perceiving a signal emitted by the neighbouring, attacked plant. While there are many report that sick or attacked plants can signal danger to neighbours, thus triggering their immunity and reducing their susceptibility (Cheol Song et al, 2016;Wenig et al, 2019), very few studies have indicated that heathy plants can directly affect immunity in their plant neighbourhood.…”

Ribosomally synthesized peptides, foreground players in microbial interactions: recent developments and unanswered questions

“…The signalling molecules called autoinducers that accumulate in the environment in a density-dependent way are not synthesized by certain mutants called signal blind mutants that use the autoinducers without having the cost of signal production; they thus have an advantage. Signals can be intercepted by unintended receivers; 27 in such a mechanism, termed eavesdropping, the signaler benefits from its signal that reaches the intended receiver as expected, but it has to pay the fitness cost when the signal secreted is intercepted by an eavesdropper. This mechanism is considered to have both ecological and evolutionary significance.…”

Biological Prescience: The Role of Anticipation in Organismal Processes

“…Plants have the ability to pick up on above-and below-ground cues from neighboring plants about potential threats, such as herbivory or drought, and use them to induce defensive responses before exposure to stress occurs (Karban et al, 2003;Engelberth et al, 2004;Kessler et al, 2006;Falik et al, 2011). The majority of work on plant eavesdropping has been done on herbivore-induced plant volatiles, but signals emitted by roots and microbes in the soil have also been studied (Falik et al, 2011;Morrell and Kessler, 2014;Blande, 2017;Rebolleda-Gómez and Wood, 2019). When plants are damaged, the composition of their volatiles change and can serve as reliable signals of impending pest presence.…”