Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants

Abstract

Whether plants respond to cues produced by neighbors has been a topic of much debate. Recent evidence suggests that wild tobacco plants transplanted near experimentally clipped sagebrush neighbors suffer less leaf herbivory than tobacco controls with unclipped neighbors. Here we expand these results by showing evidence for induced resistance in naturally rooted tobacco when sagebrush neighbors are clipped either with scissors or damaged with actual herbivores. Tobacco plants with sagebrush neighbors clipped in both ways had enhanced activity levels of polyphenol oxidase (PPO), a chemical marker of induced resistance in many solanaceous plants. Eavesdropping was found for plants that were naturally rooted, although only when sagebrush and tobacco grew within 10 cm of each other. Although tobacco with clipped neighbors experienced reduced herbivory, tobacco that grew close to sagebrush had lower production of capsules than plants that grew far from sagebrush. When neighboring tobacco rather than sagebrush was clipped, neither levels of PPO nor levels of leaf damage to tobacco were affected. Eavesdropping on neighboring sagebrush, but not neighboring tobacco, may result from plants using a jasmonate signaling system. These results indicate that plants eavesdrop in nature and that this behavior can increase resistance to herbivory although it does not necessarily increase plant fitness.

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

“…Aboveground, VOC-mediated plant-plant interactions are reported to occur over distances that vary depending on the plant species and environmental parameters (such as atmospheric ozone concentration) (Blande et al 2010). In field experiments involving sagebrush and tobacco, plant-plant signalling was demonstrated to occur over distances ranging from 10 cm (sagebrush to tobacco) to 60 cm (sagebrush to sagebrush) (Karban et al 2003(Karban et al , 2006. Similarly, the secretion of extra floral nectar by lima bean leaves was reported to occur in receiver plants located up to 50 cm away from the emitter (Heil and Adame-Álvarez 2010).…”

“…Volatile compounds Fig. 1 emitted by conspecifics or originating from individuals belonging to another plant species have been shown to promote the induction of direct and indirect defences in undamaged neighbouring plants (Dicke et al 2003;Heil and Karban 2010), thus increasing their resistance to insect herbivores (Karban et al 2000;Tscharntke et al 2001;Karban et al 2003Karban et al , 2004Rodriguez-Saona et al 2009) or phytopathogens (Shulaev et al 1997;Yi et al 2009;Girón-Calva et al 2012). Volatiles emitted by mechanically damaged or herbivore-attacked plants have also been shown to be able to prime neighbouring plants or parts of the same plant for faster and greater responsiveness to subsequent mechanical stress or herbivore attack, enabling the receiver plants to respond more efficiently when they are attacked (Engelberth et al 2004;Ton et al 2006;Heil and Kost 2006;Frost et al 2007Frost et al , 2008bLi et al 2012;Erb et al 2015).…”

Plant Defense Priming against Herbivores: Getting Ready for a Different Battle

“…Although HIPVs are also known to mediate a diverse array of interactions between plants and insects (Turlings et al, 1990;De Moraes et al, 1998;Hoballah and Turlings, 2001;De Moraes et al, 2001), the role of volatiles in signaling between plants has been one of the most fascinating and controversial topics in modern ecology (Baldwin and Schultz, 1983;Fowler and Lawton, 1985;Farmer and Ryan, 1990;Shonle and Bergelson, 1995;Karban and Baldwin, 1997;Agrawal, 2000;Bruin and Dicke, 2001;Baldwin et al, 2002Baldwin et al, , 2006Karban et al, 2003;Dudareva et al, 2006). One recurring point of controversy has been the distance over which HIPV signals can be received by plants (Baldwin et al, 2002;Karban et al, 2003;Kessler et al, 2006). Recent work has shown that vascular constraints on systemic induction can be overcome with HIPVs (Karban et al, 2006;Heil and Silva Bueno, 2007;Frost et al, 2007), as hypothesized by both Farmer (2001) and Orians (2005).…”

Alarm Pheromones—Chemical Signaling in Response to Danger

“…Arimura et al, 2000;Dolch and Tscharntke, 2000;Karban and Maron, 2002;Karban et al, 2003;Engelberth et al, 2004), and particularly in overcoming potential constraints on the internal (vascular) transmission of wound signals imposed by plants' modular architecture (Karban et al, 2006;Frost et al, 2007;Heil and Silva Bueno, 2007;Rodriguez-Saona et al, 2009).…”