| Abstract: | Herbivore-induced plant volatiles affect the systemic response of plants to local damage and hence represent potential plant hormones. These signals can also lead to “plant-plant communication,” a defense induction in yet undamaged plants growing close to damaged neighbors. We observed this phenomenon in the context of disease resistance. Lima bean (Phaseolus lunatus) plants in a natural population became more resistant against a bacterial pathogen, Pseudomonas syringae pv syringae, when located close to conspecific neighbors in which systemic acquired resistance to pathogens had been chemically induced with benzothiadiazole (BTH). Airborne disease resistance induction could also be triggered biologically by infection with avirulent P. syringae. Challenge inoculation after exposure to induced and noninduced plants revealed that the air coming from induced plants mainly primed resistance, since expression of PATHOGENESIS-RELATED PROTEIN2 (PR-2) was significantly stronger in exposed than in nonexposed individuals when the plants were subsequently challenged by P. syringae. Among others, the plant-derived volatile nonanal was present in the headspace of BTH-treated plants and significantly enhanced PR-2 expression in the exposed plants, resulting in reduced symptom appearance. Negative effects on growth of BTH-treated plants, which usually occur as a consequence of the high costs of direct resistance induction, were not observed in volatile organic compound-exposed plants. Volatile-mediated priming appears to be a highly attractive means for the tailoring of systemic acquired resistance against plant pathogens.Plants respond to attack by pathogens or herbivores with extensive changes in gene expression that lead to induced resistance phenomena (Karban and Baldwin, 1997); various traits are then expressed de novo or at much higher intensities, which reduce or prevent further tissue damage. As both pathogens and herbivores can spread from the initial site of attack to other organs, such plant responses are often not restricted to the damaged tissue but are expressed systemically, in yet undamaged organs. Three plant hormones playing central roles in the long-distance signaling that underlies this systemic response to local attack are jasmonic acid (JA), ethylene, and salicylic acid (SA). SA and JA, in particular, are transported themselves or in the form of derivatives within the plant in order to elicit systemic responses (Truman et al., 2007; Wasternack, 2007; Heil and Ton, 2008).Recent studies have revealed that long-distance signaling is not only caused by molecules that are transported in the vascular system; signals can also be volatile compounds that move in the headspace outside the plant (Heil and Ton, 2008). In particular, green-leaf volatiles and other herbivore-induced volatile organic compounds (VOCs) can mediate the systemic response of plants to local herbivore damage (Karban et al., 2006; Frost et al., 2007; Heil and Silva Bueno, 2007). Since such VOCs move freely in the air, they may also affect neighboring plants and then mediate the phenomenon of “plant-plant communication,” which has been found in taxonomically unrelated plants such as Arabidopsis (Arabidopsis thaliana), alder (Alnus glutinosa), corn (Zea mays), lima bean (Phaseolus lunatus), maple (Acer saccharum), sagebrush (Artemisia tridentata), and wild tobacco (Nicotiana attenuata; Baldwin and Schultz, 1983; Rhoades, 1983; Tscharntke et al., 2001; Engelberth et al., 2004; Heil and Kost, 2006; Karban et al., 2006; Paschold et al., 2006; Heil and Silva Bueno, 2007; Ton et al., 2007; Godard et al., 2008).Plant-plant communication via VOCs thus appears to be a common phenomenon in herbivore resistance, and similar volatile compounds can also mediate the beneficial effects that are caused by plant growth-promoting rhizobacteria (Ryu et al., 2003, 2004b). Furthermore, exposure to VOCs such as trans-2-hexenal, cis-3-hexenal, or cis-3-hexenol enhanced resistance of Arabidopsis against the fungal pathogen Botrytis cinerea (Kishimoto et al., 2005), which indicates that VOCs may also induce disease resistance. However, the wound response, the induction of VOCs, the effects of plant growth-promoting rhizobacteria, and even the resistance to necrotrophic pathogens such as B. cinerea and Alternaria brassiccicola are mediated via JA signaling (Wasternack and Parthier, 1997; Pieterse et al., 1998; Schilmiller and Howe, 2005; Francia et al., 2007; Heil, 2008; Heil and Ton, 2008). In contrast, systemic acquired resistance (SAR) to biotrophic pathogens in many plant species is mediated by SA signaling, which increases the expression of phytoalexins and of several PATHOGENESIS-RELATED (PR) proteins (van Loon, 1997; Hammerschmidt and Smith-Becker, 1999; Durrant and Dong, 2004) and which usually is thought to act as an antagonist to JA signaling (Maleck et al., 2000; Pieterse and Dicke, 2007; Korneef and Pieterse, 2008). The volatile derivative of SA, methyl salicylate (MeSA), has been proposed as the most likely systemic signal (Park et al., 2007). In tobacco (Nicotiana tabacum), MeSA is converted back to SA, which then forms the active resistance-inducing compound (Kumar and Klessig, 2003; Forouhar et al., 2005). This mechanism might underlie the resistance induction in tobacco plants that were exposed to high MeSA concentrations (Shulaev et al., 1997). In a study on the role of MeSA as a mobile signal, Park and coworkers (2007), however, only found evidence for the vascular transport of this compound.We used lima bean to investigate whether plant-plant signaling can also affect SAR to biotrophic bacterial pathogens. Plants were exposed to the VOCs emitted from neighbors that had been treated with the chemical SAR elicitor benzothiadiazole [BTH; benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester] or that had been induced biologically, and resulting changes in resistance were monitored at the phenotypic and gene expression levels. A common phenomenon involved in disease resistance is priming, which prepares the plant to respond more rapidly and/or effectively to subsequent attack (van Hulten et al., 2006; Bruce et al., 2007; Goellner and Conrath, 2008) but which comes at much lower costs than direct resistance induction (Heil and Baldwin, 2002; Walters and Boyle, 2005; Walters and Heil, 2007). Therefore, we investigated whether VOCs also can prime resistance to pathogens by first exposing plants to VOCs coming from directly induced plants and then challenging them with Pseudomonas syringae pv syringae. Finally, VOCs released from induced plants were analyzed, and the most likely candidates were evaluated for their effect on expression of the resistance marker gene PR-2 in order to understand the chemical nature of the signal. |
