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

Abstract

Plants have evolved various strategies to defend themselves against herbivores and pathogens. Although some of these strategies are constitutive, i.e. present at all times, others are induced only in response to herbivore feeding or pathogen infection. The induction of direct and indirect plant defenses in response to herbivory and other biotic stresses is well established (Karban and Baldwin, 1997), and a wide array of studies have documented such induced defenses (Schultz and Baldwin, 1982; Haruta et al., 2001; van Dam et al., 2004; Miranda et al., 2007). Induced defenses should be adaptive when: (1) defenses are costly to implement, (2) there is spatial or temporal variability in the distribution of herbivores or pathogens so that plants do not always experience attack, and (3) there are tradeoffs between defenses against different enemies (e.g. defenses against herbivores and pathogens or against different herbivore species) so that defense against one increases susceptibility to another. Although induced defenses allow plants to avoid the costs of implementing defenses in the absence of enemies, plants may suffer considerable damage during the time required to mount defenses once attack occurs. To compensate for this vulnerability, some plants appear to prime specific defenses in response to environmental cues that reliably indicate an increased probability of attack before they actually experience an herbivore or pathogen. A conceptual model of defense priming in plant-herbivore interactions. The classic model of induced resistance is highlighted at the top of the flow chart, where a relaxed leaf is induced by herbivore feeding. Induced defenses include a suite of chemical changes that are plant and situation specific and may include direct defenses by synthesizing chemicals that are toxic or unpalatable to the herbivore. Induced defenses may also include indirect defenses such as the production of volatile compounds or EFN, both of which can attract natural enemies of the herbivores. Some of the chemical changes to the wounded leaf may act as wound signals to undamaged regions within the plant or to adjacent plants. The wound signals include internal signals such as JA or external signals such as volatiles. The recognition of these signals may initiate priming, which evidently comprises changes at the molecular level and leads to a so-called primed state in undamaged leaves. Leaves in a primed state are then able, by mechanisms that are poorly understood, to respond more quickly or vigorously to herbivore attack should such an attack occur. But, primed leaves theoretically pay fewer costs relative to a fully induced defense in the event that they do not actually experience herbivory. TFs, Transcription factors. See text for citations. To date, priming has most often been considered in the context of plant-pathogen interactions (for review, see Conrath et al., 2002, 2006), but plants can also be primed by signals associated with herbivore feeding. This review focuses specifically on priming responses to herbivores to highlight current knowledge and directions for future research on defense priming in plant-herbivore interactions. Any environmental cue that provides a reliable indication of the presence of herbivores can conceivably serve as a signal to induce priming. Essentially all studies on antiherbivore priming to date have focused on plant-derived cues associated with herbivore feeding on neighboring plants or on other parts of the same plant. In the former case, the most obvious cues available are herbivore-induced plant volatiles (HIPVs), a subset of volatile organic compounds (VOCs) that are emitted in response to herbivory; in the latter, signals may be transmitted either internally through the vasculature or externally via HIPVs (Fig. 1). In the case of internal wound signals within a plant, information is most likely carried by signaling molecules transported through phloem and xylem (Malone and Alarcon, 1995; van Bel 2003) from the site of localized attack to systemic undamaged regions. Systemic regions can be either primed or induced to express defense responses depending apparently on the cost of the defense and the intensity of the signal (Rhodes et al., 1999), though it is not clear whether the priming and induced defense responses share the same systemic signal pathways. Either way, systemic signals can effectively transmit a wound signal from the site of local attack to potentially vulnerable systemic regions. Plant architecture plays a key role in such signaling (Davis et al., 1991; Orians, 2005) and can cause nonuniform distribution of systemic wound signals (Orians et al., 2000). Though a number of compounds may play a role in internal systemic signaling (for review, see Erb et al., 2008), the most likely candidate appears to be jasmonic acid (JA) and its conjugated forms (Howe, 2004; Thines et al., 2007). The majority of studies of priming in plant-pathogen interactions have foc