Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta

BMC Plant Biology Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta Marko Bosch 0 Sonja Berger 0 Andreas Schaller 0 Annick Stintzi 0 0 Institute of Plant Physiology and Biotechnology, University of Hohenheim (260) , 70593 Stuttgart , Germany Background: Jasmonates are involved in plant defense, participating in the timely induction of defense responses against insect herbivores from different feeding guilds and with different degrees of host specialization. It is less clear to what extent the induction of plant defense is controlled by different members of the jasmonate family and how specificity of the response is achieved. Using transgenic plants blocked in jasmonic acid (JA) biosynthesis, we previously showed that JA is required for the formation of glandular trichomes and trichome-borne metabolites as constitutive defense traits in tomato, affecting oviposition and feeding behavior of the specialist Manduca sexta. In contrast, JA was not required for the local induction of defense gene expression after wounding. In JA-deficient plants, the JA precursor oxophytodienoic acid (OPDA) substituted as a regulator of defense gene expression maintaining considerable resistance against M. sexta larvae. In this study, we investigate the contribution of JA and OPDA to defense against the generalist herbivore Spodoptera exigua. Results: S. exigua preferred JA-deficient over wild-type tomato plants as a host for both oviposition and feeding. Feeding preference for JA-deficient plants was caused by constitutively reduced levels of repellent terpenes. Growth and development of the larvae, on the other hand, were controlled by additional JA-dependent defense traits, including the JA-mediated induction of foliar polyphenol oxidase (PPO) activity. PPO induction was more pronounced after S. exigua herbivory as compared to mechanical wounding or M. sexta feeding. The difference was attributed to an elicitor exclusively present in S. exigua oral secretions. Conclusions: The behavior of M. sexta and S. exigua during oviposition and feeding is controlled by constitutive JA/JA-Ile-dependent defense traits involving mono- and sesquiterpenes in both species, and cis-3-hexenal as an additional chemical cue for M. sexta. The requirement of jasmonates for resistance of tomato plants against caterpillar feeding differs for the two species. While the OPDA-mediated induction of local defense is sufficient to restrict growth and development of M. sexta larvae in absence of JA/JA-Ile, defense against S. exigua relied on additional JA/JA-Ile dependent factors, including the induction of foliar polyphenol oxidase activity in response to S. exigua oral secretions. Generalist and specialist herbivores; Glucose oxidase; Insect resistance; Jasmonic acid; Oxophytodienoic acid; Plant defense; Polyphenol oxidase; Oral secretions; Terpenes - Background Some 350 million years of common history led to the diversification and species richness of present-day flowering plants and phytophagous insects. The joint success of these two closely interacting taxonomic groups has been explained by co-evolution [1-4]. In adaptation to the selection pressure exerted by herbivores, plants evolved constitutive and inducible defense systems that appear to be tailored specifically to different aggressors [5,6]. They include direct defenses such as anti-nutritive proteins, repellant or toxic secondary metabolites, and morphological features such as thorns, prickles or trichomes [7,8]. In addition, plants produce volatile compounds and nectar rewards to attract natural enemies of their pests resulting in indirect defense [9-11]. Insect herbivores vary greatly with respect to their ability to cope with multi-faceted plant defense and this variability largely determines host range and diet breadth of the insect [12,13]. As generalists, polyphagous insects tolerate a wide array of plant defense traits and they may overcome induced defense by manipulating conserved signaling mechanisms that are commonly found in all plants. With increasing specialization, oligo- and monophagous insects appear to have lost the ability to exploit many different plant species but evolved mechanisms to cope with the particular defense traits of their host, and to even manipulate host characteristics to their own benefit [4,14]. As a corollary of the generalist-specialist paradigm, it was assumed that generalist and specialist herbivores would interact with their host plants in distinct and predictable ways. However, this assumption has recently been challenged [14]: while plants clearly show different responses to insects from different feeding guilds, the evidence linking differences in plant responses to the degree of insect specialization is less convincing [5,15-19]. The open question of whether plant responses are divided along the specialist-generalist dichotomy notwithstanding, there is no doubt that plants respond differently to different insects, implying the existence of specific stimuli and recognition systems. Some plant responses are triggered by the loss of tissue integrity as it is caused by herbivory or by mechanical wounding [8]. These responses do not rely on the presence of the herbivore but rather depend on the recognition of damaged-self mediated by damage-associated molecular patterns (DAMPs), i.e. plant-derived molecules that are generated or released as a result of wounding [20,21]. A more specific second layer of defense may be activated by insect-derived effector molecules, so-called herbivore-associated molecular patterns (HAMPs) [21,22], including fatty acid-amino acid conjugates (FACs) [23,24], caeliferins [25], bruchins [26], and inceptins [27,28]. In addition to these low-molecular weight compounds, several proteins were shown to be active as elicitors of plant defense, including glucose oxidase (GOX) [29,30] and -glucosidase [31]. HAMPs and other insect-derived elicitors are produced in different combinations and quantities by different insects [24,32,33], and the response they elicit depends on the plant species [34]. They are thus likely to account for much of the specificity observed in plant-herbivore interactions. The activation of plant defense by non-specific (DAMPs) and specific cues (HAMPs) alike depends on the jasmonate pathway as the core signaling machinery [20,21,35-37]. Mechanical wounding is sufficient to trigger the rapid and transient accumulation of jasmonic acid (JA) concomitant with its bioactive isoleucine conjugate (JA-Ile) in damaged as well as in systemic leaves [20,38-40]. On top of the basal induction by wounding, the production of JA/JA-Ile is potentiated by HAMPs that are present in insect oral secretions [21,24,41]. JA-Ile then promotes the CORONATINEINSENSITIVE 1 (COI1)-dependent ubiquitinylation and degradation of repressor proteins leading to the transcriptional activat (...truncated)