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Plant Responses to Insect Egg Deposition EN60CH26-Hilker ARI 26 November 2014 15:1 Plant Responses to Insect Egg Deposition Monika Hilker1,∗ and Nina E. Fatouros1,2 1Institute of Biology, Dahlem Centre of Plant Sciences, Freie Universitat¨ Berlin, 12163 Berlin, Germany; email: [email protected] 2Laboratory of Entomology, Wageningen University, 6700 EH Wageningen, The Netherlands; email: [email protected] Annu. Rev. Entomol. 2015. 60:493–515 Keywords First published online as a Review in Advance on oviposition, induced plant defense, parasitoids, plant volatiles, priming, October 20, 2014 bacterial symbiont The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: Plants can respond to insect egg deposition and thus resist attack by herbiv- 10.1146/annurev-ento-010814-020620 orous insects from the beginning of the attack, egg deposition. We review Copyright c 2015 by Annual Reviews. Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org ecological effects of plant responses to insect eggs and differentiate between All rights reserved egg-induced plant defenses that directly harm the eggs and indirect defenses ∗ Corresponding author that involve egg parasitoids. Furthermore, we discuss the ability of plants to take insect eggs as warning signals; the eggs indicate future larval feeding damage and trigger plant changes that either directly impair larval perfor- mance or attract enemies of the larvae. We address the questions of how egg-associated cues elicit plant defenses, how the information that eggs have Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. been laid is transmitted within a plant, and which molecular and chemical plant responses are induced by egg deposition. Finally, we highlight evolu- tionary aspects of the interactions between plants and insect eggs and ask how the herbivorous insect copes with egg-induced plant defenses and may avoid them by counteradaptations. 493 EN60CH26-Hilker ARI 26 November 2014 15:1 INTRODUCTION In most insect species, the egg is the first life stage that is directly exposed to the environment. Egg deposition liberates the female from hosting and nourishing the developing embryo inside her body. Nevertheless, the highly vulnerable egg stage needs to be protected from mortality risks to ensure successful reproduction. The risks to which eggs are exposed can be limited by the devices that insect parents transfer into or onto the eggs to protect them against predators, parasitoids, and abiotic stresses (10, 34, 35, 67, 93). Moreover, some insects show sophisticated parental care behavior and guard and shield their eggs with their bodies (63, 116, 126). The type of egg-laying behavior (e.g., egg clustering; 113) and the choice of oviposition site (47, 79) may further determine the chances of eggs surviving. Successful egg development requires a site that provides (a) appropriate abiotic conditions, (b) a low risk of predation, parasitism, and disease, and (c) sufficient food for the offspring (52). Herbivorous insects laying their eggs on plant tissue face the risk of aggressive plant responses that are detrimental to the eggs. To date, oviposition by more than 20 species from a wide range of insect taxa, including plant- and leafhoppers, beetles, sawflies, butterflies, moths, and flies, has been shown to induce plant responses that either have direct negative effects on eggs or inform parasitoids about the presence of eggs and thus indirectly harm the eggs by involving the third Supplemental Material trophic level (53–55, 99) (Supplemental Table 1; follow the Supplemental Materials link from the Annual Reviews home page at http://www.annualreviews.org). Some studies suggest that in addition to these egg-induced direct and indirect plant defenses, plants can take insect egg deposition as a warning signal of future larval herbivory. Plants warned by egg deposition start to prepare their defense against feeding larvae even before larval hatching (6, 40, 44, 68, 92) or accel- erate their growth and thus begin flowering and reproducing earlier than nonwarned plants (77, 92). One counteradaptation of insects to these plant responses would be to manipulate the plant’s reaction to eggs in such a way that plant defense against larvae would be suppressed (12). Hence, the interaction between plants and insect eggs may have very different ecological effects, ranging from egg-induced direct and indirect defenses to warning (priming) effects and possibly egg- induced suppression of plant antiherbivore defense (see Figure 1 and Supplemental Table 1). Furthermore, egg-induced plant responses have been described for more than 20 plant species that cover wide taxonomic and ecological spectra ranging from short-lived herbaceous species to long-lived trees, from gymnosperms to angiosperms, from C3 plants to drought-adapted C4 plants (e.g., grasses, maize), from monocotyledon to dicotyledon plants (Supplemental Table 1). If one considers that egg deposition by numerous herbivorous insect species with very different egg-laying behaviors elicits responses in such a wide range of plant species, it is not surprising that the plant–insect egg dialogues result in a multitude of ecological effects and require sophisticated Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org molecular and chemical mechanisms that are fine-tuned to the interacting species. In this context, we sort egg-induced plant responses by their ecological effects and consider them from a molecular, chemical, and evolutionary ecological perspective. We place special emphasis on ecological and evolutionary aspects of studies on plant–insect egg interactions that have been published during the last few years; thus, we aim to augment the existing framework of the complex pattern of plant responses to eggs outlined by previous reviews (53–55, 99). Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. ECOLOGICAL EFFECTS OF EGG-INDUCED PLANT RESPONSES Researchers have observed ecological effects of plant responses to both singly and gregariously laid eggs, as well as to eggs laid on undamaged leaf tissue or on ovipositionally damaged or feeding- damaged leaf tissue. Hence, whether egg-induced plant responses result in direct or indirect plant defense or have warning or suppressive effects (Figure 1) seems to be independent of the type 494 Hilker · Fatouros EN60CH26-Hilker ARI 26 November 2014 15:1 Egg-larval parasitoids and larval parasitoids Egg parasitoids Herbivore OIPVs HIPVs Eggs are taken as a warning signal and mediate direct Changes in plant VOCs and indirect defenses against larvae Changes in internal plant secondary metabolites Direct anti-egg defenses: formation of plant neoplasms, egg-crushing plant tissue, leaf necrosis, and/or ovicidal substance Phytochemical changes in leaf surface Attraction/arrestment Deterrence/avoidance Annu. Rev. Entomol. 2015.60:493-515. Downloaded from www.annualreviews.org Leaf waxes Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 10/19/16. For personal use only. Figure 1 Overview of plant responses to herbivorous insect egg deposition and their impact on interactions between plants, herbivores, and parasitoids. Abbreviations: HIPVs, herbivore-induced plant volatiles; OIPVs, oviposition-induced plant volatiles; VOCs, volatile organic compounds. www.annualreviews.org • Plant–Insect Egg Interactions 495 EN60CH26-Hilker ARI 26 November 2014 15:1 of insect oviposition behavior. Nevertheless, the specialization of the egg-laying insect to a plant species may affect the plant response to eggs (40, 84, 87, 92); this is addressed below in the context of the evolutionary aspects of the interactions between plants and insect eggs. Hypersensitive response (HR): Egg-Induced Plant Defense Directly Targeting Egg-Laying Females or Eggs a plant’s response to phytopathogens results The first study indicating that insect egg deposition on plants can induce deterrence of further in the formation of egg deposition was conducted by Blaakmeer et al. (7, 8) when they investigated egg deposition necrotic plant tissue by the large cabbage white butterfly, Pieris brassicae, on cabbage plants (Brassica oleracea). Later that isolates the invader from healthy studies revealed that brassicaceous plants can indeed respond to Pieris egg deposition by changing tissue leaf odor or leaf surface chemistry, as outlined below (9, 37, 40, 41). Females of P. brassicae are repelled by the oviposition-induced odor of black mustard plants (Brassica nigra) (40). Egg-induced plant defense strategies directly targeting the eggs rather than the egg-laying female include plant-mediated desiccation of eggs, egg dropping, egg crushing, and egg killing Supplemental Material (Supplemental Table 1). Desiccation of eggs on plants that form necrotic leaf tissue where eggs are attached has been observed on black mustard leaves laden with Pieris eggs (40, 42, 110) (Figure 2a). Egg deposition by P. brassicae on host plant leaves induces production of reactive oxygen species, formation of callose (74), and death of plant cells. This egg-induced response is considered a hypersensitive response (HR)-like necrosis because it appears similar to HR induced by phytopathogens, but whether the mechanisms of a plant’s response to eggs are the same as those of HR to phytopathogens is unknown (40, 43, 72, 74, 88). Furthermore,
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