Abstract

Insect oviposition on plants frequently precedes herbivory. Accumulating evidence indicates that plants recognize insect oviposition and elicit direct or indirect defenses to reduce the pressure of future herbivory. Most of the oviposition-triggered plant defenses described thus far remove eggs or keep them away from the host plant or their desirable feeding sites. Here, we report induction of antiherbivore defense by insect oviposition which targets newly hatched larvae, not the eggs, in the system of tomato Solanum lycopersicum L., and tomato fruitworm moth Helicoverpa zea Boddie. When tomato plants were oviposited by H. zea moths, pin2, a highly inducible gene encoding protease inhibitor2, which is a representative defense protein against herbivorous arthropods, was expressed at significantly higher level at the oviposition site than surrounding tissues, and expression decreased with distance away from the site of oviposition. Moreover, more eggs resulted in higher pin2 expression in leaves, and both fertilized and unfertilized eggs induced pin2 expression. Notably, when quantified daily following deposition of eggs, pin2 expression at the oviposition site was highest just before the emergence of larvae. Furthermore, H. zea oviposition primed the wound-induced increase of pin2 transcription and a burst of jasmonic acid (JA); tomato plants previously exposed to H. zea oviposition showed significantly stronger induction of pin2 and higher production of JA upon subsequent simulated herbivory than without oviposition. Our results suggest that tomato plants recognize H. zea oviposition as a signal of impending future herbivory and induce defenses to prepare for this herbivory by newly hatched neonate larvae.

Highlights

  • Upon herbivory, plants induce a variety of defenses that developed via coevolution with herbivorous arthropods, especially insects [1,2,3]

  • It has been proposed that H2O2 plays a role as a second messenger between early response genes and late response genes [33,36]

  • protease inhibitor2 (Pin2) is expressed at the H. zea oviposition site and the level of expression decreased with distance from the egg

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Summary

Introduction

Plants induce a variety of defenses that developed via coevolution with herbivorous arthropods, especially insects [1,2,3]. With intensive study during the past few decades, it is generally understood that upon insect herbivory plants perceive insect-derived cues (e.g. continuous feeding damage, herbivore-associated molecular patterns or HAMPs) and initiate a set of defenses tailored to given herbivore species [3,4,5,6]. Compared to constitutive defenses, which are continuously expressed irrespective of herbivory, induced defenses are considered more flexible and efficient [7,8]. By perceiving reliable cues of impending herbivory and initiating appropriate defenses in advance, plants may be able to totally avoid or significantly reduce herbivory even before a fullinduced defense is activated [9,10]. Plants appear to recognize at least three events as indicators of future herbivory

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