Induced Plant Defense Responses against Chewing Insects. Ethylene Signaling Reduces Resistance of Arabidopsis against Egyptian Cotton Worm But Not Diamondback Moth

Abstract

The induction of plant defenses by insect feeding is regulated via multiple signaling cascades. One of them, ethylene signaling, increases susceptibility of Arabidopsis to the generalist herbivore Egyptian cotton worm (Spodoptera littoralis; Lepidoptera: Noctuidae). The hookless1 mutation, which affects a downstream component of ethylene signaling, conferred resistance to Egyptian cotton worm as compared with wild-type plants. Likewise, ein2, a mutant in a central component of the ethylene signaling pathway, caused enhanced resistance to Egyptian cotton worm that was similar in magnitude to hookless1. Moreover, pretreatment of plants with ethephon (2-chloroethanephosphonic acid), a chemical that releases ethylene, elevated plant susceptibility to Egyptian cotton worm. By contrast, these mutations in the ethylene-signaling pathway had no detectable effects on diamondback moth (Plutella xylostella) feeding. It is surprising that this is not due to nonactivation of defense signaling, because diamondback moth does induce genes that relate to wound-response pathways. Of these wound-related genes, jasmonic acid regulates a novel ␤-glucosidase 1 (BGL1), whereas ethylene controls a putative calcium-binding elongation factor hand protein. These results suggest that a specialist insect herbivore triggers general wound-response pathways in Arabidopsis but, unlike a generalist herbivore, does not react to ethylene-mediated physiological changes.Resistance or tolerance of plants to insect herbivores and pathogens is mediated via constitutive or induced defense mechanisms (Mauricio et al., 1997; Buell, 1998). Inducible defenses play a major role in conferring disease resistance against plant pathogens (Maleck and Dietrich, 1999), and their effects on phytophagous insects can include increased toxicity, delay of larval development, or increased attack by insect parasitoids (Baldwin and Preston, 1999). Inducible defenses are thought to compromise plant fitness less, and maybe more durable, than constitutive defense mechanisms (Agrawal, 1998).During their evolution, specialist herbivores have explored new ecological niches and adapted to novel plant chemical defenses (Ehrlich and Raven, 1964). It is therefore not surprising that specialist herbivores are frequently attracted to secondary metabolites from their hosts. For instance, glucosinolates and their hydrolysis products are feeding and oviposition attractants for crucifer specialists (Gupta and Thorsteinson, 1960; Hicks, 1974), but deterrents for nonadapted insects (McCloskey and Isman, 1993). Specialist herbivores frequently detoxify or sequester plant defense compounds. The latter form of adaptation can even result in protection against parasitoids and predators. Differences in metabolism of plant toxins may be one reason why some induced defenses protect against generalist, but not specialist insect herbivores (Agrawal, 1999).Several signaling pathways, including jasmonic acid (JA), salicylic acid (SA), ethylene, and perhaps hydrogen peroxide (H 2 O 2 ; Reymond and Farm...

Interaction between MYC2 and ETHYLENE INSENSITIVE3 Modulates Antagonism between Jasmonate and Ethylene Signaling inArabidopsis

“…However, such a synergistic regulatory model is inconsistent with the antagonistic roles of JA and ET signaling in many important processes. For example, JA antagonizes ET to repress apical hook formation (e.g., exaggerated hook formation in the coi1 mutant) (Figures 1 and 2) (Turner et al, 2002), whereas ET antagonizes JA to repress the expression of wound-responsive genes (VSP1, VSP2, and TAT3) and herbivore-inducible genes (CYP79B3, BCAT4, and BAT5) ( Figures 9A and 9B) (Rojo et al, 1999;Mikkelsen et al, 2003) and to attenuate plant defense against generalist herbivores ( Figures 9C and 9D) (Stotz et al, 2000;Mewis et al, 2005Mewis et al, , 2006Bodenhausen and Reymond, 2007).…”

“…wound-responsive and herbivory-inducible genes ( Figures 9A and 9B), the myc2 myc3 myc4 triple mutant, which was almost completely devoid of glucosinolates (Schweizer et al, 2013), exhibited susceptibility to the generalist herbivores Spodoptera littoralis (Schweizer et al, 2013) and Spodoptera exigua ( Figures 9C and 9D), while plant defense against these generalist herbivores was enhanced in the ET-signaling mutants ein3 eil1 ( Figures 9C and 9D), etr1, and ein2 (Stotz et al, 2000;Mewis et al, 2005Mewis et al, , 2006Bodenhausen and Reymond, 2007). These results demonstrate that the abolishment of EIN3 and EIL1 derepresses MYC2, which enhances the expression of wound-responsive and herbivore-inducible genes and elevates plant defenses against generalist herbivores.…”

Trichoderma gamsii affected herbivore feeding behaviour on Arabidopsis thaliana by modifying the leaf metabolome and phytohormones

“…For example, the Arabidopsis ein2‐1 mutant had more damage than wild‐type plants upon S. littoralis attack (Stotz et al ., 2000). In the present study, the inoculation of ein2‐1 plants with T. gamsii F18 showed a significant decrease of larva weight gain compared with the untreated ein2‐1 plants.…”

Facing the Future of Plant-Insect Interaction Research: Le Retour à la “Raison d'Être”

“…The fundamental signal transduction pathways involving jasmonate, salicylate, and ethylene have been documented to occur in this species (Schenk et al, 2000;Stotz et al, 2000), making the plant well suited for examining mechanisms characterizing early responses to herbivory that may be shared across many groups. Other fundamental findings include demonstrating a modular genetic system for regulation of selectable variation in glucosinolate production (Kliebenstein et al, 2001), genetic variation in multiple signal transduction pathways regulating glucosinolate biosynthesis , and differential biosynthetic and transcriptional responses to specialist and generalist herbivory by insects in at least two orders (Stotz et al, 2000;de Vos et al, 2007;Kusnierczyk et al, 2007).…”