Insect eggs suppress plant defence against chewing herbivores

Abstract

SUMMARYPlants activate direct and indirect defences in response to insect egg deposition. However, whether eggs can manipulate plant defence is unknown. In Arabidopsis thaliana, oviposition by the butterfly Pieris brassicae triggers cellular and molecular changes that are similar to the changes caused by biotrophic pathogens. In the present study, we found that the plant defence signal salicylic acid (SA) accumulates at the site of oviposition. This is unexpected, as the SA pathway controls defence against fungal and bacterial pathogens and negatively interacts with the jasmonic acid (JA) pathway, which is crucial for the defence against herbivores. Application of P. brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of insect-responsive genes after challenge with caterpillars, suggesting that egg-derived elicitors suppress plant defence. Consequently, larval growth of the generalist herbivore S. littoralis, but not of the specialist P. brassicae, was significantly higher on plants treated with egg extract than on control plants. In contrast, suppression of gene induction and enhanced S. littoralis performance were not seen in the SA-deficient mutant sid2-1, indicating that it is SA that mediates this phenomenon. These data reveal an intriguing facet of the cross-talk between SA and JA signalling pathways, and suggest that insects have evolved a way to suppress the induction of defence genes by laying eggs that release elicitors. We show here that egg-induced SA accumulation negatively interferes with the JA pathway, and provides an advantage for generalist herbivores.

Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize

“…The suppression of maize volatiles invoked by oviposition may therefore be indicative of a manipulative strategy by S. frugiperda to reduce the plants general defensive capacity. One possibility proposed by Bruessow et al (2010) is that oviposition induces salicylic acid (SA)-dependent defenses, which may lead to a suppression of oxylipin-mediated responses to herbivory controlled by the jasmonic acid (JA) pathway. There is ample evidence that jasmonic acid is involved in the induction of maize volatile emissions (Ozawa et al 2000;Schmelz et al 2003).…”

“…Following this idea, it has recently been demonstrated that the application of crushed Pieris brassicae L. (Lepidoptera: Pieridae) eggs to Arabidopsis thaliana (L.) activates SAdependent defenses, which function against pathogens, but enhances larval growth of Spodoptera littoralis Boisd. (Lepidoptera: Noctuidae) (Bruessow et al 2010). Yet, little is known about the possible suppression of plant defenses by insect eggs.…”

Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

“…SA regulates plant defenses against pathogens, phloem-sucking insects and plant responses to insect oviposition (de Vos et al 2005;Zarate et al 2007;Vlot et al 2009;Bruessow et al 2010). SA alone does not seem to play a signaling role, neither in plant defenses induced by BG insect herbivores (Erb et al 2009a;Pierre et al 2012), nor in BG-AG interactions in Brassica spp.…”

Plants under dual attack : consequences for plant chemistry and parasitoid behavior

“…The biotic stressors used in this thesis were selected on the basis of the defense signaling pathways they are commonly thought to induce. It is against the crosstalk background described previously that the research contained in this thesis was carried out; while Pieris brassicae caterpillar feeding is primarily activating JA-mediated defenses, all the secondary attackers (P. brassicae eggs, Brevicoryne brassicae aphids, Xanthomonas campestris bacterial pathogens) were chosen because they induce the SA signaling pathway (Ton et al, 2002;Kusnierczyk et al, 2008;Bruessow et al, 2010), though to varying degrees. In the context of dual attack, prioritization of one pathway over another, via crosstalk, would be expected to have a strong effect on subsequent plant responses.…”

“…As voracious feeders, P. brassicae caterpillars pose a major threat to plants as they are capable of entirely defoliating them. The egg stage was also chosen to be included as it has been shown that egg deposition can be sensed by the plant, triggering defense responses (Bruessow et al, 2010) and affecting both plant volatile emission and the foraging behavior of the larval parasitoid of P. brassicae, Cotesia glomerata (Fatouros et al, 2012;Pashalidou et al, 2014).…”