<scp><i>Solanum dulcamara</i></scp>'s response to eggs of an insect herbivore comprises ovicidal hydrogen peroxide production

Geuß, Daniel; Stelzer, Sandra; Lortzing, Tobias; Steppuhn, Anke

doi:10.1111/pce.13015

Cited by 46 publications

(75 citation statements)

References 54 publications

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“…However, while the elm transcriptomic response to elm leaf beetle oviposition treatment was transient and very quickly returned to the control level, other plant species maintain differential expression of a high number of egg‐induced genes for several days (Brassicaceae: Bonnet et al., ; Firtzlaff et al., ; Little et al., ; Solanaceae: Geuss, Stelzer, Lortzing, & Steppuhn, ; Kim et al., ).…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

et al. 2018

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Plant responses to insect egg depositions are known to shape subsequent defensive responses to larvae hatching from the eggs. Elm (Ulmus minor) leaves, on which elm leaf beetles laid their eggs, mount a more efficient defence against larvae hatching from the eggs. However, the molecular mechanisms of this egg‐mediated, improved defence are insufficiently understood and have so far only been studied in annual plants. We analysed the dynamics of transcriptomic changes in larval feeding‐damaged elm leaves with and without prior egg deposition using de novo assembled RNA‐seq data. Compared to egg‐free leaves, egg deposition‐treated leaves showed earlier and/or faster transcriptional regulations, as well as slightly enhanced differential transcriptional regulation after the onset of larval feeding. These early responding transcripts were overrepresented in gene ontology terms associated with post‐translational protein modification, signalling and stress (defence) responses. We found evidence of transcriptional memory in initially egg deposition‐induced transcripts whose differential expression was reset prior to larval hatching, but was more rapidly induced again by subsequent larval feeding. This potential memory effect of prior egg deposition, as well as the earlier/faster and enhanced feeding‐induced differential regulation of transcripts in egg deposition‐treated leaves, may contribute to the egg‐mediated reinforcing effect on the elm's defence against larvae. Hence, our study shows that a plant's experience of a stress‐indicating environmental cue (here: insect eggs) can push the dynamics of the plant's transcriptomic response to subsequent stress (here: larval feeding). Such experience‐mediated acceleration of a stress‐induced plant response may result in improved stress resistance.

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Section: Discussionmentioning

confidence: 99%

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

et al. 2018

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“…FA second morphological plant response to insect eggs is neoplasm formation (Petzold-Maxwell et al, 2011;Geuss et al, 2017). This process consists of the growth of a new plant tissue (callus) below insect eggs, which may lead to egg detachment (Petzold-Maxwell et al, 2011).…”

Section: Egg-induced Direct Plant Responsesmentioning

confidence: 99%

“…More recently, Geuss et al (2017) demonstrated that Solanum dulcamara responds to Spodoptera exigua eggs with the formation of neoplasms and chlorotic tissue. The accumulation of high levels of ovicidal hydrogen peroxide at the oviposition site leads to egg-killing.…”

Section: Egg-induced Direct Plant Responsesmentioning

confidence: 99%

“…benzyl cyanide), and possibly 2) egg-associated microorganisms trigger downstream defense responses regulated through hormone signaling pathways of which 3) salicylic acid (SA) plays a pivotal role (Hilfiker et al, 2014). Direct defense strategies include 4) necrotic tissue (HR-like necrosis), 5) ovicidal compounds (H 2 O 2 ) (Geuss et al, 2017) or 6) callose formation. Lepidopteran egg elicitors can also induce the production of oviposition-induced plant volatiles (OIPVs) enabling the plants 7) to attract egg or larval parasitoids, that upon locating their hosts, inject their own eggs and kill the lepidopteran instars to feed their off-spring (Tamiru et al, 2011;Fatouros et al, 2012;Cusumano et al, 2015;Ponzio et al, 2016) or 8) insectivorous birds (Mrazova et al, 2019).…”

Section: Egg-induced Indirect Plant Responsesmentioning

confidence: 99%

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Chemical, Physiological and Molecular Responses of Host Plants to Lepidopteran Egg-Laying

et al. 2020

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Plant-lepidopteran interactions involve complex processes encompassing molecules and regulators to counteract defense responses they develop against each other. Lepidoptera identify plants for oviposition and exploit them as larval food sources to complete their development. In turn, plants adopt different strategies to overcome and limit herbivorous damages. The insect egg deposition on leaves can already induce a number of defense responses in several plant species. This minireview deals with the main features involved in the interaction between plants and lepidopteran egg-laying, focusing on responses from both insect and plant side. We discuss different aspects of direct and indirect plant responses triggered by lepidopteran oviposition. In particular, we focus our attention on the mechanisms underlying egg-induced plant defenses that can i) directly damage the eggs such as localized hypersensitive response (HR)-like necrosis, neoplasm formation, production of ovicidal compounds and ii) indirect defenses, such as production of oviposition-induced plant volatiles (OIPVs) used to attract natural enemies (parasitoids) able to kill the eggs or hatching larvae. We provide an overview of chemical, physiological, and molecular egg-mediated plant responses induced by both specialist and generalist lepidopteran species, also dealing with effectors, elicitors, and chemical signals involved in the process. Egg-associated microorganisms are also discussed, although little is known about this third partner participating in plant-lepidopteran interactions.

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“…While Colias spp. and G. rhamni elicited a chlorotic response similar to that of Solanum dulcamara to Spodoptera eggs 53 . Our results demonstrate that the egg-induced HR-like necrosis evolved as a new trait at least twice in the Brassicales, but also show that plants specifically evolved this trait to lower egg survival of those pierid species that evolved effective glucosinolate detoxification mechanisms.…”

Section: Discussionmentioning

confidence: 85%

Insect egg-killing: a new front on the evolutionary arms-race between Brassicaceae plants and Pierid butterflies

Griese¹,

Caarls²,

Mohammadin³

et al. 2019

Preprint

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13Evolutionary arms-races between plants and herbivores have been proposed to generate key 14 innovations that can drive diversification of the interacting species. Recent studies reveal that plant 15 traits that target herbivore insect eggs are widespread throughout the plant kingdom. Within the 16 Brassicaceae family, some plants express a hypersensitive response (HR)-like necrosis underneath 17 the eggs of specialist cabbage white butterflies (Pieridae) that leads to eggs desiccating or dropping 18 of the leaf. Here, we studied the evolutionary basis of this trait, its egg-killing effect on and 19 elicitation by specialist butterflies, by screening 31 Brassicaceae species and nine Pieridae species. 20We show that induction of HR-like necrosis by pierid egg deposition is clade-specific in the 21 economically important Brassiceae tribe (Brassica crops and close-relatives) and in the first-22 branching genus Aethionema. The necrosis is elicited only by pierid butterflies that feed on 23 Brassicaceae plants; four Pieris and Anthocharis cardamines butterflies, of which the larvae are 24 specialists on Brassicaceae, elicited a HR-like necrosis. Eggs of pierid butterflies that feed on 25 well-studied chemical defence traits against caterpillars. 31 32 Key words: induced plant defences, counter adaptation, coevolution, plant-insect interaction, egg 33 deposition, hypersensitive response 34 35 36 37

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Solanum dulcamara's response to eggs of an insect herbivore comprises ovicidal hydrogen peroxide production

Cited by 46 publications

References 54 publications

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

Chemical, Physiological and Molecular Responses of Host Plants to Lepidopteran Egg-Laying

Insect egg-killing: a new front on the evolutionary arms-race between Brassicaceae plants and Pierid butterflies

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