Pre-exposure of Arabidopsis to the abiotic or biotic environmental stimuli “chilling” or “insect eggs” exhibits different transcriptomic responses to herbivory

Abstract

Plants can retain information about environmental stress and thus, prepare themselves for impending stress. In nature, it happens that environmental stimuli like ‘cold’ and ‘insect egg deposition’ precede insect herbivory. Both these stimuli are known to elicit transcriptomic changes in Arabidposis thaliana. It is unknown, however, whether they affect the plant’s anti-herbivore defence and feeding-induced transcriptome when they end prior to herbivory. Here we investigated the transcriptomic response of Arabidopsis to feeding by Pieris brassicae larvae after prior exposure to cold or oviposition. The transcriptome of plants that experienced a five-day-chilling period (4 °C) was not fully reset to the pre-chilling state after deacclimation (20 °C) for one day and responded differently to herbivory than that of chilling-inexperienced plants. In contrast, when after a five-day-lasting oviposition period the eggs were removed, one day later the transcriptome and, consistently, also its response to herbivory resembled that of egg-free plants. Larval performance was unaffected by previous exposure of plants to cold and to eggs, thus indicating P. brassicae tolerance to cold-mediated plant transcriptomic changes. Our results show strong differences in the persistence of the plant’s transcriptomic state after removal of different environmental cues, and consequently differential effects on the transcriptomic response to later herbivory.

Moth oviposition shapes the species-specific transcriptional and phytohormonal response of Nicotiana attenuata to larval feeding

“…Generally, it is not surprising that one day after egg-removal, systemic N. attenuata leaves did not display the large extent of changes in gene expression as described for the local leaves of A. thaliana 24–72 hours after oviposition by Pieris moths 34 . Even in local A. thaliana leaves, no transcriptional imprint was detected anymore, one day after egg-removal 41 . Yet, both plant species differ in their physiological response to insect oviposition.…”

“…Very few studies examined the influence of an earlier oviposition on plant signalling in response to the feeding larvae. Transcriptome analyses revealed no significant effects of P. brassicae oviposition on A. thaliana ’s response to larval feeding 41 or very few B. nigra genes that were altered in larval attacked plants due to a pre-treatment with P. brassicae egg extract 42 . In tomato, the increase of wound-induced expression of a defensive protease inhibitor (PI) gene in response to a moth’s oviposition coincides with a stronger JA-burst 13 .…”

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

“…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., ).…”

“…Plants on which insects deposited their eggs showed numerous transcriptional changes in response to this highly reliable herbivore‐indicating cue (Bonnet et al., ; Bruessow, Gouhier‐Darimont, Buchala, Metraux, & Reymond, ; Firtzlaff, Oberländer, Geiselhardt, Hilker, & Kunze, ; Little, Gouhier‐Darimont, Bruessow, & Reymond, ; Reymond, ). Furthermore, plants on which eggs had previously been deposited—such as Arabidopsis, tomato and tobacco plants—showed a stronger induction of defence‐related genes upon damage by feeding larvae (Bandoly, Grichnik, Hilker, & Steppuhn, ; Bandoly, Hilker, & Steppuhn, ; Kim, Tooker, Luthe, De Moraes, & Felton, ; Lortzing et al., ).…”

When does it pay off to prime for defense? A modeling analysis

“…() could not detect a significant reduction in RGR when primed. Priming can occur through various mechanisms, some of which last longer (months) and increase in intensity over time, while others have a shorter lifetime and decrease in intensity with time (days; Karban & Shiojiri, ; Ding et al ., ; Pastor et al ., ; Firtzlaff et al ., for drought). For this reason, the duration of the priming effect was varied in the model.…”