Abstract

BackgroundIn native environments plants frequently experience simultaneous or sequential unfavourable abiotic and biotic stresses. The plant’s response to combined stresses is usually not the sum of the individual responses. Here we investigated the impact of cold on plant defense against subsequent herbivory by a generalist and specialist insect.ResultsWe determined transcriptional responses of Arabidopsis thaliana to low temperature stress (4 °C) and subsequent larval feeding damage by the lepidopteran herbivores Mamestra brassicae (generalist), Pieris brassicae (specialist) or artificial wounding. Furthermore, we compared the performance of larvae feeding upon cold-experienced or untreated plants. Prior experience of cold strongly affected the plant’s transcriptional anti-herbivore and wounding response. Feeding by P. brassicae, M. brassicae and artificial wounding induced transcriptional changes of 1975, 1695, and 2239 genes, respectively. Of these, 125, 360, and 681 genes were differentially regulated when cold preceded the tissue damage. Overall, prior experience of cold mostly reduced the transcriptional response of genes to damage. The percentage of damage-responsive genes, which showed attenuated transcriptional regulation when cold preceded the tissue damage, was highest in M. brassicae damaged plants (98%), intermediate in artificially damaged plants (89%), and lowest in P. brassicae damaged plants (69%). Consistently, the generalist M. brassicae performed better on cold-treated than on untreated plants, whereas the performance of the specialist P. brassicae did not differ.ConclusionsThe transcriptional defense response of Arabidopsis leaves to feeding by herbivorous insects and artificial wounding is attenuated by a prior exposure of the plant to cold. This attenuation correlates with improved performance of the generalist herbivore M. brassicae, but not the specialist P. brassicae, a herbivore of the same feeding guild.

Highlights

  • In native environments plants frequently experience simultaneous or sequential unfavourable abiotic and biotic stresses

  • Transcriptional response of Arabidopsis to feeding damage and artificial wounding To investigate whether Arabidopsis plants respond differently to leaf damage by P. brassicae and M. brassicae larvae and to artificial wounding, we analyzed the transcriptomes in leaves from plants grown at 20 °C (Fig. 1, samples TP, TM, TW and C2)

  • A Principal Component Analysis (PCA) based on gene expression values of the differently treated plants revealed that the patterns of plants exposed to P. brassicae feeding, M. brassicae feeding and artificial wounding were clearly separated from untreated control samples

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Summary

Introduction

In native environments plants frequently experience simultaneous or sequential unfavourable abiotic and biotic stresses. Plants have evolved a plethora of mechanisms to cope with abiotic or biotic environmental stress Plant defense responses induced by herbivore attack represent a strategy, which is mobilized only on demand [8, 9]. Inducible defense responses are associated with transcriptional regulation of many genes and shifts in phytohormone levels. Studied key regulators of wounding and herbivore defense responses are the phytohormones jasmonic acid (JA), abscisic acid (ABA), salicylic acid (SA) and ethylene (ET), which are the backbone of the plant immune signaling network [10,11,12,13,14,15]. Fine-tuning of defense responses to different herbivores is achieved by crosstalk of these signaling pathways and Oberländer et al BMC Plant Biology (2019) 19:338 may involve additional plant hormonal regulators like auxins, gibberellins, and brassinosteroids [13, 16]

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