Transcriptional and metabolite analysis reveal a shift in direct and indirect defences in response to spider-mite infestation in cucumber (Cucumis sativus)

Jun He,Iris F Kappers,Marcel Dicke,Harro J Bouwmeester

doi:10.1007/s11103-020-01005-y

Jun He, Iris F Kappers + Show 2 more

Open Access

https://doi.org/10.1007/s11103-020-01005-y

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Abstract

Key messageCucumber plants adapt their transcriptome and metabolome as result of spider mite infestation with opposite consequences for direct and indirect defences in two genotypes.Plants respond to arthropod attack with the rearrangement of their transcriptome which lead to subsequent phenotypic changes in the plants’ metabolome. Here, we analysed transcriptomic and metabolite responses of two cucumber (Cucumis sativus) genotypes to chelicerate spider mites (Tetranychus urticae) during the first 3 days of infestation. Genes associated with the metabolism of jasmonates, phenylpropanoids, terpenoids and l-phenylalanine were most strongly upregulated. Also, genes involved in the biosynthesis of precursors for indirect defence-related terpenoids were upregulated while those involved in the biosynthesis of direct defence-related cucurbitacin C were downregulated. Consistent with the observed transcriptional changes, terpenoid emission increased and cucurbitacin C content decreased during early spider-mite herbivory. To further study the regulatory network that underlies induced defence to spider mites, differentially expressed genes that encode transcription factors (TFs) were analysed. Correlation analysis of the expression of TF genes with metabolism-associated genes resulted in putative identification of regulators of herbivore-induced terpenoid, green-leaf volatiles and cucurbitacin biosynthesis. Our data provide a global image of the transcriptional changes in cucumber leaves in response to spider-mite herbivory and that of metabolites that are potentially involved in the regulation of induced direct and indirect defences against spider-mite herbivory.

Highlights

Plants have two types of defence strategies that affect herbivores either in a direct or an indirect way and both strategies can be constitutively present or be induced upon herbivory (Mithofer and Boland 2012)
Comparison between TSSM-induced DEGs in Arabidopsis and tomato revealed a conserved role for genes involved in jasmonic acid (JA) signalling, and the biosynthesis of phenylpropanoids, flavonoids and terpenoids in response to this herbivore while in tomato gene sets related to anabolism were suppressed suggesting a possible shift from growth to defence (Martel et al 2015)
Green Leaf Volatiles (GLVs)—including (E)2-hexenal, (Z)-3-hexen-1-ol and (Z)-3-hexenyl acetate—rapidly increased on the first day post infestation followed by a small decrease in the 2 days and was stronger in CO compared to Chinese long (CL) (Fig. 1d)

Summary

Introduction

Plants have two types of defence strategies that affect herbivores either in a direct or an indirect way and both strategies can be constitutively present or be induced upon herbivory (Mithofer and Boland 2012). Re-configuration of the metabolome, including endogenous compounds and emitted volatiles, results from prior re-configuration of the transcriptome in which multiple phytohormones and transcription factors (TFs) interplay to regulate the complex networks that up-regulate or suppress defence-related genes (Ozawa et al 2000; Wu and Baldwin 2010). Plants perceive herbivory attack via damage- or herbivore-associated molecular patterns (Mithofer and Boland 2008) and upon recognition, phytohormones modulate the response to different attackers, the exact mechanisms are unclear (Lazebnik et al 2014). Different TF families, including MYB, bHLH, WRKY, AP2/ERF, NAC and bZIP play a role in plant defence (Seo and Choi 2015) and multiple of such TFs have been related to changes in the transcription of metabolism-associated genes, resulting in an altered metabolic profile of the infested plant (Wu and Baldwin 2010)

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