Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host

Abstract

Generalist arthropod herbivores rapidly adapt to a broad range of host plants. However, the extent of transcriptional reprogramming in the herbivore and its hosts associated with adaptation remains poorly understood. Using the spider mite Tetranychus urticae and tomato as models with available genomic resources, we investigated the reciprocal genomewide transcriptional changes in both spider mite and tomato as a consequence of mite's adaptation to tomato. We transferred a genetically diverse mite population from bean to tomato where triplicated populations were allowed to propagate for 30 generations. Evolving populations greatly increased their reproductive performance on tomato relative to their progenitors when reared under identical conditions, indicative of genetic adaptation. Analysis of transcriptional changes associated with mite adaptation to tomato revealed two main components. First, adaptation resulted in a set of mite genes that were constitutively downregulated, independently of the host. These genes were mostly of an unknown function. Second, adapted mites mounted an altered transcriptional response that had greater amplitude of changes when re-exposed to tomato, relative to nonadapted mites. This gene set was enriched in genes encoding detoxifying enzymes and xenobiotic transporters. Besides the direct effects on mite gene expression, adaptation also indirectly affected the tomato transcriptional responses, which were attenuated upon feeding of adapted mites, relative to the induced responses by nonadapted mite feeding. Thus, constitutive downregulation and increased transcriptional plasticity of genes in a herbivore may play a central role in adaptation to host plants, leading to both a higher detoxification potential and reduced production of plant defence compounds.

Cross-talk between high light stress and plant defence to the two-spotted spider mite in Arabidopsis thaliana

“…The two-spotted spider mite (TSSM) (Tetranychus urticae Koch; Prostigmata: Tetranychidae) is one of the most destructive polyphagous arthropod herbivores, feeding on hundreds of wild and crop plant species. Recently, several transcriptomic approaches allowed to establish molecular basis of its ability to adapt to different host plant species such as Arabidopsis, tomato and grapevine (Grbić et al 2011;Wybouw et al 2015;Díaz-Riquelme et al 2016;Rioja et al 2017). These thorough analyses often included monitoring of host plant transcriptional dynamics upon TSSM infestation and together with Arabidopsis and tomato focused research (Zhurov et al 2014;Martel et al 2015), gave an extensive overview on gene expression changes occurred starting from the early time points of infestation.…”

Drought-stressed tomato plants trigger bottom-up effects on key mite pests

“…The proliferation (Grbic et al, 2011) and transcriptional plasticity of gene families involved in detoxification and digestion processes (Dermauw et al, 2013;Wybouw et al, 2015) have been proposed as one of the reasons of the adaption capacity of T. urticae to novel hosts. Four main detoxification enzymes families have been described: P450 monooxygenases, carboxyl/cholinesterases, glutathione-S-transferases (GST), and ATP-binding cassette transporters; which respond strongly in T. urticae in relation to host plant switching (Van Leuween and Dermauw, 2016).…”

“…T. urticae has been reported to increase the levels of sucrose on damaged cotton tissue (Schmidt et al, 2009). In tomato, T. urticae infestation down regulates the transcriptional response associated with anabolic processes, including the expression of amino acid catabolizing enzyme genes Wybouw et al, 2015). However, when the effects of T. urticae on free amino acid content in tomato were analyzed, inconsistent results were obtained (Nachappa et al, 2013;Errard et al, 2016).…”

“…While this species has been reported feeding on more than 1000 plant species Dorkeld, 2006-2015), local mite populations do not perform equally well on all potential hosts (Gotoh et al, 1993;Kant et al, 2008). The capability of T. urticae to cope with the varying nutritional value and defense compounds of different host plants has been explained by the proliferation of gene families involved in digestion and detoxification processes (Grbic et al, 2011;Van Leeuwen and Dermauw, 2016) and by its transcriptional plasticity in response to host plant shifts (Dermauw et al, 2013;Wybouw et al, 2015).…”

“…However, some genotypes of T. urticae are able to manipulate the main defense pathways in tomato, resulting in an attenuated induction of defense genes to levels at which they are less detrimental (Kant et al, 2008;Alba et al, 2015). Interestingly, Wybouw et al (2015) demonstrated that during their adaptation to tomato, T. urticae extensively rearranged their xenobiotic metabolism through differential expression of genes that code for detoxifying enzymes and xenobiotic transporters, and acquired the ability to interfere with plant defenses.…”