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Comparative transcriptomics of tomato plants simultaneously infested with different species of herbivorous mites reveals distinct signatures of host defense suppression

ABSTRACT: Tomato plants are commonly attacked by herbivorous mites, including by generalist Tetranychus urticae and specialists Tetranychus evansi and Aculops lycopersici. Mite feeding induces plant defense responses that reduce mite performance. However, via poorly understood mechanisms, T. evansi and A. lycopersici suppress plant defenses and, consequently, maintain a high performance on tomato. Accordingly, on a shared host, non-adapted T. urticae can be facilitated by either of the specialist mites, likely via the suppression of plant defenses. To better understand defense suppression and indirect plant-mediated interactions between herbivorous mites, we used microarrays to analyze transcriptomic changes in tomato after attack by either a single mite species (T. urticae, T. evansi, A. lycopersici) or two species simultaneously (T. urticae plus T. evansi or T. urticae plus A. lycopersici). Additionally, we assessed mite-induced changes in defense-associated phytohormones using LC-MS/MS. Compared to non-infested controls, jasmonates (JAs) and salicylate (SA) accumulated to higher amounts upon all mite-infestation treatments, but lowest increases were detected after single infestations with defense-suppressors. Strikingly, whereas 8 to 10% of tomato genes was differentially expressed upon single infestations with T. urticae or A. lycopersici, only 0.1% was altered in T. evansi-infested plants. Transcriptome analysis of dual-infested leaves revealed that T. evansi dampened T. urticae-triggered host responses on a genome-wide scale, while A. lycopersici primarily suppressed T. urticae-induced JA defenses. Our results provide valuable new insights into the mechanisms underlying host defense suppression and the plant-mediated facilitation of competing herbivores.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE116827 | GEO | 2018/11/20

REPOSITORIES: GEO

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Project description:While pathogen-induced immunity is comparatively well characterized, far less is known about plant defense responses to arthropod herbivores. To date, most molecular-genetic studies of plant-arthropod interactions have focused on insects. However, plant-feeding (phytophagous) mites are also pests of diverse plants, and mites induce different patterns of damage to plant tissues than do well-studied insects (e.g., Lepidopteran larvae or aphids). The two-spotted spider mite, Tetranychus urticae, is among the most significant mite pests in agriculture. T. urticae is an extreme generalist that has been documented on a staggering number of plant hosts (more than 1,100), and is renowned for the rapid evolution of pesticide resistance. To understand reciprocal interactions between T. urticae and a plant host at the molecular level, we examined mite herbivory using Arabidopsis thaliana. Despite differences in feeding guilds, we found that transcriptional responses of A. thaliana to mite herbivory generally resembled those observed for insect herbivores. In particular, defense to mites was mediated by jasmonic acid (JA) biosynthesis and signaling. Further, indole glucosinolates dramatically increased mite mortality and development times. Variation in both basal and activated levels of these defense pathways might also explain differences in mite damage and feeding success between A. thaliana accessions. On the herbivore side, a diverse set of genes associated with detoxification of xenobiotics was induced upon exposure to increasing levels of in planta indole glucosinolates. Our findings provide molecular insights into the nature of, and response to, herbivory for a representative of a major class of arthropod herbivores. We used microarray to assess global gene expresion in Arabidopsis thaliana upon Tetranychus urticae attack in two A. thaliana accessions: Bla-2, resistant to spider mite herbivory and Kon, susceptible to spider mite herbivory. 3 week old Arabidopsis thaliana plants were subjected to Tetranychus urticae attack through application of 10 mites for various periods of time (timecourse scenario) or hundreds of mites for 1 hour (feeding site scenario).

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Comparative transcriptomics of tomato plants simultaneously infested with different species of herbivorous mites reveals distinct signatures of host defense suppression

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