Abstract

Most molecular-genetic studies of plant defense responses to arthropod herbivores have focused on insects. However, plant-feeding 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, feeding on a staggering number of plant hosts. To understand the interactions between spider mite and a plant at the molecular level, we examined reciprocal genome-wide responses of mites and its host Arabidopsis (Arabidopsis thaliana). Despite differences in feeding guilds, we found that transcriptional responses of Arabidopsis to mite herbivory resembled those observed for lepidopteran herbivores. Mutant analysis of induced plant defense pathways showed functionally that only a subset of induced programs, including jasmonic acid signaling and biosynthesis of indole glucosinolates, are central to Arabidopsis's defense to mite herbivory. On the herbivore side, indole glucosinolates dramatically increased mite mortality and development times. We identified an indole glucosinolate dose-dependent increase in the number of differentially expressed mite genes belonging to pathways associated with detoxification of xenobiotics. This demonstrates that spider mite is sensitive to Arabidopsis defenses that have also been associated with the deterrence of insect herbivores that are very distantly related to chelicerates. Our findings provide molecular insights into the nature of, and response to, herbivory for a representative of a major class of arthropod herbivores.

Highlights

  • Most molecular-genetic studies of plant defense responses to arthropod herbivores have focused on insects

  • Our current understanding of plant responses to insect herbivores suggests that plants perceive herbivore attack by recognizing general herbivory-associated molecular patterns, which are elicitors originating mainly from the herbivore’s oral secretions (Bonaventure, 2012), and by damage-associated molecular patterns (DAMPs) that result from wounding or enzymatic reactions imposed by the herbivore (Pearce et al, 1991; McGurl et al, 1992; Schmelz et al, 2006; Yamaguchi and Huffaker, 2011)

  • The transcriptional responses of Arabidopsis to spider mite feeding during the initial 24-h period are characterized by differentially expressed genes (DEGs) that can be partitioned into two broad groups

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Summary

Introduction

Most molecular-genetic studies of plant defense responses to arthropod herbivores have focused on insects. We identified an indole glucosinolate dose-dependent increase in the number of differentially expressed mite genes belonging to pathways associated with detoxification of xenobiotics This demonstrates that spider mite is sensitive to Arabidopsis defenses that have been associated with the deterrence of insect herbivores that are very distantly related to chelicerates. Others such as thrips combine rasping and sucking to feed, while the phloemfeeding insects like aphids connect their feeding tube to the phloem and cause minimal tissue disruption Another group of arthropods of major ecological and agricultural importance are the chelicerates, which include phytophagous (plant-feeding) mites that pierce plant tissue to feed on cell contents (Tanigoshi and Davis, 1978; Campbell et al, 1990). This species is a major agricultural pest worldwide and has been documented to feed on over 1,100 different plant species, including more than 150 crop plants

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