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Of mites and cyanide: Rapid spider mite adaptation to Arabidopsis defense metabolites

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To get a meal, herbivores must contend with the extensive chemical arsenal of plants, an arsenal that collectively exceeds 200,000 compounds (Pichersky and Gang, 2000). While some herbivores opt to… Click to show full abstract

To get a meal, herbivores must contend with the extensive chemical arsenal of plants, an arsenal that collectively exceeds 200,000 compounds (Pichersky and Gang, 2000). While some herbivores opt to specialize on one or a few hosts, the two-spotted spider mite (Tetranychus urticae) is an opportunistic feeder able to utilize an astounding array of plant species (Rioja et al., 2017). Many generalist herbivores enjoy a broad host range because they can quickly acclimate to a diverse portfolio of plant defenses. In contrast, individual spider mite populations are locally adapted to just one or a few species but can evolve counter-measures to combat the defense compounds of a different plant within a few generations (Salehipourshirazi et al., 2021). This rapid specialization enables spider mites to serially colonize additional plant hosts. However, the nature of adapted counter defense traits and the mechanisms through which they evolve have remained elusive. Although spider mites are able to colonize over 1,000 plant species, Arabidopsis (Arabidopsis thaliana) is not a typical host. The defense repertoire of Arabidopsis includes amino acid-derived glucosinolates. Once synthesized, glucosinolates, in their glycoside form, are stored in plant cells as innocuous precursors. Upon tissue disruption caused by herbivore attack, for example, these glycosidic precursors are hydrolyzed, releasing bioactive compounds, including isothiocyanates or nitriles (Halkier and Gershenzon, 2006). In its chemical defense against spider mites, Arabidopsis primarily uses indole glucosinolates, derived from the amino acid tryptophan (Zhurov et al., 2014; Figure 1A). Spider mites, however, are no slouches in this chemical arms race and can adapt readily to different plant defense compounds. For example, Salehipourshirazi et al. (2021) transferred a spider mite population adapted to the common bean (Phaseolus vulgaris) to two Arabidopsis genotypes: either the well-defended wild-type Col-0 (Col-0) or the vulnerable cytochrome P450 CYP79B2 CYP79B3 double mutant (cyp79b2 cyp79b3) that lacks the ability to synthesize indole glucosinolates (Figure 1B). After suffering initially, the spider mites adapted to their newly colonized hosts in 25 generations ( 18 months), yielding Col-0-adapted and cyp79b2 cyp79b3-adapted populations that are genetically distinct from their bean-adapted ancestors (Figure 1B). In this issue of Plant Physiology, Dixit et al. (2022) employed an elegant transcriptomics experiment to identify genetic and functional changes underlying spider mite adaptation to Arabidopsis. Bean-adapted, Col-0-adapted, and cyp79b2 cyp79b3-adapted mites were reared on bean, Col-0, and cyp79b2 cyp79b3 plants, after which transcriptomes of the nine mite sample groups (three mite genotypes three plant genotypes) were sequenced in triplicate, enabling the authors to quantify expression level and coding sequence differences. The authors identified 59 transcripts more highly expressed in Col-0-adapted mites than cyp79b2 cyp79b3adapted and bean-adapted mites, including several involved in detoxification of foreign metabolites (i.e. xenobiotics) (Figure 1C). One of the transcripts enriched in Col-0-adapted mites, TuCAS, which encodes b-cyanoalanine synthase (CAS), stood out to the authors. Baseline TuCAS expression was uniform across the three mite genotypes when fed bean leaves. However, when mites were reared on Arabidopsis leaves (either Col-0 or cyp79b2 cyp79b3), TuCAS expression was induced in Col-0-adapted mites, but not bean-adapted or cyp79b2 cyp79b3-adapted mites. The authors puzzled over why TuCAS would be induced in Arabidopsis-fed spider mites. Due to its ability to detoxify cyanide, TuCAS is required for spider mites to handle consumption of cyanide-releasing cyanogenic glycosides, but these defense compounds are not N ew s an d V ie w s

Keywords: spider mite; defense; spider; plant; spider mites; arabidopsis

Journal Title: Plant Physiology
Year Published: 2022

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