The Digestive System of the Two-Spotted Spider Mite, Tetranychus urticae Koch, in the Context of the Mite-Plant Interaction

Abstract

The two-spotted spider mite (TSSM), Tetranychus urticae Koch (Acari: Tetranychidae), is one of the most polyphagous herbivores, feeding on more than 1,100 plant species. Its wide host range suggests that TSSM has an extraordinary ability to modulate its digestive and xenobiotic physiology. The analysis of the TSSM genome revealed the expansion of gene families that encode proteins involved in digestion and detoxification, many of which were associated with mite responses to host shifts. The majority of plant defense compounds that directly impact mite fitness are ingested. They interface mite compounds aimed at counteracting their effect in the gut. Despite several detailed ultrastructural studies, our knowledge of the TSSM digestive tract that is needed to support the functional analysis of digestive and detoxification physiology is lacking. Here, using a variety of histological and microscopy techniques, and a diversity of tracer dyes, we describe the organization and properties of the TSSM alimentary system. We define the cellular nature of floating vesicles in the midgut lumen that are proposed to be the site of intracellular digestion of plant macromolecules. In addition, by following the TSSM's ability to intake compounds of defined sizes, we determine a cut off size for the ingestible particles. Moreover, we demonstrate the existence of a distinct filtering function between midgut compartments which enables separation of molecules by size. Furthermore, we broadly define the spatial distribution of the expression domains of genes involved in digestion and detoxification. Finally, we discuss the relative simplicity of the spider mite digestive system in the context of mite's digestive and xenobiotic physiology, and consequences it has on the effectiveness of plant defenses.

A Leaf-Mimicking Method for Oral Delivery of Bioactive Substances Into Sucking Arthropod Herbivores

“…To examine whether the mesh method can be used for oral delivery of nanoparticles, newly emerged adult T. urticae females were placed onto the feeding device (100 mites/device) using 1 cm 2 of nylon mesh sheet (opening size: 100 µm) to which polystyrene fluorescent microspheres (diameter, 500 nm; Polysciences, Warrington, PA, USA) suspended in 1% (w/v) blue tracer dye solution was added. According to Bensoussan et al (2018), mites can uptake 500-nm-diameter particles with their stylets, and the size cutoff is around 750 nm. After allowing mites to feed for 24 h, fluorescent images were taken with a digital camera (EOS Kiss X7, Canon, Tokyo, Japan) installed on a fluorescence stereomicroscope (M205FA; Leica Microsystems, Wetzlar, Germany) fitted with a GFP filter (395-455 nm excitation, >480 nm emission) with an exposure time of 5 s (ISO: 200).…”

Structural and functional characterization of an intradiol ring-cleavage dioxygenase from the polyphagous spider mite herbivore Tetranychus urticae Koch

“…Furthermore, if TuIDRCD is involved in detoxification, then it is expected that it will be secreted and active in the digestive tract, a compartment where plant and mite compartments intercept. At present, it is not known where within the gut digestion and detoxification occur (Bensoussan et al, 2018).…”

The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles

“…Khomyakov (1967) has looked at digestion and nutrition in soil haematophages. Recently an elegant dissection of anatomical and physiological flexibility of Tetranychus urticae has been published- Bensoussan et al (2018). Astigmatid carbohydrases and their relationship to feeding adaptations have been studied by various workers (Barabanova 1981;Bowman 1984b; Akimov and Oksentyuk 2018)-as have a variety of oribatids been investigated (Šustr and Starý 1998).…”