Rapid and Selective Absorption of Plant Defense Compounds From the Gut of a Sequestering Insect.

Zhi-Ling Yang,Veit Grabe,Sandor Nietzsche,Fabian Seitz,Rolf Beutel,Michael Reichelt,Adrian Richter,Franziska Beran

doi:10.3389/fphys.2022.846732

Abstract

Many herbivorous insects exploit defense compounds produced by their host plants for protection against predators. Ingested plant defense compounds are absorbed via the gut epithelium and stored in the body, a physiological process that is currently not well understood. Here, we investigated the absorption of plant defense compounds from the gut in the horseradish flea beetle, Phyllotreta armoraciae, a specialist herbivore known to selectively sequester glucosinolates from its brassicaceous host plants. Feeding experiments using a mixture of glucosinolates and other glucosides not found in the host plants showed a rapid and selective uptake of glucosinolates in adult beetles. In addition, we provide evidence that this uptake mainly takes place in the foregut, whereas the endodermal midgut is the normal region of absorption. Absorption via the foregut epithelium is surprising as the apical membrane is covered by a chitinous intima. However, we could show that this cuticular layer differs in its structure and overall thickness between P. armoraciae and a non-sequestering leaf beetle. In P. armoraciae, we observed a thinner cuticle with a less dense chitinous matrix, which might facilitate glucosinolate absorption. Our results show that a selective and rapid uptake of glucosinolates from the anterior region of the gut contributes to the selective sequestration of glucosinolates in P. armoraciae.

Highlights

Herbivorous insects evolved diverse strategies to cope with defense compounds present in their host plants (Pentzold et al, 2014; Heidel-Fischer and Vogel, 2015; Rashid War et al, 2018)
We compared how much of each glucoside was sequestered in the beetle body and found that significantly more ingested glucosinolates had been sequestered than non-host glucosides (Figure 1C; generalized least squares, F = 96.645, p < 0.001)
The relative distribution of the six glucosides in beetle tissues differed, with most glucosinolates found in the body, and most non-host glucosides found in the head and gut (Figure 1D)

Summary

Introduction

Herbivorous insects evolved diverse strategies to cope with defense compounds present in their host plants (Pentzold et al, 2014; Heidel-Fischer and Vogel, 2015; Rashid War et al, 2018). While some insects metabolize and excrete ingested plant defense compounds, others accumulate them in their body and thereby protect themselves against generalist natural enemies (Opitz and Müller, 2009; Heckel, 2014; Petschenka and Agrawal, 2016). The latter strategy, known as sequestration, requires physiological adaptations that enable the transport of ingested defense compounds from the gut to storage sites in the body cavity The membrane lipid composition has been proposed to play a role as cardiac glycosides are presumably passively absorbed across the gut (Scudder and Meredith, 1982) Another way to prevent the passive absorption of less polar defense compounds, such as ouabain, is their active excretion from gut epithelial cells by efflux carriers (Agrawal et al, 2012)

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