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

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.

Molecular characterization and functional analysis of cytochrome P450-mediated detoxification CYP302A1 gene involved in host plant adaptation in Spodoptera frugieprda

“…To survive, different tactics have been evolved by adapted herbivores to deal with the defense compound present in their host plants ( Heidel-Fischer and Vogel, 2015a ; Rashid War et al., 2018 ; Yang et al., 2022 ). Similarly, some herbivores insects metabolize and excrete plant defense compounds they consume, but others store them in their bodies to defend themselves against all-natural enemies ( Petschenka and Agrawal, 2016 ; Heckel, 2018 ).…”

Biology, Ecology, and Management of Flea Beetles in Brassica Crops

“…The closely related horseradish flea beetle (Phyllotreta armoraciae) also possesses a glucosinolatemyrosinase system that was shown to protect larvae against a generalist predator (122). The sequestration of ingested glucosinolates is presumably facilitated by a rapid glucosinolate uptake mechanism and manipulation of plant myrosinase activity in the beetle gut, which may at least partially prevent glucosinolate hydrolysis by plant myrosinases (123,151).…”

Metabolization and sequestration of plant specialized metabolites in insect herbivores: Current and emerging approaches

“…Sequestration requires the active transport of PSMs from the gut to other compartments. The transport of PSMs occurs rapidly and selectively after PSM ingestion, as PSMs such as some glucosinolates were observed to be taken up from the front gut part into the hemolymph of flea beetle Phyllotreta armoraciae and sawfly larvae Athalia rosae ( Abdalsamee et al, 2014 ; Yang et al, 2022 ). Sequestration of intact PSMs has been suggested to be a strategy to circumvent the enzymatic activation of the compound in the gut.…”