Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

Sporer, Theresa; Körnig, Johannes; Wielsch, Natalie; Gebauer-Jung, Steffi; Reichelt, Michael; Hupfer, Yvonne; Beran, Franziska

doi:10.3389/fpls.2021.645030

Cited by 25 publications

(43 citation statements)

References 52 publications

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“…However, compared to the midgut, the foregut is a poorly studied part of the insect digestive system and has been largely excluded from studies of active uptake of hydrophilic compounds. Adults of P. armoraciae were previously shown to absorb a major proportion of ingested glucosinolates within a few minutes from the gut, which demonstrates that glucosinolates are taken up in the anterior part of the digestive tract with an efficient and fast mechanism (Sporer et al, 2021). In this study, we detected ingested glucosinolates in the beetle body when the corresponding plant material was still in the foregut, suggesting that these glucosinolates have been absorbed across the foregut epithelium within less than 1 min after oral uptake (Figure 2).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2022

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2022

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Section: Countering and Exploiting The Mustard Oil Bomb By Pests And Pathogensmentioning

confidence: 99%

“…Interestingly, feeding experiments with the myrosinase-deficient Arabidopsis tgg1/tgg2 mutant and wild type plants indicate that plant myrosinases reduced the glucosinolate sequestration rate by the insect in adult beetles [99]. Further analysis revealed that P. armoraciae can inactivate plant myrosinases in the gut to both reduce glucosinolate hydrolysis and promote their sequestering [99]. These findings indicate that adaptations of P. armoraciae to their brassicaceous host plants involve both the ability to tolerate plant myrosinase activity and a fast glucosinolate uptake mechanism.…”

Section: Countering and Exploiting The Mustard Oil Bomb By Pests And Pathogensmentioning

confidence: 99%

“…Other herbivores develop other mechanisms such as sequestering glucosinolates and inhibition of plant myrosinases to counter the mustard oil bomb. The specialist flea beetle, Phyllotreta armoraciae, is capable of absorbing from the gut high levels of glucosinolates in the body and can thus at least partially avoid plant myrosinase activity [99] (Figure 5). Interestingly, feeding experiments with the myrosinase-deficient Arabidopsis tgg1/tgg2 mutant and wild type plants indicate that plant myrosinases reduced the glucosinolate sequestration rate by the insect in adult beetles [99].…”

Section: Countering and Exploiting The Mustard Oil Bomb By Pests And Pathogensmentioning

confidence: 99%

“…The specialist flea beetle, Phyllotreta armoraciae, is capable of absorbing from the gut high levels of glucosinolates in the body and can thus at least partially avoid plant myrosinase activity [99] (Figure 5). Interestingly, feeding experiments with the myrosinase-deficient Arabidopsis tgg1/tgg2 mutant and wild type plants indicate that plant myrosinases reduced the glucosinolate sequestration rate by the insect in adult beetles [99]. Further analysis revealed that P. armoraciae can inactivate plant myrosinases in the gut to both reduce glucosinolate hydrolysis and promote their sequestering [99].…”

Section: Countering and Exploiting The Mustard Oil Bomb By Pests And Pathogensmentioning

confidence: 99%

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The Cellular and Subcellular Organization of the Glucosinolate–Myrosinase System against Herbivores and Pathogens

Fan

et al. 2022

IJMS

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Glucosinolates are an important class of secondary metabolites in Brassicales plants with a critical role in chemical defense. Glucosinolates are chemically inactive but can be hydrolyzed by myrosinases to produce a range of chemically active compounds toxic to herbivores and pathogens, thereby constituting the glucosinolate–myrosinase defense system or the mustard oil bomb. During the evolution, Brassicales plants have developed not only complex biosynthetic pathways for production of a large number of glucosinolate structures but also different classes of myrosinases that differ in catalytic mechanisms and substrate specificity. Studies over the past several decades have made important progress in the understanding of the cellular and subcellular organization of the glucosinolate–myrosinase system for rapid and timely detonation of the mustard oil bomb upon tissue damage after herbivore feeding and pathogen infection. Progress has also been made in understanding the mechanisms that herbivores and pathogens have evolved to counter the mustard oil bomb. In this review, we summarize our current understanding of the function and organization of the glucosinolate–myrosinase system in Brassicales plants and discuss both the progresses and future challenges in addressing this complex defense system as an excellent model for analyzing plant chemical defense.

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Selection pressure by specialist and generalist insect herbivores leads to optimal constitutive plant defense. A mathematical model

Chakraborty,

Gershenzon,

Schuster

2023

Ecology and Evolution

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Brassicaceae plants have the glucosinolate–myrosinase defense system, jointly active against herbivory. However, constitutive glucosinolate (GLS) defense is observed to occur at levels that do not deter all insects from feeding. That prompts the question of why Brassicaceae plants have not evolved a higher constitutive defense. The answer may lie in the contrasting relationship between plant defense and host plant preference of specialist and generalist herbivores. GLS content increases a plant's susceptibility to specialist insects. In contrast, generalists are deterred by the plant GLSs. Although GLSs can attract the natural enemies (predators and parasitoids) of these herbivores, enemies can reduce herbivore pressure to some extent only. So, plants can be overrun by specialists if GLS content is too high, whereas generalists can invade the plants if it is too low. Therefore, an optimal constitutive plant defense can minimize the overall herbivore pressure. To explain the optimal defense theoretically, we model the contrasting host selection behavior of insect herbivores and the emergence of their natural enemies by non‐autonomous ordinary differential equations, where the independent variable is the plant GLS concentration. From the model, we quantify the optimal amount of GLSs, which minimizes total herbivore (specialists and generalists) pressure. That quite successfully explains the evolution of constitutive defense in plants from the perspective of optimality theory.

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Hijacking the Mustard-Oil Bomb: How a Glucosinolate-Sequestering Flea Beetle Copes With Plant Myrosinases

Cited by 25 publications

References 52 publications

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

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

The Cellular and Subcellular Organization of the Glucosinolate–Myrosinase System against Herbivores and Pathogens

Selection pressure by specialist and generalist insect herbivores leads to optimal constitutive plant defense. A mathematical model

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