Sugar transporters enable a leaf beetle to accumulate plant defense compounds

Yang, Zhi‐Ling; Nour-Eldin, Hussam Hassan; Haenniger, Sabine; Reichelt, Michael; Crocoll, Christoph; Seitz, Fabian; Vogel, Heiko; Beran, Franziska

doi:10.1101/2021.03.03.433712

Cited by 3 publications

(3 citation statements)

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“…We recently identified glucosinolatespecific transporters belonging to the major facilitator superfamily (MFS) in P. armoraciae and found two glucosinolate transporters to be expressed in the foregut, suggesting a role in glucosinolate uptake. However, silencing the expression of these transporters did not affect the uptake of ingested glucosinolates in adults, which indicates that additional or other transporters mediate glucosinolate absorption in P. armoraciae (Yang et al, 2021).…”

Section: Discussionmentioning

confidence: 92%

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

et al. 2021

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Myrosinase enzymes play a key role in the chemical defense of plants of the order Brassicales. Upon herbivory, myrosinases hydrolyze the β-S-linked glucose moiety of glucosinolates, the characteristic secondary metabolites of brassicaceous plants, which leads to the formation of different toxic hydrolysis products. The specialist flea beetle, Phyllotreta armoraciae, is capable of accumulating high levels of glucosinolates in the body and can thus at least partially avoid plant myrosinase activity. In feeding experiments with the myrosinase-deficient Arabidopsis thaliana tgg1 × tgg2 (tgg) mutant and the corresponding Arabidopsis Col-0 wild type, we investigated the influence of plant myrosinase activity on the metabolic fate of ingested glucosinolates in adult P. armoraciae beetles. Arabidopsis myrosinases hydrolyzed a fraction of ingested glucosinolates and thereby reduced the glucosinolate sequestration rate by up to 50% in adult beetles. These results show that P. armoraciae cannot fully prevent glucosinolate hydrolysis; however, the exposure of adult beetles to glucosinolate hydrolysis products had no impact on the beetle’s energy budget under our experimental conditions. To understand how P. armoraciae can partially prevent glucosinolate hydrolysis, we analyzed the short-term fate of ingested glucosinolates and found them to be rapidly absorbed from the gut. In addition, we determined the fate of ingested Arabidopsis myrosinase enzymes in P. armoraciae. Although we detected Arabidopsis myrosinase protein in the feces, we found only traces of myrosinase activity, suggesting that P. armoraciae can inactivate plant myrosinases in the gut. Based on our findings, we propose that the ability to tolerate plant myrosinase activity and a fast glucosinolate uptake mechanism represent key adaptations of P. armoraciae to their brassicaceous host plants.

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Section: Discussionmentioning

confidence: 92%

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

et al. 2021

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“…(2010) found that generalist herbivores were negatively affected by both indole and aliphatic GSL, whereas specialist herbivores were not affected. Many specialist herbivores of brassicaceous plants have evolved mechanisms to detoxify or sequester GSLs (Textor & Gershenzon, 2009; Jeschke et al ., 2016; Yang et al ., 2021). Delia radicum harbours gut microbes that can detoxify breakdown products of the aromatic GSL gluconasturtiin (Welte et al ., 2016).…”

Section: Discussionmentioning

confidence: 99%

Specialist root herbivore modulates plant transcriptome and downregulates defensive secondary metabolites in a brassicaceous plant

et al. 2022

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Plants face attackers aboveground and belowground. Insect root herbivores can lead to severe crop losses, yet the underlying transcriptomic responses have rarely been studied.We studied the dynamics of the transcriptomic response of Brussels sprouts (Brassica oleracea var. gemmifera) primary roots to feeding damage by cabbage root fly larvae (Delia radicum), alone or in combination with aboveground herbivory by cabbage aphids (Brevicoryne brassicae) or diamondback moth caterpillars (Plutella xylostella). This was supplemented with analyses of phytohormones and the main classes of secondary metabolites; aromatic, indole and aliphatic glucosinolates.Root herbivory leads to major transcriptomic rearrangement that is modulated by aboveground feeding caterpillars, but not aphids, through priming soon after root feeding starts.The root herbivore downregulates aliphatic glucosinolates. Knocking out aliphatic glucosinolate biosynthesis with CRISPR-Cas9 results in enhanced performance of the specialist root herbivore, indicating that the herbivore downregulates an effective defence.This study advances our understanding of how plants cope with root herbivory and highlights several novel aspects of insect-plant interactions for future research. Further, our findings may help breeders develop a sustainable solution to a devastating root pest.

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“…Using mutant Arabidopsis plants, Müller et al (2010) found that generalist herbivores were negatively affected by both indole and aliphatic GSL, but specialist herbivores were not affected. Many specialist herbivores of brassicaceous plants have evolved mechanisms to cope with GSLs (Textor & Gershenzon, 2009;Jeschke et al, 2016), and some species are even capable of sequestering specific GSLs for their own defence (Yang et al, 2021). Delia radicum harbours gut microbes that can detoxify breakdown products of the aromatic GSL gluconasturtiin (Welte et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Down to the roots: plant-mediated interactions between shoot- and root-feeding insect herbivores

Karssemeijer

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Plants and the tree of lifeThe first plants grew on terrestrial Earth over 450 Million year ago (Mya) (Kenrick & Crane, 1997). Early fossils show simple plants, much like liverworts that exist today. In the Devonian (420-360 Mya), plants had developed many of the structures we still see today. Vascular tissue, leaves, roots, and seeds evolved to cope with the difficulties of life on land (Kenrick & Crane, 1997). Since then, land plants have been the dominant primary producers in nearly every terrestrial ecosystem. Nowadays, over 350,000 species of plants are named and described (Royal Botanic Gardens Kew, 2016), ranging from towering trees to the smallest weed and from expansive grasses to the crops we eat. The downside of being at the basis of virtually all life on land is that everyone wants to eat you. Indeed, plants are on the menu for terrestrial life forms throughout the tree of life. Plant attackers comprise insects, arthropods, nematodes, mites, mammals, fungi, bacteria, viruses, oomycetes, unicellular eukaryotes, and even other plants. In natural ecosystems, these attackers help safeguard biodiversity by reducing dominant species (Carson & Root, 2000). However, in agricultural settings, a substantial amount of food is lost every year to pests and diseases (Oerke, 2006;Deutsch et al., 2018). To avoid economic losses, farmers commonly deploy chemical pesticides to protect their crops, causing great environmental costs and public health risks (

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Sugar transporters enable a leaf beetle to accumulate plant defense compounds

Cited by 3 publications

References 69 publications

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

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

Specialist root herbivore modulates plant transcriptome and downregulates defensive secondary metabolites in a brassicaceous plant

Down to the roots: plant-mediated interactions between shoot- and root-feeding insect herbivores

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