Glucosylation prevents plant defense activation in phloem-feeding insects

Malka, Osnat; Easson, Michael L. A. E.; Paetz, Christian; Götz, Monika; Reichelt, Michael; Stein, Beate; Luck, Katrin; Stanišić, Aleksa; Juravel, Ksenia; Santos-García, Diego; Mondaca, Lilach Lily; Springate, Simon; Colvin, John; Winter, Stephan; Gershenzon, Jonathan; Morin, Shai; Vassão, Daniel Giddings

doi:10.1038/s41589-020-00658-6

Cited by 36 publications

(27 citation statements)

References 59 publications

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“…This substrate preference also complements well another preemptive glucosinolate detoxification mechanism in B. tabaci, the formation of glucosylated glucosinolates. Analysis of honeydew from B. tabaci feeding on A. thaliana showed that glucosylation was found to occur mostly to aliphatic glucosinolates and few glucosylated indolic glucosinolate derivatives were detected (Malka et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…Nevertheless, it seems clear that B. tabaci uses several different biochemical strategies to deal with glucosinolates. Besides the serial glucosylation of glucosinolates (Malka et al, 2020), a glutathione-S-transferase enzyme has also been reported in B. tabaci (Eakteiman et al, 2018) that can metabolize the hydrolysis products of both major aliphatic and indolic glucosinolates present in A. thaliana. This latter activity might help to mitigate the potential negative effects caused by the small amounts of glucosinolates successfully activated during and after ingestion by neutralizing the toxic hydrolysis products.…”

Section: Discussionmentioning

confidence: 99%

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Identification of a Sulfatase that Detoxifies Glucosinolates in the Phloem-Feeding Insect Bemisia tabaci and Prefers Indolic Glucosinolates

et al. 2021

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Cruciferous plants in the order Brassicales defend themselves from herbivory using glucosinolates: sulfur-containing pro-toxic metabolites that are activated by hydrolysis to form compounds, such as isothiocyanates, which are toxic to insects and other organisms. Some herbivores are known to circumvent glucosinolate activation with glucosinolate sulfatases (GSSs), enzymes that convert glucosinolates into inactive desulfoglucosinolates. This strategy is a major glucosinolate detoxification pathway in a phloem-feeding insect, the silverleaf whitefly Bemisia tabaci, a serious agricultural pest of cruciferous vegetables. In this study, we identified and characterized an enzyme responsible for glucosinolate desulfation in the globally distributed B. tabaci species MEAM1. In in vitro assays, this sulfatase showed a clear preference for indolic glucosinolates compared with aliphatic glucosinolates, consistent with the greater representation of desulfated indolic glucosinolates in honeydew. B. tabaci might use this detoxification strategy specifically against indolic glucosinolates since plants may preferentially deploy indolic glucosinolates against phloem-feeding insects. In vivo silencing of the expression of the B. tabaci GSS gene via RNA interference led to lower levels of desulfoglucosinolates in honeydew. Our findings expand the knowledge on the biochemistry of glucosinolate detoxification in phloem-feeding insects and suggest how detoxification pathways might facilitate plant colonization in a generalist herbivore.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Identification of a Sulfatase that Detoxifies Glucosinolates in the Phloem-Feeding Insect Bemisia tabaci and Prefers Indolic Glucosinolates

et al. 2021

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“…Moreover, whitefly can desulfate glucosinolates as a way of detoxification and reduce the contents of glucosinolates via feeding 38,39 . A recent report shows that whitefly may glucosylate glucosinolates using two glycoside hydrolase family 13 (GH13) enzymes, thereby preventing hydrolytic activation of glucosinolates 40 . These features, alone or in combination, may affect the interactions between whitefly and glucosinolates and minimize the effects of glucosinolates of host plants on whiteflies.…”

Section: Discussionmentioning

confidence: 99%

Performance of two species of whiteflies is unaffected by glucosinolate profile in Brassica plants

Qian

Pan

et al. 2021

Pest Management Science

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BACKGROUND While plant glucosinolates are known to impart resistance to many insects, their role in the interactions between plants and many phloem‐feeding insects such as whiteflies are poorly understood. The whitefly Bemisia tabaci complex comprises many cryptic species that differ in the ability to utilize Brassica plants. However, whether Brassica plants‐specific traits such as glucosinolates determine differences of whiteflies in colonizing Brassica plants remains in question. RESULTS We first observed performance of two whitefly species MEAM1 and Asia II 3, which differ obviously in their ability to colonize Brassica plants, on four cultivars of three Brassica species that vary in glucosinolate profile. We found that the life history characteristics of each of the two whitefly species seems to be only marginally affected by cultivar. We next used wild‐type Arabidopsis plants and mutants defective in glucosinolate biosynthesis or hydrolysis to explore the effects of glucosinolates on the whitefly. We found that fecundity and development of immature stages of neither of the two whitefly species differ significantly between wild‐type and mutants. CONCLUSION The data suggest that glucosinolates may have little effect on the oviposition by adults and the survival and development of immature stages of MEAM1 and Asia II 3 whiteflies. The marked differences in colonizing Brassica crops between the two whitefly species are likely due to plant traits other than glucosinolates. © 2021 Society of Chemical Industry.

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“…Furthermore, nectar constituents such as carbohydrate are known to influence, for instance, mosquito sugar meal choices and longevity both positively and negatively or potentially toxic secondary metabolites such as alkaloids (Ignell et al, 2010;Kessler et al, 2013). Plant sugar feeding also has neutralization benefit of plant defense (Malka et al, 2020). However, we cannot rule out that feeding on plants will not affect either the number of eggs nor survival if we try other plants that S. calcitrans has a choice of under natural conditions, as plant species vary in the amount and quality of resources (Roulston et al, 2000;Nyasembe et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Supplementing Blood Diet With Plant Nectar Enhances Egg Fertility in Stomoxys calcitrans

et al. 2021

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Stomoxys calcitrans (stable fly) is a cosmopolitan biting fly of both medical and veterinary importance. Unlike blood-feeding-related behavior of stable fly, its plant feeding, the fitness value, and the S. calcitrans–plant interaction are less understood. Here we show based on two chloroplast DNA genes, ribulose bisphosphate carboxylase large chain (rbcL) and the intergenic spacer gene trnH-psbA, that field-collected male and female stable flies fed on various plant species. We investigated the fitness cost of plant feeding using Parthenium hysterophorus, one of the plant species identified to have been fed on by the field-collected flies. Supplementation of blood feeding with a flowering P. hysterophorus plant as nectar source enhanced egg hatchability significantly as compared to blood alone, showing the fitness value of nectar supplementation. However, nectar supplementation did not affect the number of eggs laid or longevity of S. calcitrans as compared to flies that fed on blood alone. S. calcitrans maintained on sugar alone failed to lay eggs. The various plants stable flies fed on demonstrated chemodiversity with their own signature scent. The behavioral response of S. calcitrans to these signature compounds varied from strong attraction (γ-terpinene) to neutral (linalool oxide and myrcene) to repellency (butanoic acid). Our study demonstrated that stable flies feed on nectar, and plant nectar supplementation of blood feeding enhanced larval emergence. Thus, our result has implication in stable fly reproduction, survival, disease transmission, boosting laboratory colony, and the possibility of using plant-derived odors for mass trapping of stable fly, for instance, using γ-terpinene.

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Glucosylation prevents plant defense activation in phloem-feeding insects

Cited by 36 publications

References 59 publications

Identification of a Sulfatase that Detoxifies Glucosinolates in the Phloem-Feeding Insect Bemisia tabaci and Prefers Indolic Glucosinolates

Identification of a Sulfatase that Detoxifies Glucosinolates in the Phloem-Feeding Insect Bemisia tabaci and Prefers Indolic Glucosinolates

Performance of two species of whiteflies is unaffected by glucosinolate profile in Brassica plants

Supplementing Blood Diet With Plant Nectar Enhances Egg Fertility in Stomoxys calcitrans

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