Glucosylation prevents plant defense activation in phloem-feeding insects

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

doi:10.1038/s41589-020-00658-6

Glucosylation prevents plant defense activation in phloem-feeding insects

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

^*Corresponding author for this work

Department of Entomology

Research output: Contribution to journal › Article › peer-review

27 Scopus citations

Abstract

The metabolic adaptations by which phloem-feeding insects counteract plant defense compounds are poorly known. Two-component plant defenses, such as glucosinolates, consist of a glucosylated protoxin that is activated by a glycoside hydrolase upon plant damage. Phloem-feeding herbivores are not generally believed to be negatively impacted by two-component defenses due to their slender piercing-sucking mouthparts, which minimize plant damage. However, here we document that glucosinolates are indeed activated during feeding by the whitefly Bemisia tabaci. This phloem feeder was also found to detoxify the majority of the glucosinolates it ingests by the stereoselective addition of glucose moieties, which prevents hydrolytic activation of these defense compounds. Glucosylation of glucosinolates in B. tabaci was accomplished via a transglucosidation mechanism, and two glycoside hydrolase family 13 (GH13) enzymes were shown to catalyze these reactions. This detoxification reaction was also found in a range of other phloem-feeding herbivores. [Figure not available: see fulltext.]

Original language	American English
Pages (from-to)	1420-1426
Number of pages	7
Journal	Nature Chemical Biology
Volume	16
Issue number	12
DOIs	https://doi.org/10.1038/s41589-020-00658-6
State	Published - Dec 2020

Bibliographical note

Funding Information:
We thank A. Douglas (Cornell University) for the SUC1 sequence, K. Falk for assistance with graphics, the MPI-CE, DSMZ and HUJI greenhouse teams for plant and insect maintenance, and other members of the African Cassava Whitefly Project (cassavawhitefly.org) for helpful discussions. This work was supported financially by the Max Planck Society, the Deutsche Forschungsgemeinschaft (DFG Collaborative Research Center 1127 ChemBioSys) and the Natural Resources Institute, University of Greenwich from a grant provided by the Bill and Melinda Gates Foundation (OPP1058938).

Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.

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Malka, O., Easson, M. L. A. E., Paetz, C., Götz, M., Reichelt, M., Stein, B., Luck, K., Stanišić, A., Juravel, K., Santos-Garcia, D., Mondaca, L. L., Springate, S., Colvin, J., Winter, S., Gershenzon, J., Morin, S., & Vassão, D. G. (2020). Glucosylation prevents plant defense activation in phloem-feeding insects. Nature Chemical Biology, 16(12), 1420-1426. https://doi.org/10.1038/s41589-020-00658-6

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title = "Glucosylation prevents plant defense activation in phloem-feeding insects",

abstract = "The metabolic adaptations by which phloem-feeding insects counteract plant defense compounds are poorly known. Two-component plant defenses, such as glucosinolates, consist of a glucosylated protoxin that is activated by a glycoside hydrolase upon plant damage. Phloem-feeding herbivores are not generally believed to be negatively impacted by two-component defenses due to their slender piercing-sucking mouthparts, which minimize plant damage. However, here we document that glucosinolates are indeed activated during feeding by the whitefly Bemisia tabaci. This phloem feeder was also found to detoxify the majority of the glucosinolates it ingests by the stereoselective addition of glucose moieties, which prevents hydrolytic activation of these defense compounds. Glucosylation of glucosinolates in B. tabaci was accomplished via a transglucosidation mechanism, and two glycoside hydrolase family 13 (GH13) enzymes were shown to catalyze these reactions. This detoxification reaction was also found in a range of other phloem-feeding herbivores. [Figure not available: see fulltext.]",

author = "Osnat Malka and Easson, {Michael L.A.E.} and Christian Paetz and Monika G{\"o}tz and Michael Reichelt and Beate Stein and Katrin Luck and Aleksa Stani{\v s}i{\'c} and Ksenia Juravel and Diego Santos-Garcia and Mondaca, {Lilach L.} and Simon Springate and John Colvin and Stephan Winter and Jonathan Gershenzon and Shai Morin and Vass{\~a}o, {Daniel G.}",

note = "Funding Information: We thank A. Douglas (Cornell University) for the SUC1 sequence, K. Falk for assistance with graphics, the MPI-CE, DSMZ and HUJI greenhouse teams for plant and insect maintenance, and other members of the African Cassava Whitefly Project (cassavawhitefly.org) for helpful discussions. This work was supported financially by the Max Planck Society, the Deutsche Forschungsgemeinschaft (DFG Collaborative Research Center 1127 ChemBioSys) and the Natural Resources Institute, University of Greenwich from a grant provided by the Bill and Melinda Gates Foundation (OPP1058938). Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.",

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doi = "10.1038/s41589-020-00658-6",

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Malka, O, Easson, MLAE, Paetz, C, Götz, M, Reichelt, M, Stein, B, Luck, K, Stanišić, A, Juravel, K, Santos-Garcia, D, Mondaca, LL, Springate, S, Colvin, J, Winter, S, Gershenzon, J, Morin, S & Vassão, DG 2020, 'Glucosylation prevents plant defense activation in phloem-feeding insects', Nature Chemical Biology, vol. 16, no. 12, pp. 1420-1426. https://doi.org/10.1038/s41589-020-00658-6

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T1 - Glucosylation prevents plant defense activation in phloem-feeding insects

AU - Malka, Osnat

AU - Easson, Michael L.A.E.

AU - Paetz, Christian

AU - Götz, Monika

AU - Reichelt, Michael

AU - Stein, Beate

AU - Luck, Katrin

AU - Stanišić, Aleksa

AU - Juravel, Ksenia

AU - Santos-Garcia, Diego

AU - Mondaca, Lilach L.

AU - Springate, Simon

AU - Colvin, John

AU - Winter, Stephan

AU - Gershenzon, Jonathan

AU - Morin, Shai

AU - Vassão, Daniel G.

N1 - Funding Information: We thank A. Douglas (Cornell University) for the SUC1 sequence, K. Falk for assistance with graphics, the MPI-CE, DSMZ and HUJI greenhouse teams for plant and insect maintenance, and other members of the African Cassava Whitefly Project (cassavawhitefly.org) for helpful discussions. This work was supported financially by the Max Planck Society, the Deutsche Forschungsgemeinschaft (DFG Collaborative Research Center 1127 ChemBioSys) and the Natural Resources Institute, University of Greenwich from a grant provided by the Bill and Melinda Gates Foundation (OPP1058938). Publisher Copyright: © 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2020/12

Y1 - 2020/12

N2 - The metabolic adaptations by which phloem-feeding insects counteract plant defense compounds are poorly known. Two-component plant defenses, such as glucosinolates, consist of a glucosylated protoxin that is activated by a glycoside hydrolase upon plant damage. Phloem-feeding herbivores are not generally believed to be negatively impacted by two-component defenses due to their slender piercing-sucking mouthparts, which minimize plant damage. However, here we document that glucosinolates are indeed activated during feeding by the whitefly Bemisia tabaci. This phloem feeder was also found to detoxify the majority of the glucosinolates it ingests by the stereoselective addition of glucose moieties, which prevents hydrolytic activation of these defense compounds. Glucosylation of glucosinolates in B. tabaci was accomplished via a transglucosidation mechanism, and two glycoside hydrolase family 13 (GH13) enzymes were shown to catalyze these reactions. This detoxification reaction was also found in a range of other phloem-feeding herbivores. [Figure not available: see fulltext.]

AB - The metabolic adaptations by which phloem-feeding insects counteract plant defense compounds are poorly known. Two-component plant defenses, such as glucosinolates, consist of a glucosylated protoxin that is activated by a glycoside hydrolase upon plant damage. Phloem-feeding herbivores are not generally believed to be negatively impacted by two-component defenses due to their slender piercing-sucking mouthparts, which minimize plant damage. However, here we document that glucosinolates are indeed activated during feeding by the whitefly Bemisia tabaci. This phloem feeder was also found to detoxify the majority of the glucosinolates it ingests by the stereoselective addition of glucose moieties, which prevents hydrolytic activation of these defense compounds. Glucosylation of glucosinolates in B. tabaci was accomplished via a transglucosidation mechanism, and two glycoside hydrolase family 13 (GH13) enzymes were shown to catalyze these reactions. This detoxification reaction was also found in a range of other phloem-feeding herbivores. [Figure not available: see fulltext.]

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ER -

Glucosylation prevents plant defense activation in phloem-feeding insects

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