Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)

Abstract Herbivorous insects often possess the ability to detoxify chemical defenses from their host plants. The fall armyworm (Spodoptera frugiperda), which feeds principally on maize, detoxifies the maize benzoxazinoid 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) by stereoselective re-glu...

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Main Authors: Bhawana Israni, Katrin Luck, Samantha C. W. Römhild, Bettina Raguschke, Natalie Wielsch, Yvonne Hupfer, Michael Reichelt, Aleš Svatoš, Jonathan Gershenzon, Daniel Giddings Vassão
Format: Article
Language:English
Published: Nature Portfolio 2022-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-14551-w
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author Bhawana Israni
Katrin Luck
Samantha C. W. Römhild
Bettina Raguschke
Natalie Wielsch
Yvonne Hupfer
Michael Reichelt
Aleš Svatoš
Jonathan Gershenzon
Daniel Giddings Vassão
author_facet Bhawana Israni
Katrin Luck
Samantha C. W. Römhild
Bettina Raguschke
Natalie Wielsch
Yvonne Hupfer
Michael Reichelt
Aleš Svatoš
Jonathan Gershenzon
Daniel Giddings Vassão
author_sort Bhawana Israni
collection DOAJ
description Abstract Herbivorous insects often possess the ability to detoxify chemical defenses from their host plants. The fall armyworm (Spodoptera frugiperda), which feeds principally on maize, detoxifies the maize benzoxazinoid 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) by stereoselective re-glucosylation using a UDP-glucosyltransferase, SfUGT33F28. SfUGT33F28 activity is induced by feeding on a DIMBOA-containing diet, but how this induction is regulated is unknown. In the present work, we describe the alternative splicing of the SfUGT33F28 transcript. Variant transcripts are differentially expressed in response to DIMBOA, and this transcriptional response is mediated by an insect aryl hydrocarbon receptor. These variants have large deletions leading to the production of truncated proteins that have no intrinsic UGT activity with DIMBOA but interact with the full-length enzyme to raise or lower its activity. Therefore, the formation of SfUGT33F28 splice variants induces DIMBOA-conjugating UGT activity when DIMBOA is present in the insect diet and represses activity in the absence of this plant defense compound.
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spelling doaj.art-1f85b9c5afaf41978ee6f850402ebec12022-12-22T02:38:30ZengNature PortfolioScientific Reports2045-23222022-06-0112111710.1038/s41598-022-14551-wAlternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)Bhawana Israni0Katrin Luck1Samantha C. W. Römhild2Bettina Raguschke3Natalie Wielsch4Yvonne Hupfer5Michael Reichelt6Aleš Svatoš7Jonathan Gershenzon8Daniel Giddings Vassão9Max Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyMax Planck Institute for Chemical EcologyAbstract Herbivorous insects often possess the ability to detoxify chemical defenses from their host plants. The fall armyworm (Spodoptera frugiperda), which feeds principally on maize, detoxifies the maize benzoxazinoid 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) by stereoselective re-glucosylation using a UDP-glucosyltransferase, SfUGT33F28. SfUGT33F28 activity is induced by feeding on a DIMBOA-containing diet, but how this induction is regulated is unknown. In the present work, we describe the alternative splicing of the SfUGT33F28 transcript. Variant transcripts are differentially expressed in response to DIMBOA, and this transcriptional response is mediated by an insect aryl hydrocarbon receptor. These variants have large deletions leading to the production of truncated proteins that have no intrinsic UGT activity with DIMBOA but interact with the full-length enzyme to raise or lower its activity. Therefore, the formation of SfUGT33F28 splice variants induces DIMBOA-conjugating UGT activity when DIMBOA is present in the insect diet and represses activity in the absence of this plant defense compound.https://doi.org/10.1038/s41598-022-14551-w
spellingShingle Bhawana Israni
Katrin Luck
Samantha C. W. Römhild
Bettina Raguschke
Natalie Wielsch
Yvonne Hupfer
Michael Reichelt
Aleš Svatoš
Jonathan Gershenzon
Daniel Giddings Vassão
Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)
Scientific Reports
title Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)
title_full Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)
title_fullStr Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)
title_full_unstemmed Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)
title_short Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda)
title_sort alternative transcript splicing regulates udp glucosyltransferase catalyzed detoxification of dimboa in the fall armyworm spodoptera frugiperda
url https://doi.org/10.1038/s41598-022-14551-w
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