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-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.

Transcriptomic investigation of the molecular mechanisms underlying resistance to the neonicotinoid thiamethoxam and the pyrethroid lambda‐cyhalothrin in Euschistus heros (Hemiptera: Pentatomidae)

“…[46][47][48] UGTs are common, highly diverse enzymes that mediate the metabolization of xenobiotics in insects, including pyrethroids and neonicotinoids. [49][50][51][52] The specific UDP-glucosyltransferase overexpressed in our study was highly similar to the 2- Galactosylceramides are cerebrosides commonly associated with vertebrates, while ceramide phosphoethanolamine is the cerebroside reported as the main constituent of myelinic membranes in invertebrates. 53,54 Additionally, the domain families of 2-hydroxyacylsphingosine 1-beta-galactosyltransferases from hemipterans differ from those of human 2-hydroxyacylsphingosine 1-beta-galactosyltransferases (data not shown), supporting the different role of this UGT in insects.…”

“…Increased activity of GSTs is commonly reported as a resistance mechanism to pesticides in insects 46–48 . UGTs are common, highly diverse enzymes that mediate the metabolization of xenobiotics in insects, including pyrethroids and neonicotinoids 49–52 . The specific UDP‐glucosyltransferase overexpressed in our study was highly similar to the 2‐hydroxyacylsphingosine 1‐beta‐galactosyltransferase‐like gene from Halyomorpha halys.…”

Influence of plant defense signaling and innate insect metabolic differences to the overall performance of fall armyworm (Spodoptera frugiperda) corn and rice strains on maize as a host

“…Furthermore, an alternate SfUGT33F28 variant was discovered that is formed by alternative splicing and is inducible by DIMBOA. This variant is truncated, but interacts with full length SfUGT33F28 to enhance re-glucosylation (Israni et al 2022). Accordingly, both the canonical SfUGT33F28 and alternately spliced transcript SfUGT33F28_tv1 were measured from the RNA isolated from insect guts and normalized to housekeeping gene SfRPL10 .…”

“…Subsequent work has provided evidence for the expression of UGT33F28 splicing variants that can regulate the reglucosylation activity of the canonical protein. The expression of transcript variant 1 ( tv1 ) in particular was demonstrated to be induced in response to DIMBOA treatment, with the translated protein SfUGT33F28_v1 physically interacting with, and positively regulating the activity of the canonical protein (Israni et al 2022). Transcript variant 1 expression was constitutively higher in rice strain than corn strain larvae.…”

“…But more work needs to be done to understand strain differences in detoxifying BXDs. Recently, we have demonstrated that SfUGT33F28 can be expressed as transcriptional variants that are regulated by DIMBOA and can interact with the canonical protein and regulate the basal activity of SfUGT33F28 (Israni et al 2022). It would be thus interesting to learn how alternate SfUGT33F28 transcripts differ between FAW strains.…”