Comparative analysis of the UDP-glycosyltransferase multigene family in insects

Department of Entomology, Max Planck Institute for Chemical Ecology, Jena 07745, Germany.
Insect biochemistry and molecular biology (Impact Factor: 3.45). 12/2011; 42(2):133-47. DOI: 10.1016/j.ibmb.2011.11.006
Source: PubMed


UDP-glycosyltransferases (UGT) catalyze the conjugation of a range of diverse small lipophilic compounds with sugars to produce glycosides, playing an important role in the detoxification of xenobiotics and in the regulation of endobiotics in insects. Recent progress in genome sequencing has enabled an assessment of the extent of the UGT multigene family in insects. Here we report over 310 putative UGT genes identified from genomic databases of eight different insect species together with a transcript database from the lepidopteran Helicoverpa armigera. Phylogenetic analysis of the insect UGTs showed Order-specific gene diversification and inter-species conservation of this multigene family. Only one family (UGT50) is found in all insect species surveyed (except the pea aphid) and may be homologous to mammalian UGT8. Three families (UGT31, UGT32, and UGT305) related to Lepidopteran UGTs are unique to baculoviruses. A lepidopteran sub-tree constructed with 40 H. armigera UGTs and 44 Bombyx mori UGTs revealed that lineage-specific expansions of some families in both species appear to be driven by diversification in the N-terminal substrate binding domain, increasing the range of compounds that could be detoxified or regulated by glycosylation. By comparison of the deduced protein sequences, several important domains were predicted, including the N-terminal signal peptide, UGT signature motif, and C-terminal transmembrane domain. Furthermore, several conserved residues putatively involved in sugar donor binding and catalytic mechanism were also identified by comparison with human UGTs. Many UGTs were expressed in fat body, midgut, and Malpighian tubules, consistent with functions in detoxification, and some were expressed in antennae, suggesting a role in pheromone deactivation. Transcript variants derived from alternative splicing, exon skipping, or intron retention produced additional UGT diversity. These findings from this comparative study of two lepidopteran UGTs as well as other insects reveal a diversity comparable to this gene family in vertebrates, plants and fungi and show the magnitude of the task ahead, to determine biochemical function and physiological relevance of each UGT enzyme.

Download full-text


Available from: Heiko Vogel, Jul 25, 2014
  • Source
    • "In the tobacco hornworm, Manduca sexta, a GST restricted to pheromone sensilla called GST-msolf1 plays a significant role in sex pheromone detection by inactivating the aldehyde component of the sex pheromone blend (Rogers et al., 1999). UGTs are another group of enzymes linked to odorant and xenobiotic degradation (Ahn et al., 2012). In insects UGTs are known to assist in enzymatic detoxification by catalyzing the glycosylation of lipophilic compounds (Despres et al., 2007). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The metabolism of volatile signal molecules by odorant degrading enzymes (ODEs) is crucial to the ongoing sensitivity and specificity of chemoreception in various insects, and a few specific esterases, cytochrome P450s, glutathione S-transferases (GSTs) and UDP-glucosyltransferases (UGTs) have previously been implicated in this process. Significant progress has been made in characterizing ODEs in Lepidoptera but very little is known about them in Diptera, including in D. melanogaster, a major insect model. We have therefore carried out a transcriptomic analysis of the antennae of D.melanogaster in order to identify candidate ODEs. Virgin male and female and mated female antennal transcriptomes were determined by RNAseq. As with the Lepidoptera, we found that many esterases, cytochrome P450 enzymes, GSTs and UGTs are expressed in D. melanogaster antennae. As olfactory genes generally show selective expression in the antennae, a comparison to previously published transcriptomes for other tissues has been performed, showing preferential expression in the antennae for one esterase, JHEdup, one cytochrome P450, CYP308a1, and one GST, GSTE4. These largely uncharacterized enzymes are now prime candidates for ODE functions. Jhedup was expressed heterologously and found to have high catalytic activity against a chemically diverse group of known ester odorants for this species. This is a finding consistent with an ODE although it might suggest a general role in clearing several odorants rather than a specific role in clearing a particular odorant. Our findings do not preclude the possibility of odorant degrading functions for other antennally expressed esterases, P450s, GSTs and UGTs but, if so, they suggest that these enzymes also have additional functions in other tissues.
    Insect Biochemistry and Molecular Biology 10/2014; 53. DOI:10.1016/j.ibmb.2014.07.003 · 3.45 Impact Factor
  • Source
    • "Two sequences, UGT40R2 and UGT40R3 were very similar: their C-terminal parts were nearly identical, whereas their N-terminal substrate binding domains were more variable. This suggested that they might be produced by alternative splicing of the same gene, according to different substrate specificities, as shown for several B. mori and H. armigera UGTs (Ahn et al., 2012). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Uridine diphosphate UDP-glycosyltransferases (UGTs) are detoxification enzymes widely distributed within living organisms. They are involved in the biotransformation of various lipophilic endogenous compounds and xenobiotics, including odorants. Several UGTs have been reported in the olfactory organs of mammals and involved in olfactory processing and detoxification within the olfactory mucosa but, in insects, this enzyme family is still poorly studied. Despite recent transcriptomic analyses, the diversity of antennal UGTs in insects has not been investigated. To date, only three UGT cDNAs have been shown to be expressed in insect olfactory organs. In the present study, we report the identification of eleven putative UGTs expressed in the antennae of the model pest insect Spodoptera littoralis. Phylogenetic analysis revealed that these UGTs belong to five different families, highlighting their structural diversity. In addition, two genes, UGT40R3 and UGT46A6, were either specifically expressed or overexpressed in the antennae, suggesting specific roles in this sensory organ. Exposure of male moths to the sex pheromone and to a plant odorant differentially downregulated the transcription levels of these two genes, revealing for the first time the regulation of insect UGTs by odorant exposure. Moreover, the specific antennal gene UGT46A6 was upregulated by insecticide topical application on antennae, suggesting its role in the protection of the olfactory organ towards xenobiotics. This work highlights the structural and functional diversity of UGTs within this highly specialized tissue.
    Insect Molecular Biology 05/2014; 23(5). DOI:10.1111/imb.12100 · 2.59 Impact Factor
  • Source
    • "The observed optimum at physiological pH suggests an intracellular localisation of the respective enzyme, presumably in gut epithelial cells. Enzymatic glycosylation of toxic compounds is a widespread counter-adaptation of insect herbivores to deactivate the chemical defence systems of their host plants (Ahn et al., 2012; Despres et al., 2007). The transfer of a sugar moiety from a donor to an acceptor molecule is typically catalysed by UDP-glucosyltransferases (UGTs). "
    [Show abstract] [Hide abstract]
    ABSTRACT: In order to defend themselves against arthropod herbivores, maize plants produce 1,4-benzoxazin-3-ones (BXs), which are stored as weakly active glucosides in the vacuole. Upon tissue disruption, BXs come into contact with beta-glucosidases, resulting in the release of active aglycones and their breakdown products. While some aglycones can be reglucosylated by specialist herbivores, little is known about how they detoxify BX breakdown products. Here we report on the structure of an N-glucoside, 3-beta-D-glucopyranosyl-6-methoxy-2-benzoxazolinone (MBOA-N-Glc), purified from Spodoptera frugiperda faeces. In vitro assays showed that MBOA-N-Glc is formed enzymatically in the insect gut using the BX breakdown product 6-methoxy-2-benzoxazolinone (MBOA) as precursor. While Spodoptera littoralis and S. frugiperda caterpillars readily glucosylated MBOA, larvae of the European corn borer Ostrinia nubilalis were hardly able to process the molecule. Accordingly, Spodoptera caterpillar growth was unaffected by the presence of MBOA, while O. nubilalis growth was reduced. We conclude that glucosylation of MBOA is an important detoxification mechanism that helps insects tolerate maize BXs.
    Phytochemistry 03/2014; 102. DOI:10.1016/j.phytochem.2014.03.018 · 2.55 Impact Factor
Show more