The UDP-Glycosyltransferase Gene Family in Achelura yunnanensis (Lepidoptera: Zygaenidae): Identification, Phylogeny, and Diverse Expression Patterns

Abstract

The caterpillars of the Lepidoptera are important herbivores as most of them belong to serious agricultural and forestry pests. To adapt to their habitats and feeding host plants, the larvae utilize uridine diphosphate (UDP)-glycosyltransferases (UGTs) to metabolize plant defensive compounds and insecticides. However, information on the UGT gene family in Achelura yunnanensis remains scarce. Here, we characterized the UGT genes through gene identification, phylogenic analyses, and comprehensive expression profiles regarding sexes, tissues, and stages. Transcriptome analyses led to the yields of 50 transcripts encoding UGTs in A. yunnanensis, representing a comparable gene number compared to those in other lepidopteran species. Sequence and phylogenetic analyses revealed a low amino acid identity of 28.23% among 31 full-length AyunUGTs, but some members shared relatively high conservation (>50% identities) with a phylogenetically clustered distribution. In addition, the majority of AyunUGTs possessed conserved residues involved in the catalysis and sugar-donor binding. Combining RNA sequencing and PCR approaches, a number of AyunUGTs were found to have the expression in chemosensory or detoxification tissues, possibly associated with the sensing of odorant molecules and the metabolism of toxic chemicals. More importantly, at least 27 AyunUGTs displayed detectable expression in reproductive tissues of both sexes. This study identifies candidate A. yunnanensis UGTs responsible for detoxification, olfaction, and reproduction, allowing us to address putative roles of UGTs in the adaptation of larvae to the habitats and feeding hosts.

Identification and characterization of uridine diphosphate glycosyltransferases in Dioryctria abietella, with an emphasis on putative roles in olfaction and reproduction

“…Each proportion of reproductive tissues was presented in a previous study (Wu et al 2022) samples of 16 tissues (Wang et al 2021). This hypothesis was further supported by the result of 50 AyunUGTs identified from two transcriptomes of female pheromone glands and 12 adult tissues in Achelura yunnanensis (Li et al 2021;Nuo et al 2021;Xiao et al 2022). However, D. abietella harbored fewer UGT genes than most of the moths with available genome sequences, including four noctuid species (see Table 2), B. mori (Huang et al 2008;Ahn et al 2012) and Manduca sexta (Kanost et al 2016), varying from 44 to 51 representatives.…”

“…Intriguingly, apart from the tissues correlated with detoxification, our present expression profiles revealed the presence of over 90% of DabiUGT genes in reproductive tissues. The high proportion of UGTs in reproductive systems was also observed in Helicoverpa armigera (>80%) (Pearce et al 2017), S. litura (>63%) (Xiao et al 2021) and A. yunnanensis (>54%) (Xiao et al 2022), suggestive of putative reproductive roles of moth UGTs.…”

“…for UGT43 specific to Noctuidae and Bombycidae and UGT45 not included in Noctuidae, Pyralidae, Bombycidae or Plutellidae (see Table 2). In D. abietella and other lepidopteran species, lineage-specific expansions in UGT33 and UGT40 subfamilies were generally observed, contributing mainly to the differences of UGT gene repertoire sizes across lepidopteran species (Ahn et al 2012;He et al 2017;Xiao et al 2022). Concerning the roles of the UGTs in the two subfamilies, it was noted that studies have documented their involvement in insect resistance to insecticides and plant defensive compounds, such as BmorUGT1 (BmorUGT40A1) in B. mori against plant allelochemicals (Luque et al 2002), CsupUGT33AG3 and CsupUGT40AL1 in C. suppressalis against chlorantraniliprole (Zhao et al 2019), PxylUGT2B17 (PxylUGT33AA2) in P. xylostella against chlorantraniliprole (Li et al 2017) and SfruUGT33F28 in S. frugiperda against benzoxazinoids (Israni et al 2020).…”

“…Initially, the olfactory association of insect UGTs was revealed as their transcripts were found to be abundantly present in the antennae (Robertson et al 1999;Wang et al 1999). Afterwards, many studies have indicated putative roles of UGTs in smell through antennal transcriptome sequencing and PCR-based strategies: AyunUGT9, AyunUGT18 and AyunUGT25 in A. yunnanensis (Xiao et al 2022); BmorUGT013829 (namely BmorUGT33D8) in B. mori (Huang et al 2008); PxylUGT33A1, PxylUGT33W1 and PxylUGT33Z1 in P. xylostella (He et al 2017); PantUGT3 and PantUGT18 in Pharsalia antennata (Yin et al 2022); HparUGT12651, HparUGT3119 and HparUGT8312 in Holotrichia parallela (Wang et al 2018); and DmelUGT35A1, DmelUGT37D1 and DmelUGT302C1 in Drosophila melanogaster (Younus et al 2014). Functional evidence of insect UGTs in olfaction was derived from SlitUGT40R3 and SlitUGT46A6 in Spodoptera littoralis as well as DmelUGT36E1 in D. melanogaster, with involvement in the detection of sex pheromones and plant odorants (Bozzolan et al 2014;Fraichard et al 2020).…”

“…Given the importance of UGTs in insect resistance, prior studies have mainly focused on their glycosylation of plant defensive substances and insecticides, as UGTs are enriched in three major detoxification organs in the larvae of Lepidoptera (fat body, midgut and Malpighian tubules) (Hu et al 2019;Zhao et al 2019;Israni et al 2020;Xiao et al 2022). In addition to larval stages, lepidopteran adults are also equipped with these three tissues, albeit less developed than in the larvae.…”