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. 2023 Apr 4:14:1183610.
doi: 10.3389/fphys.2023.1183610. eCollection 2023.

Antennal transcriptomic analysis of carboxylesterases and glutathione S-transferases associated with odorant degradation in the tea gray geometrid, Ectropis grisescens (Lepidoptera, Geometridae)

Fangmei Zhang  1   2 , Yijun Chen  1   3 , Xiaocen Zhao  1 , Shibao Guo  1 , Feng Hong  1 , Yanan Zhi  1 , Li Zhang  1 , Zhou Zhou  1 , Yunhui Zhang  2 , Xuguo Zhou  4 , Xiangrui Li  2
Affiliations

Antennal transcriptomic analysis of carboxylesterases and glutathione S-transferases associated with odorant degradation in the tea gray geometrid, Ectropis grisescens (Lepidoptera, Geometridae)

Fangmei Zhang et al. Front Physiol. .

Abstract

Introduction: Carboxylesterases (CXEs) and glutathione S-transferases (GSTs) can terminate olfactory signals during chemosensation by rapid degradation of odorants in the vicinity of receptors. The tea grey geometrid, Ectropis grisescens (Lepidoptera, Geometridae), one of the most devastating insect herbivores of tea plants in China, relies heavily on plant volatiles to locate the host plants as well as the oviposition sites. However, CXEs and GSTs involved in signal termination and odorant clearance in E. grisescens remains unknown. Methods: In this study, identification and spatial expression profiles of CXEs and GSTs in this major tea pest were investigated by transcriptomics and qRT-PCR, respectively. Results: As a result, we identified 28 CXEs and 16 GSTs from female and male antennal transcriptomes. Phylogenetic analyses clustered these candidates into several clades, among which antennal CXEs, mitochondrial and cytosolic CXEs, and delta group GSTs contained genes commonly associated with odorants degradation. Spatial expression profiles showed that most CXEs (26) were expressed in antennae. In comparison, putative GSTs exhibited a diverse expression pattern across different tissues, with one GST expressed specifically in the male antennae. Disscussion: These combined results suggest that 12 CXEs (EgriCXE1, 2, 4, 6, 8, 18, 20-22, 24, 26, and 29) and 5 GSTs (EgriGST1 and EgriGST delta group) provide a major source of candidate genes for odorants degradation in E. grisescens.

Keywords: Ectropis grisescens; antennal transcriptome; carboxylesterases; glutathione S-transferases; odorant-degrading enzyme.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer WX declared a shared parent affiliation with the authors YZ and XL to the handling editor at the time of review.

Figures

FIGURE 1
FIGURE 1
Characterization and transcriptome analysis of RNA sequences from antennae of E. grisescens. (A) Length distributions of the transcriptome and unigenes of E. grisescens. (B) Species distribution from the Blastx results of E. grisescens unigenes in the NR database. (C) GO classifications of E. grisescens unigenes. (D) KEGG classifications of E. grisescens unigenes; a: cellular processes, b: environmental information processing, c: genetic information processing, d: metabolism, e: organismal systems.
FIGURE 2
FIGURE 2
Phylogenetic analysis of candidate EgriCXEs with other insect CXEs. MCEs: mitochondrial and cytosolic esterases; JHEs: Lepidopteran juvenile hormone esterases; NR: neuroreceptor; NL: neuroligin; C/AEs: cuticular and antennal esterases; β-EPEs: β-esterases and pheromone esterases; MAEs: moth antennal esterases; M-α-Es: microsomal α-esterases. Egri, Ectropis grisescens (N = 28); Eobl, Ectropis obliqua (N = 34); Slitt, Spodoptera littoralis (N = 19); Pint, Plodia interpunctella (N = 19); Sexi, Spodoptera exigua (N = 8); Slitu, Spodoptera litura (N = 3); Sinf, Sesamia inferens (N = 16). Candidate EgriCXEs are indicated by red. The GenBank accession numbers of the 127 CXEs protein used in the phylogenetic analysis are listed in Supplementary Table S8.
FIGURE 3
FIGURE 3
Phylogenetic analysis of candidate EgriGSTs with other insect GSTs. Egri, Ectropis grisescens (N = 16); Pint, Plodia interpunctella (N = 12); Pxyl, Plutella xylostella (N = 19); Cpom, Cydia pomonella (N = 11); Bmor, Bombyx mori (N = 18); Csup, Chilo suppressalis (N = 15); Apis, Acyrthosiphon pisum (N = 14); Dmel, Drosophila melanogaster (N = 20); Agam, Anopheles gambiae (N = 16); Tcas, Tribolium castaneum (N = 12); Gmol, Grapholita molesta (N = 1); Szea, Sitophilus zeamais (N = 1). Candidate EgriGSTs are indicated by red. The GenBank accession numbers of the 159 GSTs protein used in the phylogenetic analysis are listed in Supplementary Table S9.
FIGURE 4
FIGURE 4
Tissue- and sex-specific expression pattern of the EgriCXEs. A total of 28 EgriCXEs were clustered using relative expression values from each of the tissues. Expression values are relative to female head tissue (one-fold), with red and blue representing the highest and the lowest values, respectively. FAn: female antennae; FH: female head; FT: female thorax; FAb: female abdomen; FL: female leg; FW: female wing; MAn: male antennae; MH: male head; MT: male thorax; MAb: male abdomen; ML: male leg; MW: male wing.
FIGURE 5
FIGURE 5
Tissue- and sex-specific expression pattern of the EgriGSTs. A total of 16 EgriGSTs were clustered using relative expression values from each of the tissues.
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