Antennal and Abdominal Transcriptomes Reveal Chemosensory Genes in the Asian Citrus Psyllid, Diaphorina citri

Abstract

The Asian citrus psyllid, Diaphorina citri is the principal vector of the highly destructive citrus disease called Huanglongbing (HLB) or citrus greening, which is a major threat to citrus cultivation worldwide. More effective pest control strategies against this pest entail the identification of potential chemosensory proteins that could be used in the development of attractants or repellents. However, the molecular basis of olfaction in the Asian citrus psyllid is not completely understood. Therefore, we performed this study to analyze the antennal and abdominal transcriptome of the Asian citrus psyllid. We identified a large number of transcripts belonging to nine chemoreception-related gene families and compared their expression in male and female adult antennae and terminal abdomen. In total, 9 odorant binding proteins (OBPs), 12 chemosensory proteins (CSPs), 46 odorant receptors (ORs), 20 gustatory receptors (GRs), 35 ionotropic receptors (IRs), 4 sensory neuron membrane proteins (SNMPs) and 4 different gene families encoding odorant-degrading enzymes (ODEs): 80 cytochrome P450s (CYPs), 12 esterase (ESTs), and 5 aldehyde dehydrogenases (ADE) were annotated in the D. citri antennal and abdominal transcriptomes. Our results revealed that a large proportion of chemosensory genes exhibited no distinct differences in their expression patterns in the antennae and terminal abdominal tissues. Notably, RNA sequencing (RNA-seq) data and quantitative real time-PCR (qPCR) analyses showed that 4 DictOBPs, 4 DictCSPs, 4 DictIRs, 1 DictSNMP, and 2 DictCYPs were upregulated in the antennae relative to that in terminal abdominal tissues. Furthermore, 2 DictOBPs (DictOBP8 and DictOBP9), 2 DictCSPs (DictOBP8 and DictOBP12), 4 DictIRs (DictIR3, DictIR6, DictIR10, and DictIR35), and 1 DictCYP (DictCYP57) were expressed at higher levels in the male antennae than in the female antennae. Our study provides the first insights into the molecular basis of chemoreception in this insect pest. Further studies on the identified differentially expressed genes would facilitate the understanding of insect olfaction and their role in the interactions between olfactory system and biological processes.

Modulation of Sex Pheromone Discrimination by a UDP-Glycosyltransferase in Drosophila melanogaster

“…In insects, the characterization of metabolizing enzymes received an increasing interest with regard to their role in insecticide resistance, adaptation to host plant volatile and their function; as ODEs, in the termination of the olfactory signal to maintain a relatively high olfactory sensitivity toward new stimuli. In particular, recent studies investigating the antennal transcriptome in different species identified varied ODEs including CYP, CES, GST and UGT [11][12][13][14][15][16][17][18][19][20][21][22][23][24]. These reports have completed and confirmed the case-by-case identification of previously characterized ODEs [25][26][27][28][29][30][31].…”

Chemosensory proteins in the CSP4 clade evolved as plant immunity suppressors before two suborders of plant-feeding hemipteran insects diverged

“…CSPs may therefore be expressed in multiple tissues where they regulate a variety of processes in insects often, but not always, upon binding small molecules. Aphids have about 10 CSP genes, and similar numbers were identified in related plant-sucking insects of the order Hemiptera, such as the whitefly Bemisia tabaci and psyllid Diaphorina citri (13)(14)(15)(16). Aphid CSPs were previously known as OS-D-like proteins (17).…”

Molecular cloning and comparative analysis of transcripts encoding chemosensory proteins from two plant bugs, Lygus lineolaris and Lygus hesperus

“…The discovery that all of the annotated CSPs in Daphnia pulex , an aquatic crustacean that is evolutionarily distant to insects, are pentahelical suggests that the pentahelical CSP clade pre‐dates terrestrial colonization and has thus likely gained new functionalities in development and cellular homeostasis. The presence of two different genes encoding these CSPs in L. lineolaris and L. hesperus along with T. castaneum (Vieira & Rozas, ), A. mellifera (Wanner et al ., ; Forêt et al ., ; Vieira & Rozas, ), A. pisum (Vieira & Rozas, ), Anopheles gambiae (Vieira & Rozas, ), and Diaphorina citri (Wu et al ., ) suggests that the lone genes reported in D. melanogaster (Vieira & Rozas, ) and Pediculus humanus (Vieira & Rozas, ) may be the result of gene loss.…”

“…Although CSPs have been most extensively characterized in dipterans and lepidopterans, advances in transcriptomic resources have facilitated their identification in a number of hemipterans (Jacobs et al ., ; Zhou et al ., , , , ; Xu et al ., ; Gu et al ., , ; Hua et al ., , ; Futahashi et al ., ; Ribeiro et al ., ; Sun et al ., ; Cui et al ., ; Wang et al ., ; Wu et al ., ; Xue et al ., ; Liu et al ., ). Similar to CSPs in other insect orders, hemipteran CSPs are broadly expressed (Zhou et al ., , , ; Wang et al ., ).…”