Identification of Odor-Processing Genes in the Emerald Ash Borer, Agrilus planipennis

Abstract

BackgroundInsects rely on olfaction to locate food, mates, and suitable oviposition sites for successful completion of their life cycle. Agrilus planipennis Fairmaire (emerald ash borer) is a serious invasive insect pest that has killed tens of millions of North American ash (Fraxinus spp) trees and threatens the very existence of the genus Fraxinus. Adult A. planipennis are attracted to host volatiles and conspecifics; however, to date no molecular knowledge exists on olfaction in A. planipennis. Hence, we undertook an antennae-specific transcriptomic study to identify the repertoire of odor processing genes involved in A. planipennis olfaction.Methodology and Principal FindingsWe acquired 139,085 Roche/454 GS FLX transcriptomic reads that were assembled into 30,615 high quality expressed sequence tags (ESTs), including 3,249 isotigs and 27,366 non-isotigs (contigs and singletons). Intriguingly, the majority of the A. planipennis antennal transcripts (59.72%) did not show similarity with sequences deposited in the non-redundant database of GenBank, potentially representing novel genes. Functional annotation and KEGG analysis revealed pathways associated with signaling and detoxification. Several odor processing genes (9 odorant binding proteins, 2 odorant receptors, 1 sensory neuron membrane protein and 134 odorant/xenobiotic degradation enzymes, including cytochrome P450s, glutathione-S-transferases; esterases, etc.) putatively involved in olfaction processes were identified. Quantitative PCR of candidate genes in male and female A. planipennis in different developmental stages revealed developmental- and sex-biased expression patterns.Conclusions and SignificanceThe antennal ESTs derived from A. planipennis constitute a rich molecular resource for the identification of genes potentially involved in the olfaction process of A. planipennis. These findings should help in understanding the processing of antennally-active compounds (e.g. 7-epi-sesquithujene) previously identified in this serious invasive pest.

Identification of candidate chemosensory genes in the antennal transcriptome of Tenebrio molitor (Coleoptera: Tenebrionidae)

“…We identified 20 ORs in T. molitor, which is far fewer than the 341 OR genes (including 79 pseudogenes) identified in the T. castaneum genome (Engsontia et al, 2008), and also fewer than identified for M. caryae (57) (Mitchell et al, 2012), I. typographus (43) and D. ponderosae (49) (Andersson et al, 2013), but more than that in A. planipennis (2) (Mamidala et al, 2013) and M. alternatus (9) . In insects, an OR unit consists of one conventional OR and one highly conserved, nonconventional Orco (Touhara and Vosshall, 2009).…”

“…Prior to this study, chemosensory gene families in the order Coleoptera had been only identified from the genome of the model insect T. castaneum (Tribolium Genome Sequencing Consortium, 2008), and from the antennal transcriptome of four non-model beetle species (I. typographus, D. ponderosae, A. planipennis and M. alternatus) (Andersson et al, 2013;Mamidala et al, 2013;Wang et al, 2014). Antennal transcriptome sequencing has also been conducted for the cerambycid beetle, Megacyllene caryae, from which only ORs were identified (Mitchell et al, 2012).…”

“…The order Coleoptera contains the largest number of insect species, most of which are agricultural pests that cause great economic losses. However, apart from T. castaneum, the first coleopteran species with a sequenced genome (Tribolium Genome Sequencing Consortium, 2008), chemosensory gene families have only been identified from a limited number of nonmodel coleopteran insects (the tree killing bark beetles Ips typographus and Dendroctonus ponderosae, the emerald ash borer Agrilus planipennis, and the Japanese sawyer beetle Monochamus alternatus (Andersson et al, 2013;Mamidala et al, 2013;Wang et al, 2014). Studies examining a wider range of species will further our understanding of the chemosensory genes involved in olfactory signal pathways in this important insect guild.…”

Sensory genes identification with head transcriptome of the migratory armyworm, Mythimna separata

“…Lepidopteran SNMPs contain two conserved groups of SNMP1 and SNMP2101105. While more than two SNMPs has been reported in coleopteran, lepidopteran and dipteran species1196106107. In the moth, SNMP1 was primarily expressed in antennae and SNMP2 was abundant expressed in antennae as well as in legs18.…”

Glutathione-S-Transferases in the Olfactory Organ of the Noctuid Moth Spodoptera littoralis, Diversity and Conservation of Chemosensory Clades

“…However, the expression of GSTs as well as their activities have been also highlighted in the olfactory organs of several insect species. Antennal expressed GSTs have been indeed identified in various moth species, such as Manduca sexta (Rogers et al, 1999), Helicoverpa armigera (Wang et al, 2004), Amyelois transitella (Leal et al, 2009), Bombyx mori (Tan et al, 2014), Chilo suppressalis (Liu et al, 2015a), Epiphyas postvittana (Corcoran et al, 2015), Cnaphalocris medinalis (Liu et al, 2015b), and Cydia pomonella (Huang et al, 2017), but also in the fruit fly Drosophila melanogaster (Younus et al, 2014) or in the beetles Agrilus planipennis (Mamidala et al, 2013), Dendroctonus valens (Gu et al, 2015), and Phyllotreta striolata (Wu et al, 2016). This particular localization led to the hypothesis of a possible dual function of GSTs in antennae where, besides their original implication in xenobiotic metabolism, they could play a role in the signal termination and in odorant clearance, as Odorant-Degrading Enzymes (ODEs, Vogt and Riddiford, 1981; Chertemps, 2017).…”