The ionotropic receptor gene family in Lepidoptera and Trichoptera: Annotation, evolutionary and functional perspectives

Yin, Ning-Na; Nuo, Shu-Mei; Xiao, Haiyan; Zhao, Yujie; Zhu, Jia‐Ying; Liu, Nai-Yong

doi:10.1016/j.ygeno.2020.09.056

Cited by 28 publications

(37 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For the identification of chemosensory genes in D. abietella, two de novo transcriptomes were used, i.e., the transcript transcriptome and the unigene transcriptome. First, a homologybased search with TBLASTN, implemented in Geneious v10.1.3 1 , was employed to identify genes from the transcriptomes, with queries of chemosensory genes from D. abietella, Galleria mellonella, Ostrinia furnacalis, and Bombyx mori (Zhang T. et al, 2015;Guo et al, 2017;Liu et al, 2018;Zhao et al, 2019;Jiang et al, 2021;Xing et al, 2021;Yin et al, 2021). In search of each query, we set e-value and maximum blast hits as 1e −5 and 20, respectively.…”

Section: Gene Identification and Comparisonmentioning

confidence: 99%

“…Difference in the repertoire sizes of antennae-expressed OBPs, ORs, or IRs were possibly attributed to the following reasons: (1) sequencing depth as discussed above; (2) sequencing sexes such as S. nonagrioides, and (3) sequencing platforms or techniques (Figure 1 and Supplementary Table 1). In addition, it was also possible that a wide diversity of host plants drove the evolution of olfactory genes (Pelosi et al, 2018;Robertson, 2019;Auer et al, 2020;Yin et al, 2021). Although lepidopteran GRs, except for CO 2 -sensing receptors, were mainly expressed in gustatory-related tissues like proboscises and legs, they were indeed present in the antennae from D. abietella and other lepidopterans, including sugar, GR43a-like and some bitter receptors (Xu et al, 2016;Guo et al, 2017;Li G. C. et al, 2021).…”

Section: Antennae-expressed Chemosensory Genes In Adult Mothsmentioning

confidence: 99%

“…With the discovery of three chemosensory receptor gene families in D. melanogaster (Clyne et al, 1999(Clyne et al, , 2000Benton et al, 2009), to date a large number of ORs, GRs and IRs have been identified and characterized in Diptera (Nozawa and Nei, 2007;Croset et al, 2010), Lepidoptera (Engsontia et al, 2014;Xu, 2020;Yin et al, 2021), Coleoptera (Andersson et al, 2019;Mitchell et al, 2020;Mitchell and Andersson, 2021), Hemiptera (Smadja et al, 2009;, and Hymenoptera (Ferguson et al, 2021;Obiero et al, 2021). In insects, ORs are expressed in sensilla basiconica and sensilla trichoidea separately responsible for general odorants (i.e., general ORs) and sex pheromones (i.e., pheromone receptors, PRs) (Krieger et al, 2009;de Fouchier et al, 2017;Guo et al, 2020), while olfactory sensory neurons expressing IRs are distributed in sensilla coeloconica sensitive to amines, acids, alcohols and aldehydes (Yao et al, 2005;Silbering et al, 2011;Rytz et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Transcriptome Analysis and Characterization of Chemosensory Genes in the Forest Pest, Dioryctria abietella (Lepidoptera: Pyralidae)

Wang

Chun

et al. 2021

Front. Ecol. Evol.

Self Cite

View full text Add to dashboard Cite

In Lepidoptera, RNA sequencing has become a useful tool in identifying chemosensory genes from antennal transcriptomes, but little attention is paid to non-antennal tissues. Though the antennae are primarily responsible for olfaction, studies have found that a certain number of chemosensory genes are exclusively or highly expressed in the non-antennal tissues, such as proboscises, legs and abdomens. In this study, we report a global transcriptome of 16 tissues from Dioryctria abietella, including chemosensory and non-chemosensory tissues. Through Illumina sequencing, totally 952,658,466 clean reads were generated, summing to 142.90 gigabases of data. Based on the transcriptome, 235 chemosensory-related genes were identified, comprising 42 odorant binding proteins (OBPs), 23 chemosensory proteins (CSPs), 75 odorant receptors (ORs), 62 gustatory receptors (GRs), 30 ionotropic receptors (IRs), and 3 sensory neuron membrane proteins (SNMPs). Compared to a previous study in this species, 140 novel genes were found. A transcriptome-wide analysis combined with PCR results revealed that except for GRs, the majority of other five chemosensory gene families in Lepidoptera were expressed in the antennae, including 160 chemosensory genes in D. abietella. Using phylogenetic and expression profiling analyses, members of the six chemosensory gene repertoires were characterized, in which 11 DabiORs were candidates for detecting female sex pheromones in D. abietella, and DabiOR23 may be involved in the sensing of plant-derived phenylacetaldehyde. Intriguingly, more than half of the genes were detected in the proboscises, and one fourth of the genes were found to have the expression in the legs. Our study not only greatly extends and improves the description of chemosensory genes in D. abietella, but also identifies potential molecular targets involved in olfaction, gustation and non-chemosensory functions for control of this pest.

show abstract

Section: Gene Identification and Comparisonmentioning

confidence: 99%

Section: Antennae-expressed Chemosensory Genes In Adult Mothsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Transcriptome Analysis and Characterization of Chemosensory Genes in the Forest Pest, Dioryctria abietella (Lepidoptera: Pyralidae)

Wang

Chun

et al. 2021

Front. Ecol. Evol.

Self Cite

View full text Add to dashboard Cite

show abstract

“…IRs are conserved across protostome species and bioinformatic analyses of IR genes have been performed in many species (Benton et al, 2009;Croset et al, 2010;Bengtsson et al, 2012;Glaser et al, 2013;Poivet et al, 2013;Rytz et al, 2013;Cao et al, 2014;Groh-Lunow et al, 2014;Liu et al, 2014Liu et al, , 2017Liu et al, , 2018Missbach et al, 2014;Ahmed et al, 2016;Dippel et al, 2016;Macharia et al, 2016;van Schooten et al, 2016;Cicconardi et al, 2017;Latorre-Estivalis et al, 2017;Yang et al, 2017Yang et al, , 2020Zbinden et al, 2017;Harrison et al, 2018;Kozma et al, 2018;Matthews et al, 2018;Robertson et al, 2018Robertson et al, , 2019Rojas et al, 2018;Andersson et al, 2019;Lei et al, 2019;Li et al, 2019;Ma et al, 2019;Xu et al, 2019;Balart-García et al, 2020;Sun et al, 2020;Wu et al, 2020;Yin et al, 2020). However, the functional studies of IRs in non-model organisms are largely lacking.…”

Section: Discussionmentioning

confidence: 99%

The Structure and Function of Ionotropic Receptors in Drosophila

2021

Front. Mol. Neurosci.

View full text Add to dashboard Cite

Ionotropic receptors (IRs) are a highly divergent subfamily of ionotropic glutamate receptors (iGluR) and are conserved across Protostomia, a major branch of the animal kingdom that encompasses both Ecdysozoa and Lophothrochozoa. They are broadly expressed in peripheral sensory systems, concentrated in sensory dendrites, and function in chemosensation, thermosensation, and hygrosensation. As iGluRs, four IR subunits form a functional ion channel to detect environmental stimuli. Most IR receptors comprise individual stimulus-specific tuning receptors and one or two broadly expressed coreceptors. This review summarizes the discoveries of the structure of IR complexes and the expression and function of each IR, as well as discusses the future direction for IR studies.

show abstract

“…A number of the so-called Lepidoptera-specific IRs (LS-IRs) are absent in Drosophila and were originally identified in Lepidoptera (Olivier et al, 2011;Bengtsson et al, 2012;Poivet 2013;van Schooten et al, 2016;Liu et al, 2018;Zhu et al, 2018a). Despite the name, some of them are also present in Trichoptera and mosquitos with overall high support values, although in some cases the orthology remains somewhat ambiguous (Yuvaraj et al, 2018;Yin et al, 2020). The LS-IRs do not represent a single monophyletic IR subfamily, because they are scattered across the phylogenetic tree, with some (IR1, IR75p, IR75q and IR87a) located within the A-IR while others (IR7d, IR100b-j and IR143) nested within the D-IR clade, and also include a putative pseudogene (IR2) (Liu et al, 2018;Zhu et al, 2018a).…”

Section: Introductionmentioning

confidence: 99%

Ionotropic receptors in the turnip mothAgrotis segetumrespond to repellent medium-chain fatty acids

Hou

Zhang

Powell

et al. 2021

Preprint

View full text Add to dashboard Cite

In insects, airborne chemical signals are mainly detected by two receptor families, odorant receptors (ORs) and ionotropic receptors (IRs). Functions of ORs have been intensively investigated in Diptera and Lepidoptera, while the functions and evolution of the more ancient IR family remain largely unexplored beyond Diptera. Here, we identified a repertoire of 26 IRs from transcriptomes of female and male antennae, and ovipositors in the moth Agrotis segetum. We observed that a large clade formed by IR75p and IR75q expansions is closely related to the acid-sensing IRs identified in Diptera. We functionally assayed each of the five AsegIRs from this clade using Xenopus oocytes and found that two receptors responded to the tested ligands. AsegIR75p.1 responded to several compounds but hexanoic acid was revealed to be the primary ligand, and AsegIR75q.2 responded primarily to octanoic acid, and less so to nonanoic acid. It has been reported that the C6-C10 medium-chain fatty acids repel various insects including many drosophilids and mosquitos. Our GC-EAD recordings showed that C6-C10 medium-chain fatty acids elicited antennal responses of both sexes of A. segetum, while only octanoic acid had repellent effect to the moths in a behavioural assay. In addition, using fluorescence in situ hybridization, we demonstrated that AsegIR75q.2 and its co-receptor AsegIR8a are not located in coeloconic sensilla as found in Drosophila, but in basiconic or trichoid sensilla. These functional data in combination with our phylogenetic analysis suggest that subfunctionalization of the acid-sensing IRs after gene duplication plays an important role in the evolution of ligand specificities of the acid-sensing IRs in Lepidoptera.

show abstract

The ionotropic receptor gene family in Lepidoptera and Trichoptera: Annotation, evolutionary and functional perspectives

Cited by 28 publications

References 38 publications

Transcriptome Analysis and Characterization of Chemosensory Genes in the Forest Pest, Dioryctria abietella (Lepidoptera: Pyralidae)

Transcriptome Analysis and Characterization of Chemosensory Genes in the Forest Pest, Dioryctria abietella (Lepidoptera: Pyralidae)

The Structure and Function of Ionotropic Receptors in Drosophila

Ionotropic receptors in the turnip mothAgrotis segetumrespond to repellent medium-chain fatty acids

Contact Info

Product

Resources

About