Antennal ionotropic receptors IR64a1 and IR64a2 of the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidate) collaboratively perceive habitat and host cues

Shan, Shuang; Wang, Shan-Ning; Song, Xuan; Khashaveh, Adel; Lu, Ziyue; Dhiloo, Khalid Hussain; Li, Ruijun; Gao, Xiwu; Zhang, Yongjun

doi:10.1016/j.ibmb.2019.103204

Cited by 22 publications

(26 citation statements)

References 76 publications

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“…Although this major gene family spans across protostomes [ 29 , 40 ], the functional information of IRs beyond dipterans is still limited, restricting our knowledge concerning the evolution and specialization of this ancient gene family. To our knowledge, only two IRs from the parasitoid wasp Microplitis mediator have been functionally investigated [ 41 ]. The second largest insect order, Lepidoptera, rely on their remarkable olfactory abilities to sense the external environment.…”

Section: Introductionmentioning

confidence: 99%

Ionotropic receptors in the turnip moth Agrotis segetum respond to repellent medium-chain fatty acids

et al. 2022

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Background 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. Results 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.1 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. We show that the 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 behavioral assay. In addition, using fluorescence in situ hybridization, we demonstrated that the five IRs and their co-receptor AsegIR8a are not located in coeloconic sensilla as found in Drosophila, but in basiconic or trichoid sensilla. Conclusions Our results significantly expand the current knowledge of the insect IR family. Based on the functional data in combination with phylogenetic analysis, we propose that subfunctionalization after gene duplication plays an important role in the evolution of ligand specificities of the acid-sensing IRs in Lepidoptera.

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Section: Introductionmentioning

confidence: 99%

Ionotropic receptors in the turnip moth Agrotis segetum respond to repellent medium-chain fatty acids

et al. 2022

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“…The sensitive olfactory systems of parasitoid wasps play an important role in host location. In our previous work, we identified large sets of chemosensory genes, including 169 odorant receptors (ORs), 17 ionotropic receptors (IRs), two gustatory receptors (GRs), two SNMPs, 20 OBPs, three chemosensory proteins (CSPs) and two Niemann‐Pick type C2 proteins in the antennae of M. mediator , and a number of specific and olfactory‐associated proteins have been functionally characterized in this wasp (Zhang et al ., 2009, 2011; Li et al ., 2014; Ma et al ., 2014; Wang et al ., 2015, 2016a, 2017b, 2018; Peng et al ., 2017; Zheng et al ., 2018; Shan et al ., 2019a,b). Nonetheless, little is known about the roles of miRNAs in chemoreception in M. mediator and other hymenopteran wasps.…”

Section: Introductionmentioning

confidence: 99%

Characterization and target gene analysis of microRNAs in the antennae of the parasitoid wasp Microplitis mediator

et al. 2020

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MicroRNAs (miRNAs), a class of non-coding single-strand RNA molecules encoded by endogenous genes, are about 21-24 nucleotides long and are involved in the post-transcriptional regulation of gene expression in plants and animals. Generally, the types and quantities of miRNAs in the different tissues of an organism are diverse, and these divergences may be related to their specific functions. Here we have identified 296 known miRNAs and 46 novel miRNAs in the antennae of the parasitoid wasp Microplitis mediator by high-throughput sequencing. Thirty-three miRNAs were predicted to target olfactory-associated genes, including odorant binding proteins (OBPs), chemosensory proteins, odorant receptors (ORs), ionotropic receptors (IRs) and gustatory receptors. Among these, 17 miRNAs were significantly highly expressed in the antennae, four miRNAs were highly expressed both in the antennae and head or wings, while the remaining 12 miRNAs were mainly expressed in the head, thorax, abdomen, legs and wings. Notably, miR-9a-5p and miR-2525-3p were highly expressed in male antennae, whereas miR-1000-5p and novel-miR-13 were enriched in female antennae. The 17 miR-NAs highly expressed in antennae are likely to be associated with olfaction, and were predicted to target one OBP (targeted by miR-3751-3p), one IR (targeted by miR-7-5p) and 14 ORs (targeted by 15 miRNAs including miR-6-3p, miR-9a-5p, miR-9b-5p, miR-29-5p, miR-71-5p, miR-275-3p, miR-1000-5p, miR-1000-3p, miR-2525-3p, miR-6012-3p, miR-9719-3p, novel-miR-10, novel-miR-13, novel-miR-14 and novel-miR-28). These candidate olfactory-associated miRNAs are all likely to be involved in chemoreception through the regulation of chemosensory gene expression in the antennae of M. mediator.

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“…This number is, however, lower compared to those identified from the genomes of the other species (e.g., 45 in S. litura , 39 in H. armigera and 66 in D. melanogaster ; Croset et al, 2010; Zhu et al, 2018a; Liu et al, 2018), which include the IRs expressed in the other body parts and pseudogenes. From the phylogenetic analysis, the IR75p/q expansions together with IR1.1 and 1.2 clades were grouped into a large cluster in which some receptors including IR31a, IR64a and IR75a,b,c have been reported as acid-sensors in D. melanogaster ; IR64a.1 and IR64a.2 in the parasitoid wasp M. mediator ; and IR75k in the mosquito A. gambiae (Abuin et al, 2011; Silbering et al, 2011; Rytz et al, 2013; Ai et al, 2013; Pitts et al, 2017; Shan et al, 2019). This suggested that the receptors within the IR75p/q expansions may also be involved in acid detection.…”

Section: Discussionmentioning

confidence: 99%

“…Although this major gene family spans across protostomes (Croset et al, 2010;Eyun et al, 2017), the functional information of IRs beyond dipterans is still limited, restricting our knowledge concerning the evolution and specialization of this ancient gene family. To our knowledge, only two IRs from the parasitoid wasp Microplitis mediator have been functionally investigated (Shan et al, 2019). The second largest insect order, Lepidoptera, rely on their remarkable olfactory abilities to sense the external environment.…”

Section: Introductionmentioning

confidence: 99%

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

Hou

Zhang

Powell

et al. 2021

Preprint

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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

Antennal ionotropic receptors IR64a1 and IR64a2 of the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidate) collaboratively perceive habitat and host cues

Cited by 22 publications

References 76 publications

Ionotropic receptors in the turnip moth Agrotis segetum respond to repellent medium-chain fatty acids

Ionotropic receptors in the turnip moth Agrotis segetum respond to repellent medium-chain fatty acids

Characterization and target gene analysis of microRNAs in the antennae of the parasitoid wasp Microplitis mediator

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

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