Co-expression of six tightly clustered odorant receptor genes in the antenna of the malaria mosquito Anopheles gambiae

Karner, Tim; Kellner, Isabelle; Schultze, Anna; Breer, Heinz; Krieger, JÃ1⁄4rgen

doi:10.3389/fevo.2015.00026

Cited by 46 publications

(46 citation statements)

References 42 publications

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“…GRs share motifs with ORs in their transmembrane domains, and phylogenetically, they are suggested to predate the expansion of the insect ORs (Missbach et al, 2014;Robertson, Warr, & Carlson, 2003). Gustatory receptor neurons (GRNs) express a manifold subset of GRs; however, the design principles of taste are much less understood to date than olfaction (Karner, Kellner, Schultze, Breer, & Krieger, 2015;Koutroumpa, Kárpáti, Monsempes, Hill, & Hansson, 2014).…”

Section: Introductionmentioning

confidence: 99%

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

Wang

Pentzold

Kunert

et al. 2018

Ecology and Evolution

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Due to its fundamental role in shaping host selection behavior, we have analyzed the chemosensory repertoire of Chrysomela lapponica. This specialized leaf beetle evolved distinct populations which shifted from the ancestral host plant, willow (Salix sp., Salicaceae), to birch (Betula rotundifolia, Betulaceae). We identified 114 chemosensory candidate genes in adult C. lapponica: 41 olfactory receptors (ORs), eight gustatory receptors, 17 ionotropic receptors, four sensory neuron membrane proteins, 32 odorant binding proteins (OBPs), and 12 chemosensory proteins (CSP) by RNA‐seq. Differential expression analyses in the antennae revealed significant upregulation of one minus‐C OBP (Clap OBP27) and one CSP (Clap CSP12) in the willow feeders. In contrast, one OR (Clap OR17), four minus‐C OBPs (Clap OBP02, 07, 13, 20), and one plus‐C OBP (Clap OBP32) were significantly upregulated in birch feeders. The differential expression pattern in the legs was more complex. To narrow down putative ligands acting as cues for host discrimination, the relative abundance and diversity of volatiles of the two host plant species were analyzed. In addition to salicylaldehyde (willow‐specific), both plant species differed mainly in their emission rate of terpenoids such as (E,E)‐α‐farnesene (high in willow) or 4,8‐dimethylnona‐1,3,7‐triene (high in birch). Qualitatively, the volatiles were similar between willow and birch leaves constituting an “olfactory bridge” for the beetles. Subsequent structural modeling of the three most differentially expressed OBPs and docking studies using 22 host volatiles indicated that ligands bind with varying affinity. We suggest that the evolution of particularly minus‐C OBPs and ORs in C. lapponica facilitated its host plant shift via chemosensation of the phytochemicals from birch as novel host plant.

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Section: Introductionmentioning

confidence: 99%

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

Wang

Pentzold

Kunert

et al. 2018

Ecology and Evolution

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“…Selection drives the evolution of genes that facilitate host and mate finding, whereas behaviorally redundant OR genes are no longer expressed (Sánchez-Gracia et al, 2009;Hansson and Stensmyr, 2011;Suh et al, 2014;Andersson et al, 2015). Consequently, the insect OR repertoire is expected to be tuned to odor cues of ecological relevance, as indicated in the functional comparison between the OR repertoire of the vinegar fly, Drosophila melanogaster, and the malaria mosquito Anopheles gambiae, which shows little overlap (Hill et al, 2002;Carey et al, 2010;Suh et al, 2014;Karner et al, 2015). Orthologous ORs are of particular interest since may be tuned to odorants that are behaviorally and ecologically relevant across species (Bohbot et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

A Conserved Odorant Receptor Detects the Same 1-Indanone Analogs in a Tortricid and a Noctuid Moth

et al. 2015

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Odorant receptors (ORs) interface animals with airborne chemical signals. They are under strong selection pressure and are therefore highly divergent in different taxa. Yet, some OR orthologs are highly conserved. These ORs may be tuned to odorants of broad importance, across species boundaries. Two widely distributed lepidopteran herbivores, codling moth Cydia pomonella (Tortricidae) feeding in apples and pears, and the African cotton leafworm Spodoptera littoralis (Noctuidae), a moth feeding on foliage of a wide range of herbaceous plants, both express a receptor ortholog, OR19, which shares 58% amino acid identity and 69% amino acid similarity. Following heterologous expression in the empty neuron system of Drosophila melanogaster, we show by single sensillum recordings that CpomOR19 and SlitOR19 show similar affinity to several substituted indanes. Tests with a series of compounds structurally related to 1-indanone show that 2-methyl-1-indanone, 2-ethyl-1-indanone, 3-methyl-1-indanone, and 1-indanone elicit a strong response from both ORs. A keto group in position 1 is essential for biological activity and so are both rings of the indane skeleton. However, there is an important difference in steric complementary of the indane rings and the receptor. Methyl substituents on the benzene ring largely suppressed the response. On the other hand, alkyl substituents at position 2 and 3 of the five-membered ring increased the response indicating a higher complementarity with the receptor cavity, in both CpomOR19 and SlitOR19. Our results demonstrate a conserved function of an odorant receptor in two moths that are phylogenetically and ecologically distant. It is conceivable that a conserved OR is tuned to signals that are relevant for both species, although their ecological roles are yet unknown. Our finding demonstrates that functional characterization of ORs leads to the discovery of novel semiochemicals that have not yet been found through chemical analysis of odorants from insects and their associated host plants.

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“…In Drosophila melanogaster , six sugar receptor genes in the gustatory receptor 64 ( Gr64 ) cluster are transcribed as a polycistronic transcript (Dahanukar et al ., ; Slone et al ., ; Jiao et al ., ). A case with features similar to the Gr64 cluster was found in the OR genes in A. gambiae (Karner et al ., ). In our study, the six MmedOR genes within the same cluster were transcribed as single mRNAs, and a bicistronic mRNA was only detected with a faint PCR band in two adjacent OR genes ( OR124 and OR98 ).…”

Section: Discussionmentioning

confidence: 98%

“…Co‐expression of multiple receptor types has been observed in the insect olfactory system. Many of the receptor pairs that are co‐expressed in sensory neurones appear to be the result of the transcription of multiple genes as polycistronic mRNA (Ray et al ., ; Karner et al ., ). Although the bicistronic mRNA for MmedOR124 and MmedOR98 was detected by RT‐PCR, there was no co‐expression between them in ORNs of female antennae.…”

Section: Discussionmentioning

confidence: 98%

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Gene structure and expression characteristic of a novel odorant receptor gene cluster in the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidae)

Wang

Shan

Zheng

et al. 2017

Insect Molecular Biology

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Odorant receptors (ORs) expressed in the antennae of parasitoid wasps are responsible for detection of various lipophilic airborne molecules. In the present study, 107 novel OR genes were identified from Microplitis mediator antennal transcriptome data. Phylogenetic analysis of the set of OR genes from M. mediator and Microplitis demolitor revealed that M. mediator OR (MmedOR) genes can be classified into different subfamilies, and the majority of MmedORs in each subfamily shared high sequence identities and clear orthologous relationships to M. demolitor ORs. Within a subfamily, six MmedOR genes, MmedOR98, 124, 125, 126, 131 and 155, shared a similar gene structure and were tightly linked in the genome. To evaluate whether the clustered MmedOR genes share common regulatory features, the transcription profile and expression characteristics of the six closely related OR genes were investigated in M. mediator. Rapid amplification of cDNA ends-PCR experiments revealed that the OR genes within the cluster were transcribed as single mRNAs, and a bicistronic mRNA for two adjacent genes (MmedOR124 and MmedOR98) was also detected in female antennae by reverse transcription PCR. In situ hybridization experiments indicated that each OR gene within the cluster was expressed in a different number of cells. Moreover, there was no co-expression of the two highly related OR genes, MmedOR124 and MmedOR98, which appeared to be individually expressed in a distinct population of neurons. Overall, there were distinct expression profiles of closely related MmedOR genes from the same cluster in M. mediator. These data provide a basic understanding of the olfactory coding in parasitoid wasps.

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Co-expression of six tightly clustered odorant receptor genes in the antenna of the malaria mosquito Anopheles gambiae

Abstract: Co-expression of six tightly clustered odorant receptor genes in the antenna of the malaria mosquito Anopheles gambiae.

Cited by 46 publications

References 42 publications

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

A subset of chemosensory genes differs between two populations of a specialized leaf beetle after host plant shift

A Conserved Odorant Receptor Detects the Same 1-Indanone Analogs in a Tortricid and a Noctuid Moth

Gene structure and expression characteristic of a novel odorant receptor gene cluster in the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidae)

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