Abstract
Carbon dioxide (CO2) is important in insect ecology, eliciting a range of behaviours across different species. Interestingly, the numbers of CO2 gustatory receptors (GRs) vary among insect species. In the model organism Drosophila melanogaster, two GRs (DmelGR21a and DmelGR63a) have been shown to detect CO2. In the butterfly, moth, beetle and mosquito species studied so far, three CO2 GR genes have been identified, while in tsetse flies, four CO2 GR genes have been identified. In other species including honeybees, pea aphids, ants, locusts and wasps, no CO2 GR genes have been identified from the genome. These genomic differences may suggest different mechanisms for CO2 detection exist in different insects but, with the exception of Drosophila and mosquitoes, limited attention has been paid to the CO2 GRs in insects. Here, we cloned three putative CO2 GR genes from the cotton bollworm Helicoverpa armigera and performed phylogenetic and expression analysis. All three H. armigera CO2 GRs (HarmGR1, HarmGR2 and HarmGR3) are specifically expressed in labial palps, the CO2-sensing tissue of this moth. HarmGR3 is significantly activated by NaHCO3 when expressed in insect Sf9 cells but HarmGR1 and HarmGR2 are not. This is the first report characterizing the function of lepidopteran CO2 receptors, which contributes to our general understanding of the molecular mechanisms of insect CO2 gustatory receptors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ai M, Blais S, Park JY, Min S, Neubert TA, Suh GS (2013) Ionotropic glutamate receptors IR64a and IR8a form a functional odorant receptor complex in vivo in Drosophila. J Neurosci 33:10741–10749. doi:10.1523/JNEUROSCI. 5419-12.2013
Anderson AR, Wanner KW, Trowell SC, Warr CG, Jaquin-Joly E, Zagatti P, Robertson H, Newcomb RD (2009) Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem Mol Biol 39:189–197. doi:10.1016/j.ibmb.2008.11.002
Bogner F, Boppre M, Ernst KD, Boeckh J (1986) CO2 sensitive receptors on labial palps of Rhodogastria moths (Lepidoptera: Arctiidae): physiology, fine structure and central projection. J Comp Physiol A 158:741–749
Briscoe AD, Macias-Munoz A, Kozak KM, Walters JR, Yuan F, Jamie GA, Martin SH, Dasmahapatra KK, Ferguson LC, Mallet J, Jacquin-Joly E, Jiggins CD (2013) Female behaviour drives expression and evolution of gustatory receptors in butterflies. PLoS Genet 9:e1003620. doi:10.1371/journal.pgen.1003620
Cayirlioglu P, Kadow IG, Zhan X, Okamura K, Suh GS, Gunning D, Lai EC, Zipursky SL (2008) Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems. Science 319:1256–1260. doi:10.1126/science.1149483
Cserzo M, Eisenhaber F, Eisenhaber B, Simon I (2002) On filtering false positive transmembrane protein predictions. Protein Eng 15:745–752
Dahanukar A, Foster K, van der Goes van Naters WM, Carlson JR (2001) A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci 4:1182–1186. doi:10.1038/nn765
Dahanukar A, Lei YT, Kwon JY, Carlson JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56:503–516
Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827–841
Erdelyan CN, Mahood TH, Bader TS, Whyard S (2012) Functional validation of the carbon dioxide receptor genes in Aedes aegypti mosquitoes using RNA interference. Insect Mol Biol 21:119–127. doi:10.1111/j.1365-2583.2011.01120.x
Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178. doi:10.1146/annurev.ento.53.103106.093402
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512. doi:10.1038/nprot.2013.084
Hartl M, Loschek LF, Stephan D, Siju KP, Knappmeyer C, Kadow IC (2011) A new Prospero and microRNA-279 pathway restricts CO2 receptor neuron formation. J Neurosci 31:15660–15673. doi:10.1523/JNEUROSCI. 2592-11.2011
Jiao Y, Moon SJ, Wang X, Ren Q, Montell C (2008) Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr Biol 18:1797–1801
Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445:86–90. doi:10.1038/nature05466
Juretic D, Lee B, Trinajstic N, Williams RW (1993) Conformational preference functions for predicting helices in membrane proteins. Biopolymers 33:255–273. doi:10.1002/bip.360330208
Kiely A, Authier A, Kralicek AV, Warr CG, Newcomb RD (2007) Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells. J Neurosci Methods 159:189–194. doi:10.1016/j.jneumeth.2006.07.005
Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. doi:10.1006/jmbi.2000.4315
Liu NY, Xu W, Papanicolaou A, Dong SL, Anderson A (2014) Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera. BMC Genomics 15:597. doi:10.1186/1471-2164-15-597
McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB (2014) Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156:1060–1071. doi:10.1016/j.cell.2013.12.044
Montell C (2013) Gustatory receptors: not just for good taste. Curr Biol 23:R929–R932. doi:10.1016/j.cub.2013.09.026
Moon SJ, Kottgen M, Jiao Y, Xu H, Montell C (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16:1812–1817
Obiero GF, Mireji PO, Nyanjom SR, Christoffels A, Robertson HM, Masiga DK (2014) Odorant and gustatory receptors in the tsetse fly Glossina morsitans morsitans. PLoS Negl Trop Dis 8:e2663. doi:10.1371/journal.pntd.0002663
Rasch C, Rembold H (1994) Carbon-dioxide—highly attractive signal for larvae of Helicoverpa armigera. Naturwissenschaften 81:228–229
Robertson HM, Kent LB (2009) Evolution of the gene lineage encoding the carbon dioxide receptor in insects. J Insect Sci 9:1–14. doi:10.1673/031.009.1901
Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 101:16653–16658. doi:10.1073/pnas.0407596101
Sato K, Pellegrino M, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006. doi:10.1038/nature06850
Sato K, Tanaka K, Touhara K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci U S A 108:11680–11685
Savard J, Tautz D, Richards S, Weinstock GM, Gibbs RA, Werren JH, Tettelin H, Lercher MJ (2006) Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res 16:1334–1338. doi:10.1101/gr.5204306
Seeley TD (1974) Atmospheric carbon dioxide regulation in honey-bee (Apis mellifera) colonies. J Insect Physiol 20:2301–2305
Sharm HC (2001) Cotton bollworm/legume pod borer, Helicoverpa armigera (Hubner) (Noctuidae: Lepidoptera): biology and management. In: Crop protection compendium. Commonwealth Agricultural Bureau International Oxon, UK, 77
Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38:770–780. doi:10.1016/j.ibmb.2008.05.002
Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431:854–859. doi:10.1038/nature02980
Syed Z, Leal WS (2007) Maxillary palps are broad spectrum odorant detectors in Culex quinquefasciatus. Chem Senses 32:727–738. doi:10.1093/chemse/bjm040
Tauxe GM, MacWilliam D, Boyle SM, Guda T, Ray A (2013) Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell 155:1365–1379. doi:10.1016/j.cell.2013.11.013
Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, Chen Z, Childers CP, Glastad KM, Gokhale K, Gowin J, Gronenberg W, Hermansen RA, Hu H, Hunt BG, Huylmans AK, Khalil SM, Mitchell RD, Munoz-Torres MC, Mustard JA, Pan H, Reese JT, Scharf ME, Sun F, Vogel H, Xiao J, Yang W, Yang Z, Zhou J, Zhu J, Brent CS, Elsik CG, Goodisman MA, Liberles DA, Roe RM, Vargo EL, Vilcinskas A, Wang J, Bornberg-Bauer E, Korb J, Zhang G, Liebig J (2014) Molecular traces of alternative social organization in a termite genome. Nat Commun 5:3636. doi:10.1038/ncomms4636
Thom C, Guerenstein PG, Mechaber WL, Hildebrand JG (2004) Floral CO2 reveals flower profitability to moths. J Chem Ecol 30:1285–1288
Turner SL, Ray A (2009) Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461:277–281. doi:10.1038/nature08295
Viklund H, Elofsson A (2008) OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar. Bioinformatics 24:1662–1668. doi:10.1093/bioinformatics/btn221
Wasserman S, Salomon A, Frye MA (2013) Drosophila tracks carbon dioxide in flight. Curr Biol 23:301–306. doi:10.1016/j.cub.2012.12.038
Xu W, Zhang HJ, Anderson A (2012) A sugar gustatory receptor identified from the foregut of cotton bollworm Helicoverpa armigera. J Chem Ecol 38:1513–1520. doi:10.1007/s10886-012-0221-8
Zhang HJ, Anderson AR, Trowell SC, Luo AR, Xiang ZH, Xia QY (2011) Topological and functional characterization of an insect gustatory receptor. PLoS One 6:e24111. doi:10.1371/journal.pone.0024111
Zhao XC, Tang QB, Berg BG, Liu Y, Wang YR, Yan FM, Wang GR (2013) Fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of Helicoverpa armigera (Insecta). Cell Tissue Res 353:399–408. doi:10.1007/s00441-013-1657-z
Acknowledgments
We would like to thank all the members of Helicoverpa genome consortium for permission to use the genome and transcriptome sequences ahead of the publication. We also thank Olivia Leitch and Faisal Younus who provided critical feedback.
This work was supported by the Commonwealth Scientific and Industrial Research Organisation (CSIRO) Julius Award (R-00094-01-005) and the CSIRO Office of the Chief Executive (OCE) Postdoctoral Fellowship (R-01479-1).
Conflict of interest
The authors declare that they have no competing interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplement Table 1
The identifies (%) of insect CO2 GR amino acids inGR1 group (blue), GR2 group (green) and GR3 group (red).. (PPTX 91 kb)
Supplement Figure 1
The change in fluorescent intensity of a single Sf9 cell transfected withpIBV5-HarmGR1, 2 or 3 over the course of a calcium assay experiment. Mean pixel intensityfor this cell is plotted every 10 s. At the times indicated by arrows, 50 mM NaHCO3 and 2μMionomycin were added to the cell. (PPTX 54 kb)
Rights and permissions
About this article
Cite this article
Xu, W., Anderson, A. Carbon dioxide receptor genes in cotton bollworm Helicoverpa armigera . Sci Nat 102, 11 (2015). https://doi.org/10.1007/s00114-015-1260-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-015-1260-0