Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Liu, Nai Yong ^a,b   Xu, Wei ^a   Papanicolaou, Alexie ^a   Dong, Shuang Lin ^b   Anderson, Alisha ^a  

^a CSIRO   (Australia)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Expression profile; Gustatory receptor; Helicoverpa armigera; Ionotropic receptor; Olfactory receptor

Indexed keywords

IONOTROPIC RECEPTOR; PHEROMONE RECEPTOR; TRANSCRIPTOME; INSECT PROTEIN; OLFACTORY RECEPTOR; PROTEIN BINDING; RNA;

ADULT; AMINO ACID SEQUENCE; ANIMAL TISSUE; ANTENNA (ORGAN); ARTICLE; CONTROLLED STUDY; FAT BODY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC VARIABILITY; HARMIR2 GENE; HARMIR7D.1 GENE; HARMIR7D.2 GENE; HARMIR7D.3 GENE; HARMOR51 GENE; HELICOVERPA ARMIGERA; LARVA; MALE; MATING; MOUTH; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY RECEPTOR; PHYLOGENETIC TREE; PHYLOGENY; RNA SEQUENCE; TASTE BUD; ANIMAL; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MOTH; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

HELICOVERPA ARMIGERA; HEXAPODA;

AMINO ACID SEQUENCE; ANIMALS; CLUSTER ANALYSIS; FEMALE; INSECT PROTEINS; LARVA; MALE; MOLECULAR SEQUENCE DATA; MOTHS; PHYLOGENY; PROTEIN BINDING; RECEPTORS, IONOTROPIC GLUTAMATE; RECEPTORS, ODORANT; RECEPTORS, PHEROMONE; RNA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84904082275     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-597     Document Type: Article

References (54)

1. Leal WS. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 2013, 58:373-391.
2. Syed Z, Leal WS. Maxillary palps are broad spectrum odorant detectors in Culex quinquefasciatus. Chem Senses 2007, 32(8):727-738.
3. Keil TA. Reconstruction and morphometry of silkmoth olfactory hairs: A comparative study of sensilla trichodea on the antennae of male Antheraea polyphemus and Antheraea pernyi (Insecta, Lepidoptera). Zoomorphology 1984, 104(3):147-156.
4. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 1999, 22(2):327-338.
5. Clyne PJ, Warr CG, Carlson JR. Candidate taste receptors in Drosophila. Science 2000, 287(5459):1830-1834.
6. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 2009, 136(1):149-162.
7. Tunstall NE, Warr CG. Chemical communication in insects: the peripheral odour coding system of Drosophila melanogaster. Adv Exp Med Biol 2012, 739:59-77.
8. Spehr M, Munger SD. Olfactory receptors: G protein-coupled receptors and beyond. J Neurochem 2009, 109(6):1570-1583.
9. Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 2007, 445(7123):86-90.
10. Slone J, Daniels J, Amrein H. Sugar receptors in Drosophila. Curr Biol 2007, 17(20):1809-1816.
11. Sato K, Tanaka K, Touhara K. Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci U S A 2011, 108(28):11680-11685.
12. Lee Y, Moon SJ, Montell C. Multiple gustatory receptors required for the caffeine response in Drosophila. Proc Natl Acad Sci U S A 2009, 106(11):4495-4500.
13. Wada-Katsumata A, Silverman J, Schal C. Changes in Taste Neurons Support the Emergence of an Adaptive Behavior in Cockroaches. Science 2013, 340(6135):972-975.
14. Zhang HJ, Anderson AR, Trowell SC, Luo AR, Xiang ZH, Xia QY. Topological and functional characterization of an insect gustatory receptor. PLoS One 2011, 6(8):e24111.
15. Xu W, Zhang HJ, Anderson A. A sugar gustatory receptor identified from the foregut of cotton bollworm Helicoverpa armigera. J Chem Ecol 2012, 38(12):1513-1520.
16. Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 2010, 6(8):e1001064.
17. Liu Y, Gu S, Zhang Y, Guo Y, Wang G. Candidate olfaction genes identified within the Helicoverpa armigera antennal transcriptome. PLoS One 2012, 7(10):e48260.
18. Liu Y, Liu C, Lin K, Wang G. Functional specificity of sex pheromone receptors in the cotton bollworm Helicoverpa armigera. PLoS One 2013, 8(4):e62094.
19. Wang G, Vasquez GM, Schal C, Zwiebel LJ, Gould F. Functional characterization of pheromone receptors in the tobacco budworm Heliothis virescens. Insect Mol Biol 2011, 20(1):125-133.
20. Grosse-Wilde E, Gohl T, Bouche E, Breer H, Krieger J. Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur J Neurosci 2007, 25(8):2364-2373.
21. Mitsuno H, Sakurai T, Murai M, Yasuda T, Kugimiya S, Ozawa R, Toyohara H, Takabayashi J, Miyoshi H, Nishioka T. Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur J Neurosci 2008, 28(5):893-902.
22. Liu C, Liu Y, Walker WB, Dong S, Wang G. Identification and functional characterization of sex pheromone receptors in beet armyworm Spodoptera exigua (Hübner). Insect Biochem Mol Biol 2013, 43(8):747-754.
23. Montagne N, Chertemps T, Brigaud I, Francois A, Francois MC, de Fouchier A, Lucas P, Larsson MC, Jacquin-Joly E. Functional characterization of a sex pheromone receptor in the pest moth Spodoptera littoralis by heterologous expression in Drosophila. Eur J Neurosci 2012, 36(5):2588-2596.
24. Olivier V, Monsempes C, Francois MC, Poivet E, Jacquin-Joly E. Candidate chemosensory ionotropic receptors in a Lepidoptera. Insect Mol Biol 2011, 20(2):189-199.
25. Zhang YV, Ni J, Montell C. The Molecular Basis for Attractive Salt-Taste Coding in Drosophila. Science 2013, 340(6138):1334-1338.
26. Poivet E, Gallot A, Montagne N, Glaser N, Legeai F, Jacquin-Joly E. A comparison of the olfactory gene repertoires of adults and larvae in the noctuid moth Spodoptera littoralis. PLoS One 2013, 8(4):e60263.
27. Kiely A, Authier A, Kralicek AV, Warr CG, Newcomb RD. Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells. J Neurosci Methods 2007, 159(2):189-194.
28. Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, Touhara K. Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 2009, 19(11):881-890.
29. Briscoe AD, Macias-Muñoz A, Kozak KM, Walters JR, Yuan F, Jamie GA, Martin SH, Dasmahapatra KK, Ferguson LC, Mallet J, Jacquin-Joly E, Jiggins CD. Female Behaviour Drives Expression and Evolution of Gustatory Receptors in Butterflies. PLoS Genet 2013, 9(7):e1003620.
30. Rytz R, Croset V, Benton R. Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol 2013, 43(9):888-897.
31. Scott K, Brady R, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 2001, 104(5):661-673.
32. Akhurst RJ, James W, Bird LJ, Beard C. Resistance to the Cry1Ac delta-endotoxin of Bacillus thuringiensis in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 2003, 96(4):1290-1299.
33. 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. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protocols 2013, 8(8):1494-1512.
34. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9(4):357-359.
35. Roberts A, Pachter L. Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 2013, 10(1):71-73.
36. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140.
37. Wickham H. ggplot2: elegant graphics for data analysis 2009, New York: Springer.
38. Soding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005, 21(7):951-960.
39. Wanner KW, Robertson HM. The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol Biol 2008, 17(6):621-629.
40. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
41. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25(9):1189-1191.
42. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
43. Zhan S, Merlin C, Boore JL, Reppert SM. The monarch butterfly genome yields insights into long-distance migration. Cell 2011, 147(5):1171-1185.
44. Dasmahapatra KK, Walters JR, Briscoe AD, Davey JW, Whibley A, Nadeau NJ, Zimin AV, Hughes DST, Ferguson LC, Martin SH, Salazar C, Lewis JJ, Adler S, Ahn S-J, Baker DA, Baxter SW. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 2012, 487(7405):94-98.
45. Bengtsson JM, Trona F, Montagne N, Anfora G, Ignell R, Witzgall P, Jacquin-Joly E. Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS One 2012, 7(2):e31620.
46. Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS. Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci U S A 2011, 108(18):7449-7454.
47. Glaser N, Gallot A, Legeai F, Montagne N, Poivet E, Harry M, Calatayud PA, Jacquin-Joly E. Candidate chemosensory genes in the stemborer Sesamia nonagrioides. Int J Biol Sci 2013, 9(5):481-495.
48. Letunic I, Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 2011, 39(suppl 2):W475-W478.
49. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007, 23(1):127-128.
50. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13(11):2498-2504.
51. Morris JH, Apeltsin L, Newman AM, Baumbach J, Wittkop T, Su G, Bader GD, Ferrin TE. clusterMaker: a multi-algorithm clustering plugin for Cytoscape. BMC Bioinformatics 2011, 12:436.
52. Grosse-Wilde E, Svatos A, Krieger J. A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem Senses 2006, 31(6):547-555.
53. Anderson AR, Wanner KW, Trowell SC, Warr CG, Jaquin-Joly E, Zagatti P, Robertson H, Newcomb RD. Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem Mol Biol 2009, 39(3):189-197.
54. Jiang X-J, Guo H, Di C, Yu S, Zhu L, Huang L-Q, Wang C-Z. Sequence similarity and functional comparisons of pheromone receptor orthologs in two closely related Helicoverpa species. Insect Biochem Mol Biol 2014, 48:63-74.