BMC Genomics | |
Genes involved in sex pheromone biosynthesis of Ephestia cautella, an important food storage pest, are determined by transcriptome sequencing | |
Arnab Pain4  Abdulrahman S. Aldawood2  Saleh A. Aldosari3  Koko D. Sutanto3  Sulieman Alfaifi3  Jernej Jakše1  Alan Soffan2  Binu Antony3  | |
[1] Agronomy Department, University of Ljubljana, Biotechnical Faculty, Ljubljana, SI-1000, Slovenia;Department of Plant Protection, King Saud University, EERU, Riyadh, Saudi Arabia;Department of Plant Protection, King Saud University, Chair of Date Palm Research, College of Food and Agricultural Sciences, Riyadh 11451, Saudi Arabia;BASE Division, KAUST, Thuwal, Jeddah 23955-6900, Saudi Arabia | |
关键词: Pheromone biosynthetic enzymes; Transcriptome; Pheromone gland; Pheromone; Ephestia; | |
Others : 1222414 DOI : 10.1186/s12864-015-1710-2 |
|
received in 2014-09-17, accepted in 2015-06-22, 发布年份 2015 | |
【 摘 要 】
Background
Insects use pheromones, chemical signals that underlie all animal behaviors, for communication and for attracting mates. Synthetic pheromones are widely used in pest control strategies because they are environmentally safe. The production of insect pheromones in transgenic plants, which could be more economical and effective in producing isomerically pure compounds, has recently been successfully demonstrated. This research requires information regarding the pheromone biosynthetic pathways and the characterization of pheromone biosynthetic enzymes (PBEs). We used Illumina sequencing to characterize the pheromone gland (PG) transcriptome of the Pyralid moth, Ephestia cautella, a destructive storage pest, to reveal putative candidate genes involved in pheromone biosynthesis, release, transport and degradation.
Results
We isolated the E. cautella pheromone compound as (Z,E)-9,12-tetradecadienyl acetate, and the major pheromone precursors 16:acyl, 14:acyl, E14-16:acyl, E12-14:acyl and Z9,E12-14:acyl. Based on the abundance of precursors, two possible pheromone biosynthetic pathways are proposed. Both pathways initiate from C16:acyl-CoA, with one involving ∆14 and ∆9 desaturation to generate Z9,E12-14:acyl, and the other involving the chain shortening of C16:acyl-CoA to C14:acyl-CoA, followed by ∆12 and ∆9 desaturation to generate Z9,E12-14:acyl-CoA. Then, a final reduction and acetylation generates Z9,E12-14:OAc. Illumina sequencing yielded 83,792 transcripts, and we obtained a PG transcriptome of ~49.5 Mb. A total of 191 PBE transcripts, which included pheromone biosynthesis activating neuropeptides, fatty acid transport proteins, acetyl-CoA carboxylases, fatty acid synthases, desaturases, β-oxidation enzymes, fatty acyl-CoA reductases (FARs) and fatty acetyltransferases (FATs), were selected from the dataset. A comparison of the E. cautella transcriptome data with three other Lepidoptera PG datasets revealed that 45 % of the sequences were shared. Phylogenetic trees were constructed for desaturases, FARs and FATs, and transcripts that clustered with the ∆14, ∆12 and ∆9 desaturases, PG-specific FARs and potential candidate FATs, respectively, were identified. Transcripts encoding putative pheromone degrading enzymes, and candidate pheromone carrier and receptor proteins expressed in the E. cautella PG, were also identified.
Conclusions
Our study provides important background information on the enzymes involved in pheromone biosynthesis. This information will be useful for the in vitro production of E. cautella sex pheromones and may provide potential targets for disrupting the pheromone-based communication system of E. cautella to prevent infestations.
【 授权许可】
2015 Antony et al.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150821020731706.pdf | 2259KB | download | |
Fig. 11. | 94KB | Image | download |
Fig. 10. | 109KB | Image | download |
Fig. 9. | 64KB | Image | download |
Fig. 8. | 120KB | Image | download |
Fig. 7. | 87KB | Image | download |
Fig. 6. | 43KB | Image | download |
Fig. 5. | 32KB | Image | download |
Fig. 4. | 76KB | Image | download |
Fig. 3. | 34KB | Image | download |
Fig. 2. | 38KB | Image | download |
Fig. 1. | 15KB | Image | download |
【 图 表 】
Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.
Fig. 11.
【 参考文献 】
- [1]El-Sayed A. The pherobase: database of insect pheromones and semiochemicals. http://www.pherobase.com. Accessed 15 Aug 2014.
- [2]Wyatt TD. Pheromones and animal behavior. Chemical signals and signatures. Cambridge University Press, Cambridge; 2014.
- [3]Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ. Insect pheromones—an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol. 1999; 29:481-514.
- [4]Jurenka R. Insect pheromone biosynthesis. Top Curr Chem. 2004; 239:97-132.
- [5]Rafaeli A. Mechanisms involved in the control of pheromone production in female moths: recent developments. Entomol Exp Appl. 2005;115(1):7–15.
- [6]Roelofs WL, Rooney AP. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc Natl Acad Sci. 2003; 100 Suppl 2:14599.
- [7]Cardé RT, Haynes KF. Structure of the pheromone communication channel in moths. In: Advances in insect chemical ecology Cambridge (UK). Cardé RT, Millar JG, editors. Cambridge University Press, Cambridge; 2004: p.283-332.
- [8]Matsumoto S, Hull J, Ohnishi A, Moto K, Fónagy A. Molecular mechanisms underlying sex pheromone production in the silkmoth, Bombyx mori: characterization of the molecular components involved in bombykol biosynthesis. J Insect Physiol. 2007; 53(8):752-9.
- [9]Matsumoto S, Ohnishi A, Lee JM, Hull JJ. Unraveling the Pheromone Biosynthesis Activating Neuropeptide (PBAN) signal transduction cascade that regulates sex pheromone production in moths. Vitam Horm. 2010; 83:425-45.
- [10]Blomquist GJ, Jurenka R, Schal C, Tittiger C.. Insect endocrinology. Gilbert LI, editor. Academic, London; 2011. [10.1016/B978-0-12-384749-2.10015-9] webcite
- [11]Wang H-L, Liénard MA, Zhao C-H, Wang C-Z, Löfstedt C. Neofunctionalization in an ancestral insect desaturase lineage led to rare Δ6 pheromone signals in the Chinese tussah silkworm. Insect Biochem Mol Biol. 2010; 40(10):742-51.
- [12]Albre J, Liénard MA, Sirey TM, Schmidt S, Tooman LK, Carraher C, et al. Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of leafroller moths. PLoS Genet. 2012;8(1), e1002489.
- [13]Liénard MA, Lassance J-M, Wang H-L, Zhao C-H, Piškur J, Johansson T, et al. Elucidation of the sex-pheromone biosynthesis producing 5, 7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals Δ11-and Δ9-desaturases with unusual catalytic properties. Insect Biochem Mol Biol. 2010;40(6):440–52.
- [14]Liénard MA, Strandh M, Hedenström E, Johansson T, Löfstedt C. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol Biol. 2008; 8(1):270. BioMed Central Full Text
- [15]Hao G, Liu W, O’Connor M, Roelofs W. Acyl-CoA Z9-and Z10-desaturase genes from a New Zealand leafroller moth species, Planotortrix octo. Insect Biochem Mol Biol. 2002; 32(9):961-6.
- [16]Moto K, Suzuki MG, Hull JJ, Kurata R, Takahashi S, Yamamoto M, et al. Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. Proc Natl Acad Sci. 2004;101(23):8631–6.
- [17]Liu W, Rooney AP, Xue B, Roelofs WL. Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. Gene. 2004; 342(2):303-11.
- [18]Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, Linn C. Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci. 2002; 99(21):13621-6.
- [19]Moto K, Yoshiga T, Yamamoto M, Takahashi S, Okano K, Ando T, et al. Pheromone gland-specific fatty-acyl reductase of the silkmoth, Bombyx mori. Proc Natl Acad Sci. 2003;100(16):9156–61.
- [20]Lassance JM, Groot A, Liénard M, Antony B, Borgwardt C, Andersson F, et al. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature. 2010;466(7305):486–9.
- [21]Lassance JM, Liénard M, Antony B, Qian S, Fujii T, Tabata J, et al. Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths. Proc Natl Acad Sci. 2013;110(10):3967–72.
- [22]Antony B, Fujii T, Moto K, Matsumoto S, Fukuzawa M, Nakano R, et al. Pheromone-gland-specific fatty-acyl reductase in the adzuki bean borer, Ostrinia scapulalis (Lepidoptera: Crambidae). Insect Biochem Mol Biol. 2009;39(2):90–5.
- [23]Liénard MA, Hagström AK, Lassance JM, Löfstedt C. Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. Proc Natl Acad Sci. 2010; 107(24):10955-60.
- [24]Hagström ÅK, Liénard MA, Groot AT, Hedenström E, Löfstedt C. Semi–selective fatty acyl reductases from four heliothine moths influence the specific pheromone composition. PLoS One. 2012; 7(5): Article ID e37230
- [25]Hallem EA, Ho MG, Carlson JR. The molecular basis of odor coding in the Drosophila Antenna. Cell. 2004; 117(7):965-79.
- [26]Vogt RG. Biochemical diversity of odor detection: OBPs, ODEs, and SNMPs. In: Insect pheromone biochemistry and molecular biology. Blomquist GJ, Vogt RG, editors. Elsevier Academic Press, London; 2003: p.391-446.
- [27]Blomquist GJ, Vogt RG. The biosynthesis and detection of pheromones and plant volatiles. Insect pheromone biochemistry and molecular biology. Blomquist GJ, Vogt RG, editors. Elsevier Academic Press, London; 2003.
- [28]Pelosi P, Zhou JJ, Ban L, Calvello M. Soluble proteins in insect chemical communication. Cell Mol Life Sci. 2006; 63(14):1658-76.
- [29]Rogers ME, Krieger J, Vogt RG. Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. J Neurobiol. 2001; 49(1):47-61.
- [30]Rogers ME, Steinbrecht R, Vogt RG. Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus. Cell Tissue Res. 2001; 303(3):433-46.
- [31]Benton R, Vannice KS, Vosshall LB. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature. 2007; 450(7167):289-93.
- [32]Oakeshott JG, Claudianos C, Campbell P, Newcomb R, Russell RJ. Biochemical genetics and genomics of insect esterases. In: Comprehensive molecular insect science. Gilbert L, Iatrou K, Gill SS, editors. Elsevier, London; 2005: p.309-81.
- [33]UNEP. United Nations Environment Programme, Division of Technology, Industry and Economics, Ozone Action Programme, Methyl Bromide Phase-Out Strategies, A Global Compilation of Laws and Regulations. NY, USA: United Nations Publication; 1999. ISBN: 92-807-1773-1.
- [34]Ryne C, Ekeberg M, Jonzén N, Oehlschlager C, Löfstedt C, Anderbrant O. Reduction in an almond moth Ephestia cautella (Lepidoptera: Pyralidae) population by means of mating disruption. Pest Manag Sci. 2006; 62(10):912-8.
- [35]Ding BJ, Hofvander P, Wang HL, Durrett TP, Stymne S, Löfstedt C. A plant factory for moth pheromone production. Nat Commun. 2014;5.
- [36]Heckel DG. Genomics in pure and applied entomology. Ann Rev Entomol. 2003; 48(1):235-60.
- [37]Strandh M, Johansson T, Ahrén D, Löfstedt C. Transcriptional analysis of the pheromone gland of the turnip moth, Agrotis segetum (Noctuidae), reveals candidate genes involved in pheromone production. Insect Mol Biol. 2008; 17(1):73-85.
- [38]Vogel H, Heidel AJ, Heckel DG, Groot AT. Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genomics. 2010; 11:29. BioMed Central Full Text
- [39]Gu SH, Wu KM, Guo YY, Pickett JA, Field LM, Zhou JJ, et al. Identification of genes expressed in the sex pheromone gland of the black cutworm Agrotis ipsilon with putative roles in sex pheromone biosynthesis and transport. BMC Genomics. 2013;14(1):636.
- [40]Zhang YN, Xia YH, Zhu JY, Li SY, Dong SL. Putative pathway of sex pheromone biosynthesis and degradation by expression patterns of genes identified from female pheromone gland and adult antenna of Sesamia inferens (Walker). J Chem Ecol. 2014; 40:439-51.
- [41]Jung CR, Kim Y. Comparative transcriptome analysis of sex pheromone glands of two sympatric lepidopteran congener species. Genomics. 2014; 103(4):308-15.
- [42]Brady UE. Isolation, identification and stimulatory activity of a second component of the sex pheromone system (complex) of the female almond moth, Cadra cautella (Walker). Life Sci. 1973; 13:227-35.
- [43]Valle D. Vitellogenesis in insects and other groups--a review. Mem Inst Oswaldo Cruz. 1993; 88(1):1-26.
- [44]Jurenka R. Insect pheromone biosynthesis. In: The chemistry of pheromones and other semiochemicals I. Berlin, Germany: Springer; 2004. p. 97–132.
- [45]Nusawardani T, Kroemer JA, Choi MY, Jurenka RA. Identification and characterization of the pyrokinin/pheromone biosynthesis activating neuropeptide family of G protein-coupled receptors from Ostrinia nubilalis. Insect Mol Biol. 2013; 22(3):331-40.
- [46]Kim YJ, Nachman RJ, Aimanova K, Gill S, Adams ME. The pheromone biosynthesis activating neuropeptide (PBAN) receptor of Heliothis virescens: Identification, functional expression, and structure–activity relationships of ligand analogs. Peptides. 2008; 29(2):268-75.
- [47]Ohnishi A, Hashimoto K, Imai K, Matsumoto S. Functional characterization of the Bombyx mori fatty acid transport protein (BmFATP) within the silkmoth pheromone gland. J Biol Chem. 2009; 284(8):5128-36.
- [48]Qian S, Fujii T, Ito K, Nakano R, Ishikawa Y. Cloning and functional characterization of a fatty acid transport protein (FATP) from the pheromone gland of a lichen moth, Eilema japonica, which secretes an alkenyl sex pheromone. Insect Biochem Mol Biol. 2011; 41(1):22-8.
- [49]Volpe JJ, Vagelos PR. Saturated fatty acid biosynthesis and its regulation. Ann Rev Biochem. 1973; 42:21-60.
- [50]Pape ME, Lopez-Casillas F, Kim KH. Physiological regulation of acetyl-CoA carboxylase gene expression: effects of diet, diabetes, and lactation on acetyl-CoA carboxylase mRNA. Arch Biochem Biophys. 1988; 267(1):104-9.
- [51]Foster SP, Roelofs WL. Sex pheromone biosynthesis in the tortricid moth, Ctenopseustis herana (Felder & Rogenhofer). Arch Insect Biochem Physiol. 1996; 33(2):135-47.
- [52]Löfstedt C, Bengtsson M. Sex pheromone biosynthesis of (E, E)-8,10-dodecadienol in codling moth Cydia pomonella involves E9 desaturation. J Chem Ecol. 1988; 14(3):903-15.
- [53]Martinez T, Fabriás G, Camps F. Sex pheromone biosynthetic pathway in Spodoptera littoralis and its activation by a neurohormone. J Biol Chem. 1990; 265(3):1381-7.
- [54]Foster S, Roelofs W. Sex pheromone biosynthesis in the leafroller moth Planotortix excessana by Δ10 desaturation. Arch Insect Biochem Physiol. 1988; 8(1):1-9.
- [55]Bjostad LB, Roelofs WL. Sex pheromone biosynthesis from radiolabeled fatty acids in the redbanded leafroller moth. J Biol Chem. 1981; 256(15):7936-40.
- [56]Bjostad LB, Roelofs WL. Sex pheromone biosynthesis in Trichoplusia ni: key steps involve delta-11 desaturation and chain-shortening. Science. 1983; 220(4604):1387-9.
- [57]Zhao C, Löfstedt C, Wang X. Sex pheromone biosynthesis in the Asian corn borer Ostrinia furnacalis (II): biosynthesis of (E)‐and (Z)‐12‐tetradecenyl acetate involves Δ14 desaturation. Arch Insect Biochem Physiol. 1990; 15(1):57-65.
- [58]Los DA, Murata N. Structure and expression of fatty acid desaturases. Biochim Biophys Acta Lipids Lipid Metab. 1998; 1394(1):3-15.
- [59]Xue B, Rooney AP, Kajikawa M, Okada N, Roelofs WL. Novel sex pheromone desaturases in the genomes of corn borers generated through gene duplication and retroposon fusion. Proc Natl Acad Sci. 2007; 104(11):4467-72.
- [60]Ikeda Y, Okamura-Ikeda K, Tanaka K. Purification and characterization of short-chain, medium-chain, and long-chain acyl-CoA dehydrogenases from rat liver mitochondria. Isolation of the holo-and apoenzymes and conversion of the apoenzyme to the holoenzyme. J Biol Chem. 1985; 260(2):1311-25.
- [61]Schulz H. Oxidation of fatty acids in eukaryotes. In: Biochemistry of lipids, lipoproteins and membranes. Vance DE, Vance J, editors. Elsevier, Amsterdam; 2008: p.131-54.
- [62]Uchida YKTT, Izai K, Orii T, Hashimoto T. Novel fatty acid beta-oxidation enzymes in rat liver mitochondria. II. Purification and properties of enoyl-coenzyme A (CoA) hydratase/3-hydroxyacyl-CoA dehydrogenase/3-ketoacyl-CoA thiolase trifunctional protein. J Biol Chem. 1992; 267(2):1034-41.
- [63]Kunau W, Dommes V, Schulz H. beta-oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog. Lipid Res. 1995; 34(4):267-342.
- [64]Schreurs M, Kuipers F, van der Leij FR. Regulatory enzymes of mitochondrial beta-oxidation as targets for treatment of the metabolic syndrome. Obes Rev. 2010; 11(5):380-8.
- [65]Eirín-López JM, Rebordinos L, Rooney AP, Rozas J. The birth-and-death evolution of multigene families revisited. In: Garrido-Ramos MA, editors. Basel, Switzerland: Repetitive DNA. Karger Medical and Scientific Publishers; 2012. p. 170–196.
- [66]Günther CS, Chervin C, Marsh KB, Newcomb RD, Souleyre EJ. Characterisation of two alcohol acyltransferases from kiwifruit (Actinidia spp.) reveals distinct substrate preferences. Phytochem. 2011; 72(8):700-10.
- [67]Durand N, Carot-Sans G, Bozzolan F, Rosell G, Siaussat D, Debernard S, et al. Degradation of pheromone and plant volatile components by a same odorant-degrading enzyme in the cotton leafworm, Spodoptera littoralis. PLoS One. 2011;6(12):e29147.
- [68]Ishida Y, Leal WS. Rapid inactivation of a moth pheromone. Proc Natl Acad Sci. 2005; 102(39):14075-9.
- [69]Merlin C, Rosell G, Carot-Sans G, François MC, Bozzolan F, Pelletier J, et al. Antennal esterase cDNAs from two pest moths, Spodoptera littoralis and Sesamia nonagrioides, potentially involved in odorant degradation. Insect Mol Biol. 2007;16(1):73–81.
- [70]Merlin C, François MC, Bozzolan F, Pelletier J, Jacquin-Joly E, Maïbèche-Coisne M. A new aldehyde oxidase selectively expressed in chemosensory organs of insects. Biochem Biophys Res Commun. 2005; 332(1):4-10.
- [71]Pelletier J, Bozzolan F, Solvar M, François MC, Jacquin-Joly E, Maïbèche-Coisne M. Identification of candidate aldehyde oxidases from the silkworm Bombyx mori potentially involved in antennal pheromone degradation. Gene. 2007; 404(1–2):31-40.
- [72]Rybczynski R, Reagan J, Lerner MR. A pheromone-degrading aldehyde oxidase in the antennae of the moth Manduca sexta. J Neurosci. 1989; 9(4):1341-53.
- [73]Maïbèche-Coisne M, Nikonov A, Ishida Y, Jacquin-Joly E, Leal W. Pheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme. Proc Natl Acad Sci. 2004; 101(31):11459-64.
- [74]Maïbèche-Coisne M, Merlin C, François MC, Porcheron P, Jacquin-Joly E. P450 and P450 reductase cDNAs from the moth Mamestra brassicae: cloning and expression patterns in male antennae. Gene. 2005; 346:195-203.
- [75]Wojtasek H, Leal WS. Degradation of an alkaloid pheromone from the pale-brown chafer, Phyllopertha diversa (Coleoptera: Scarabaeidae), by an insect olfactory cytochrome P450. FEBS Lett. 1999; 458(3):333-6.
- [76]Rogers ME, Jani M, Vogt RG. An olfactory-specific glutathione-S-transferase in the sphinx moth Manduca sexta. J Exp Biol. 1999; 202(12):1625-37.
- [77]Widmayer P, Heifetz Y, Breer H. Expression of a pheromone receptor in ovipositor sensilla of the female moth (Heliothis virescens). Insect Mol Biol. 2009; 18(4):541-7.
- [78]Durand N, Carot‐Sans G, Chertemps T, Montagné N, Jacquin‐Joly E, Debernard S, et al. A diversity of putative carboxylesterases are expressed in the antennae of the noctuid moth Spodoptera littoralis. Insect Mol Biol. 2010;19(1):87–97.
- [79]Picimbon JF. Biochemistry and Evolution of OSD and OBP proteins. In: Pheromone biochemistry and molecular biology. Blomquist GJ, Vogt RG, editors. Academic, New York; 2003: p.539-66.
- [80]Tegoni M, Campanacci V, Cambillau C. Structural aspects of sexual attraction and chemical communication in insects. Trends Biochem Sci. 2004; 29(5):257-64.
- [81]Laue M, Steinbrecht RA, Ziegelberger G. Immunocytochemical localization of general odorant binding protein in olfactory Sensilla of the silkworm Antheraea polyphemus. Natuurwissenschaften. 1994; 81:178-80.
- [82]Steinbrecht R, Ozaki M, Ziegelberger G. Immunocytochemical localization of pheromone-binding protein in moth antennae. Cell Tissue Res. 1992; 270(2):287-302.
- [83]Zhang SG, Maida R, Steinbrecht RA. Immunolocalization of odorant-binding proteins in noctuid moths (Insecta, Lepidoptera). Chem Senses. 2001; 26(7):885-96.
- [84]Krieger J, von Nickisch-Rosenegk E, Mameli M, Pelosi P, Breer H. Binding proteins from the antennae of Bombyx mori. Insect Biochem Mol Biol. 1996; 26(3):297-307.
- [85]Vogt R, Riddiford L. Pheromone binding and inactivation by moth antennae. Nature. 1981; 293(5828):161-3.
- [86]Wojtasek H, Leal WS. Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J Biol Chem. 1999; 274(43):30950-6.
- [87]Zhou JJ, Kan Y, Antoniw J, Pickett J, Field LM. Genome and EST analyses and expression of a gene family with putative functions in insect chemoreception. Chem Senses. 2006; 31(5):453-65.
- [88]Zhou JJ. Odorant-binding proteins in insects. Vitam Horm. 2010; 83:241-72.
- [89]Vieira FG, Rozas J. Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol. 2011; 3:476-90.
- [90]Maleszka J, Forêt S, Saint R, Maleszka R. RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Dev Genes Evol. 2007; 217(3):89-196.
- [91]Gong DP, Zhang HJ, Zhao P, Xia QY, Xiang ZH. The odorant binding protein gene family from the genome of silkworm, Bombyx mori. BMC Genomics. 2009; 10(1):332. BioMed Central Full Text
- [92]Liu NY, Xu W, Papanicolaou A, Dong SL, Anderson A. Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera. BMC Genomics. 2014; 15(1):597-609. BioMed Central Full Text
- [93]Roelofs W, Bjostad L. Biosynthesis of lepidopteran pheromones. Bioorg Chem. 1984; 12(4):279-98.
- [94]Patel RK, Jain M. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One. 2012; 7(2): Article ID e30619
- [95]Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinf. 2009;10(1):421.
- [96]Mortazavi A, Williams B, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008; 5(7):621-8.
- [97]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST. a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402.
- [98]Anderson I, Brass A. Searching DNA databases for similarities to DNA sequences: when is a match significant? Bioinformatics. 1998; 14(4):349-56.
- [99]Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. BLAST2GO. a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21(18):3674-6.
- [100]Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. High-throughput functional annotation and data mining with the BLAST2GO suite. Nucleic Acids Res. 2008;36(10):3420–35.
- [101]Aparicio G, Gotz S, Conesa A, Segrelles D, Blanquer I, García JM, et al. BLAST2GO goes grid: developing a grid-enabled prototype for functional genomics analysis. St Heal T. 2006;120:194.
- [102]Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997; 25(24):4876-82.
- [103]Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013; 30(12):2725-9.