De novo transcriptome analysis and identification of genes associated with immunity, detoxification and energy metabolism from the fat body of the tephritid gall fly, Procecidochares utilis

Autoři: Lifang Li aff001;  Xi Gao aff001;  Mingxian Lan aff001;  Yuan Yuan aff001;  Zijun Guo aff001;  Ping Tang aff001;  Mengyue Li aff001;  Xianbin Liao aff001;  Jiaying Zhu aff002;  Zhengyue Li aff001;  Min Ye aff001;  Guoxing Wu aff001
Působiště autorů: State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, China aff001;  Key Laboratory of Forest Disaster Warning and Control of Yunnan Province, Southwest Forestry University, Kunming, China aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226039


The fat body, a multifunctional organ analogous to the liver and fat tissue of vertebrates, plays an important role in insect life cycles. The fat body is involved in protein storage, energy metabolism, elimination of xenobiotics, and production of immunity regulator-like proteins. However, the molecular mechanism of the fat body’s physiological functions in the tephritid stem gall-forming fly, Procecidochares utilis, are still unknown. In this study, we performed transcriptome analysis of the fat body of P. utilis using Illumina sequencing technology. In total, 3.71 G of clean reads were obtained and assembled into 30,559 unigenes, with an average length of 539 bp. Among those unigenes, 21,439 (70.16%) were annotated based on sequence similarity to proteins in NCBI’s non-redundant protein sequence database (Nr). Sequences were also compared to NCBI’s non-redundant nucleotide sequence database (Nt), a manually curated and reviewed protein sequence database (SwissProt), and KEGG and gene ontology annotations were applied to better understand the functions of these unigenes. A comparative analysis was performed to identify unigenes related to detoxification, immunity and energy metabolism. Many unigenes involved in detoxification were identified, including 50 unigenes of putative cytochrome P450s (P450s), 18 of glutathione S-transferases (GSTs), 35 of carboxylesterases (CarEs) and 26 of ATP-binding cassette (ABC) transporters. Many unigenes related to immunity were identified, including 17 putative serpin genes, five peptidoglycan recognition proteins (PGRPs) and four lysozyme genes. In addition, unigenes potentially involved in energy metabolism, including 18 lipase genes, five fatty acid synthase (FAS) genes and six elongases of very long chain fatty acid (ELOVL) genes, were identified. This transcriptome improves our genetic understanding of P. utilis and the identification of a numerous transcripts in the fat body of P. utilis offer a series of valuable molecular resources for future studies on the functions of these genes.

Klíčová slova:

Detoxification – Drosophila melanogaster – Fats – Insects – Phylogenetic analysis – Sequence databases – Transcriptome analysis – Lipases


1. Sang W, Zhu L, Axmacher JC. Invasion pattern of Eupatorium adenophorum Spreng in southern China. Biolo Invasions, 2010;12(6):1721–1730.

2. Zhou ZX, Jiang H, Yang C, Yang MZ, Zhang HB. Microbial community on healthy and diseased leaves of an invasive plant Eupatorium adenophorum in Southwest China. J Microbiol. 2010;48(2):139–145. doi: 10.1007/s12275-010-9185-y 20437143.

3. Erasmus DJ, Bennett PH. The effect of galls induced by the gall fly Procecidochares utilis on vegetative growth and reproductive potential of crofton weed, Ageratina andenophora. Ann Appl Biolo. 2010; 120(1):173–181. doi: 10.1111/j.1744-7348.1992.tb03414.x

4. Wang Y. Predicting the potential geographic distribution of crofton weed (Ageratina adenophora) around the world using maxent modeling. Int J Plant Res. 2012; 25(2):324–335.

5. Bess HA and Frank HH. Biological control of Pamakani, Eupatorium adenophorum, in Hawaii by a tephritid gall fly, Procecidochares utilis. 2. Population studies of the weed, the fly and the parasites of the fly. Ecolo. 1959; 40(2): 244–249. doi: 10.2307/1930034

6. Rahman O, Agarwal ML. Biological control of crofton weed (Eupatorium adenophorum Sprengel) by a fruit fly Procecidochares utilis Stone in eastern Himalayas. Indian J Weed Sci. 1990; 22:98–101.

7. Buccellato L, Byrne MJ, Witkowski ETF. Interactions between a stem gall fly and a leaf-spot pathogen in the biological control of Ageratina adenophora. Biolo Control. 2012;61(3):222–229. doi: 10.1016/j.biocontrol.2012.02.004

8. Gao X, Zhu JY, Ma S, Zhang Z, Xiao C, Li Q, et al. Transcriptome profiling of the crofton weed gall fly Procecidochares utilis. Genet Mol Res. 2014;13(2):2857–2864. doi: 10.4238/2014.March.19.1 24682983.

9. Li AF, Gao XM, Dang WG, Huang RX, Deng ZP, Tang HC. Parasitism of Procecidochares utilis and its effect on growth and reproduction of Eupatorium adenophorum. J Plant Ecol. 2006; 30(3): 496–503.

10. Arrese EL, Soulages JL. Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol. 2010; 55(55):207–225. doi: 10.1146/annurev-ento-112408-085356 19725772.

11. Yu H, Ji R, Ye W, Chen H, Lai W, Fu Q, Lou Y. Transcriptome analysis of fat bodies from two brown planthopper (Nilaparvata lugens) populations with different virulence levels in rice. PLoS ONE. 2014; 9(2):e88528. doi: 10.1371/journal.pone.0088528 24533099.

12. Dunn PE. Biochemical aspects of insect immunology. Annu Rev Entomol. 1986; 31(31):321–339. doi: 10.1146/annurev.en.31.010186.001541

13. Yang WJ, Yuan GR, Cong L, Xie YF, Wang JJ. De novo cloning and annotation of genes associated with immunity, detoxification and energy metabolism from the fat body of the oriental fruit fly, Bactrocera dorsalis. PLoS ONE. 2014; 9(4):e94470. doi: 10.1371/journal.pone.0094470 24710118.

14. Attardo GM, Strickler-Dinglasan P, Perkin SA, Caler E, Bonaldo MF, Soares MB, et al. Analysis of fat body transcriptome from the adult tsetse fly, Glossina morsitans morsitans. Insect Mol Biol. 2006; 15(4):411–24. doi: 10.1111/j.1365-2583.2006.00649.x 16907828.

15. Price DP, Nagarajan V, Churbanov A, Houde P, Milligan B, Drake LL, et al. The fat body transcriptomes of the yellow fever mosquito Aedes aegypti, pre- and post- blood meal. PLoS ONE. 2011; 6(7):e22573. doi: 10.1371/journal.pone.0022573 21818341.

16. Snyder MJ, Stevens JL, Andersen JF, Feyereisen R. Expression of cytochrome P450 genes of the CYP4 family in midgut and fat body of the tobacco hornworm, Manduca sexta. Arch Biochem Biophys. 1995; 321(1):13–20. doi: 10.1006/abbi.1995.1362 7639512.

17. Yang J, McCart C, Woods DJ, Terhzaz S, Greenwood KG, ffrench-Constant RH, et al. A Drosophila systems approach to xenobiotic metabolism. Physiol Genomics. 2007; 30(3):223–231. doi: 10.1152/physiolgenomics.00018.2007 17488889.

18. Jiang Z, Wu XL, Michal JJ, McNamara JP. Pattern profiling and mapping of the fat body transcriptome in Drosophila melanogaster. Obes Res. 2005; 13(11):1898–904. doi: 10.1038/oby.2005.233 16339120.

19. Feitosa FM, Calvo E, Merino EF, Durham AM, James AA, de Bianchi AG, et al. A transcriptome analysis of the Aedes aegypti vitellogenic fat body. J Insect Sci. 2006;6(6):1–26. doi: 10.1673/1536-2442(2006)6[1:ATAOTA]2.0.CO;2 19537968.

20. Nanoth Vellichirammal N, Zera AJ, Schilder RJ, Wehrkamp C, Riethoven JJ, Brisson JA. De novo transcriptome assembly from fat body and flight muscles transcripts to identify morph-specific gene expression profiles in Gryllus firmus. PLoS ONE. 2014; 9(1):e82129. doi: 10.1371/journal.pone.0082129 24416137.

21. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full–length transcriptome assembly from RNA–Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644–652. doi: 10.1038/nbt.1883 21572440.

22. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, et al. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics. 2003; 19(5):651–652. doi: 10.1093/bioinformatics/btg034 12651724.

23. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool (BLAST). J Mol Biol. 1990; 215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712.

24. 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):3674–3676. doi: 10.1093/bioinformatics/bti610 16081474.

25. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, et al. InterProScan: protein domains identifer. Nucleic Acids Res. 2005; 33:116–20. doi: 10.1093/nar/gki442 15980438.

26. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol. 2011; 28(10):2731–2739. doi: 10.1093/molbev/msr121 21546353.

27. Li LF, Lan MX, Lu WF, Li ZY, Xia T, Zhu JY, et al. De novo transcriptomic analysis of the alimentary tract of the tephritid gall fly, Procecidochares utilis. PLoS ONE. 2018; 13(8):e0201679. doi: 10.1371/journal.pone.0201679 30138350.

28. Feyereisen R. Insect P450 enzymes. Annu Rev Entomol. 1999; 44(44):507–533. doi: 10.1146/annurev.ento.44.1.507 9990722.

29. Zhou D, Liu X, Sun Y, Ma L, Shen B, Zhu C. Genomic analysis of detoxification supergene families in the mosquito Anopheles sinensis. PLoS ONE. 2015; 10(11):e0143387. doi: 10.1371/journal.pone.0143387 26588704.

30. Guo Y, Chai Y, Zhang L, Zhao Z, Gao LL, Ma R. Transcriptome analysis and identification of major detoxification gene families and insecticide targets in Grapholita Molesta (Busck) (Lepidoptera: Tortricidae). J Insect Sci. 2017; 17(2):43. doi: 10.1093/jisesa/iex014 28365764.

31. Qiu Z, Liu F, Lu H, Yuan H, Zhang Q, Huang Y. De Novo assembly and characterization of the transcriptome of Grasshopper Shirakiacris shirakii. Int J Mol Sci. 2016;17(7):1110. doi: 10.3390/ijms17071110 27455245.

32. Aljabr AM, Hussain A, Rizwan-Ul-Haq M, Al-Ayedh H. Toxicity of plant secondary metabolites modulating detoxification genes expression for natural red palm weevil pesticide development. Molecules. 2017; 22(1):169–181. doi: 10.3390/molecules22010169 28117698.

33. Huang X, Ma J, Qin X, Tu X, Cao G, Wang G, et al. Biology, physiology and gene expression of grasshopper Oedaleus asiaticus exposed to diet stress from plant secondary compounds. Sci Rep. 2017; 7(1):8655–8664. doi: 10.1038/s41598-017-09277-z 28819233.

34. Qin Q, Li Y, Zhong D, Zhou N, Chang X, Li C, et al. Insecticide resistance of Anopheles sinensis and An. vagus in Hainan Island, a malaria-endemic area of China. Parasit Vectors. 2014; 7:92. doi: 10.1186/1756-3305-7-92 24589247.

35. Wang RL, Staehelin C, Xia QQ, Su YJ, Zeng RS. Identification and characterization of CYP9A40 from the tobacco cutworm moth (Spodoptera litura), a cytochrome P450 gene induced by plant allelochemicals and insecticides. Int J Mol Sci. 2015;16(9):22606–20. doi: 10.3390/ijms160922606 26393579.

36. Rupasinghe SG, Wen Z, Chiu TL, Schuler MA. Helicoverpa zea CYP6B8 and CYP321A1: different molecular solutions to the problem of metabolizing plant toxins and insecticides. Protein Eng Des Sel. 2007; 20(12):615–624. doi: 10.1093/protein/gzm063 18065401.

37. Yu L, Tang W, He W, Ma X, Vasseur L, Baxter SW, et al. Characterization and expression of the cytochrome P450 gene family in diamondback moth, Plutella xylostella (L.). Sci Rep. 2015; 5:8952. doi: 10.1038/srep08952 25752830.

38. Guo Y, Zhang X, Wu H, Yu R, Zhang J, Zhu KY, et al. Identification and functional analysis of a cytochrome P450 gene CYP9AQ2 involved in deltamethrin detoxification from Locusta migratoria. Pestic Biochem Physiol. 2015; 122:1–7. doi: 10.1016/j.pestbp.2015.01.003 26071800.

39. Guo Y, Wu H, Zhang X, Ma E, Guo Y, Zhu KY, Zhang J. RNA interference of cytochrome P450 CYP6F subfamily genes affects susceptibility to different insecticides in Locusta migratoria. Pest Manag Sci. 2016;72(11):2154–2165. doi: 10.1002/ps.4248 26853074.

40. Arouri R, Le Goff G, Hemden H, Navarro-Llopis V, M'saad M, Castañera P, et al. Resistance to lambda-cyhalothrin in Spanish field populations of Ceratitis capitata and metabolic resistance mediated by P450 in a resistant strain. Pest Manag Sci. 2015;71(9):1281–1291. doi: 10.1002/ps.3924 25296621.

41. Gellatly KJ, Yoon KS, Doherty JJ, Sun W, Pittendrigh BR, Clark JM. RNAi validation of resistance genes and their interactions in the highly DDT-resistant 91-R strain of Drosophila melanogaster. Pestic Biochem Physiol. 2015; 121:107–115. doi: 10.1016/j.pestbp.2015.01.001 26047118.

42. Bautista MA, Miyata T, Miura K, Tanaka T. RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. 2009; 39(1):38–46. doi: 10.1016/j.ibmb.2008.09.005 18957322.

43. Pavlidi N, Kampouraki A, Tseliou V, Wybouw N, Dermauw W, Roditakis E, et al. Molecular characterization of pyrethroid resistance in the olive fruit fly Bactrocera oleae. Pestic Biochem Physiol. 2018; 148:1–7. doi: 10.1016/j.pestbp.2018.03.011 29891359.

44. Hussain A, Rizwan-Ul-Haq M, Al-Ayedh H, Aljabr AM. Toxicity and Detoxification Mechanism of Black Pepper and Its Major Constituent in Controlling Rhynchophorus ferrugineus Olivier (Curculionidae: Coleoptera). Neotrop Entomol. 2017; 46(6):685–693. doi: 10.1007/s13744-017-0501-7 28326461.

45. Mao W, Rupasinghe SG, Johnson RM, Zangerl AR, Schuler MA, Berenbaum MR. Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp Biochem Physiol B Biochem Mol Biol. 2009; 154(4):427–434. doi: 10.1016/j.cbpb.2009.08.008 19737624.

46. Mao W, Schuler MA, Berenbaum MR. Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera). Proc Natl Acad Sci USA. 2017;114(10):2538–2543. doi: 10.1073/pnas.1614864114 28193870.

47. Mao W, Schuler MA, Berenbaum MR. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proc Natl Acad Sci USA. 2011; 108(31):12657–62. doi: 10.1073/pnas.1109535108 21775671.

48. Wang RL, He YN, Staehelin C, Liu SW, Su YJ, Zhang JE. Identification of Two Cytochrome Monooxygenas P450 Genes, CYP321A7 and CYP321A9, from the Tobacco Cutworm Moth (Spodoptera Litura) and Their Expression in Response to Plant Allelochemicals. Int J Mol Sci. 2017; 18(11): pii:E2278; doi: 10.3390/ijms18112278 29084173.

49. Jensen HR, Scott IM, Sims S, Trudeau VL, Arnason JT. Gene expression profiles of Drosophila melanogaster exposed to an insecticidal extract of Piper nigrum. J Agric Food Chem. 2006;54(4):1289–1295. doi: 10.1021/jf052046n 16478250.

50. Bhaskara S, Dean ED, Lam V, Ganguly R. Induction of two cytochrome P450 genes, Cyp6a2 and Cyp6a8, of Drosophila melanogaster by caffeine in adult flies and in cell culture. Gene. 2006; 377 (1):56–64. doi: 10.1016/j.gene.2006.02.032 16713132.

51. Bass C, Hebsgaard M B, Hughes J. Genomic resources for the brown planthopper, Nilaparvata lugens: Transcriptome pyrosequencing and microarray design. Insect Sci. 2012; 19(1):1–12. doi: 10.1111/j.1744-7917.2011.01440.x

52. Sparks ME, Rhoades JH, Nelson DR, Kuhar D, Lancaster J, Lehner B, et al. A transcriptome survey spanning life stages and sexes of the harlequin bug, Murgantia histrionica. Insects. 2017; 8(2): 55. doi: 10.3390/insects8020055 28587099.

53. Friedman R. Genomic organization of the glutathione S-transferase family in insects. Mol Phylogenet Evol. 2011; 61(3):924–32. doi: 10.1016/j.ympev.2011.08.027 21930223.

54. Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, Sharakhova MV, et al. Evolution of supergene families associated with insecticide resistance. Sci. 2002; 298(5591):179–81. doi: 10.1126/science.1076781 12364796.

55. Zhang J, Zhang Y, Li J, Liu M, Liu Z. Midgut transcriptome of the cockroach Periplaneta americana and its microbiota: digestion, detoxification and oxidative stress response. PLoS ONE. 2016; 11(5):e0155254. doi: 10.1371/journal.pone.0155254 27153200.

56. Shen GM, Dou W, Niu JZ, Jiang HB, Yang WJ, Jia FX, et al. Transcriptome analysis of the oriental fruit fly (Bactrocera dorsalis). PLoS ONE. 2011; 6(12):e29127. doi: 10.1371/journal.pone.0029127 22195006.

57. Wang J, Xiong KC, Liu YH. De novo Transcriptome analysis of chinese citrus fly, Bactrocera minax (Diptera: Tephritidae), by high-throughput illumina sequencing. PLoS ONE. 2016; 11(6):e0157656. doi: 10.1371/journal.pone.0157656 27331903.

58. Singh SP, Coronella JA, Benes H, Cochrane BJ, Zimniak P. Catalytic function of Drosophila melanogaster glutathione S-transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur J Biochem. 2001; 268(10):2912–23. doi: 10.1046/j.1432-1327.2001.02179.x 11358508.

59. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara LA, et al. The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochem Mol Biol. 2011;41(3):203–9. doi: 10.1016/j.ibmb.2010.12.005 21195177.

60. Lu XP, Wang LL, Huang Y, Dou W, Chen CT, Wei D, et al. The epsilon glutathione S -transferases contribute to the malathion resistance in the oriental fruit fly, Bactrocera dorsalis (Hendel). Comp Biochem Physiol C Toxicol Pharmacol. 2016; 180:40–48. doi: 10.1016/j.cbpc.2015.11.001 26610787.

61. Qin G, Liu T, Guo Y, Zhang X, Ma E, Zhang J. Effects of chlorpyrifos on glutathione S -transferase in migratory locust, Locusta migratoria. Pestic Biochem Physiol. 2014;109(1):1–5. doi: 10.1016/j.pestbp.2013.12.008 24581378.

62. Yepiskoposyan H, Egli D, Fergestad T, Selvaraj A, Treiber C, Multhaup G, et al. Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res. 2006; 34(17):4866–77. doi: 10.1093/nar/gkl606 16973896.

63. Wu K, Hoy MA. The Glutathione-S-Transferase, Cytochrome P450 and carboxyl/cholinesterase gene superfamilies in predatory mite Metaseiulus occidentalis. PLoS One. 2016; 11(7):e0160009. doi: 10.1371/journal.pone.0160009 27467523.

64. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol. 2005; 45:51–88. doi: 10.1146/annurev.pharmtox.45.120403.095857 15822171.

65. Pavlidi N, Tseliou V, Riga M, Nauen R, Van Leeuwen T, Labrou NE, et al. Functional characterization of glutathione S-transferases associated with insecticide resistance in Tetranychus urticae. Pestic Biochem Physiol. 2015; 121:53–60. doi: 10.1016/j.pestbp.2015.01.009 26047112.

66. Board PG, Baker RT, Chelvanayagam G, Jermiin LS. Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem J. 1997; 328 (Pt 3):929–35. doi: 10.1042/bj3280929 9396740.

67. Yamamoto K, Shigeoka Y, Aso Y, Banno Y, Kimura M, Nakashima T. Molecular and biochemical characterization of a Zeta-class glutathione S-transferase of the silkmoth. Pestic Biochem Physiol. 2009;94(1):30–35.

68. Huang Y, Xu Z, Lin X, Feng Q, Zheng S. Structure and expression of glutathione S-transferase genes from the midgut of the common cutworm, Spodoptera litura (Noctuidae) and their response to xenobiotic compounds and bacteria. J Insect Physiol. 2011; 57(7):1033–44. doi: 10.1016/j.jinsphys.2011.05.001 21605564.

69. Pan L, Ren L, Chen F, Feng Y, Luo Y. Antifeedant Activity of Ginkgo biloba Secondary Metabolites against Hyphantria cunea Larvae: Mechanisms and Applications. PLoS ONE. 2016; 11(5):e0155682. doi: 10.1371/journal.pone.0155682 27214257.

70. Al-Ayedh H, Hussain A, Rizwan-Ul-Haq M, Al-Jabr AM. Status of insecticide resistance in field-collected populations of Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Int J Agric Biol. 2016;18(1):103–110. doi: 10.17957/IJAB/15.0070

71. Yu QY, Lu C, Li WL, Xiang ZH, Zhang Z. Annotation and expression of carboxylesterases in the silkworm, Bombyx mori. BMC Genomics. 2009;10(1):553. doi: 10.1186/1471-2164-10-553 19930670.

72. Lindroth RL. Biochemical detoxication: mechanism of differential tiger swallowtail tolerance to phenolic glycosides. Oecologia. 1989; 81(2):219–224. doi: 10.1007/BF00379809 28312541.

73. Scully ED, Hoover K, Carlson JE, Tien M, Geib SM. Midgut transcriptome profiling of Anoplophora glabripennis, a lignocellulose degrading cerambycid beetle. BMC Genomics. 2013; 14:850. doi: 10.1186/1471-2164-14-850 24304644.

74. Boeckler GA, Gershenzon J, Unsicker SB. Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry. 2011;72(13):1497–509. doi: 10.1016/j.phytochem.2011.01.038 21376356.

75. Li X, Schuler MA, Berenbaum MR. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2007; 52:231–53. doi: 10.1146/annurev.ento.51.110104.151104 16925478.

76. Pavlidi N, Dermauw W, Rombauts S, Chrysargyris A, Chrisargiris A, Van Leeuwen T, et al. Analysis of the olive fruit fly Bactrocera oleae transcriptome and phylogenetic classification of the major detoxification gene families. PLoS ONE. 2015; 10(5):e0128056. doi: 10.1371/journal.pone.0128056 25955294.

77. Oakeshott JG, Claudianos C, Campbell PM, Newcomb RD, Russel RJ. Biochemical genetics and genomics of insect esterases. Compreh Mol Insect Science-Pharmacology Vol.5 (editors Gilbert LI, Iatrou K and Gill SS) 309–381 Elsevier Oxford.

78. Hsu JC, Chien TY, Hu CC, Chen MJ, Wu WJ, Feng HT, et al. Discovery of genes related to insecticide resistance in Bactrocera dorsalis by functional genomic analysis of a de novo assembled transcriptome. PLoS ONE. 2012; 7(8):e40950. doi: 10.1371/journal.pone.0040950 22879883.

79. Zhang J, Li D, Ge P, Guo Y, Zhu KY, Ma E, et al. Molecular and functional characterization of cDNAs putatively encoding carboxylesterases from the migratory locust, Locusta migratoria. PLoS ONE 2014; 9(4):e94809. doi: 10.1371/journal.pone.0094809 24722667.

80. Sun H, Pu J, Chen F, Wang J, Han Z. Multiple ATP-binding cassette transporters are involved in insecticide resistance in the small brown planthopper, Laodelphax striatellus. Insect Mol Biol. 2017;26(3):343–355. doi: 10.1111/imb.12299 28299835.

81. Higgins CF, Linton KJ. The ATP switch model for ABC transporters. Nat Struct Mol Biol. 2004;11(10):918–26. doi: 10.1038/nsmb836 15452563.

82. Hollenstein K, Dawson RJ, Locher KP. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol. 2007; 17(4):412–418. doi: 10.1016/ 17723295.

83. Dean M, Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu Rev Genomics Hum Genet. 2005;6(1):123–142. doi: 10.1146/annurev.genom.6.080604.162122 16124856.

84. Dermauw W, Van Leeuwen T. The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol. 2014; 45:89–110. doi: 10.1016/j.ibmb.2013.11.001 24291285.

85. Xiao LF, Zhang W, Jing TX, Zhang MY, Miao ZQ, Wei DD, et al. Genome-wide identification, phylogenetic analysis, and expression profiles of ATP-binding cassette transporter genes in the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Comp Biochem Physiol Part D Genomics Proteomics. 2018; 25:1–8. doi: 10.1016/j.cbd.2017.10.001 29121518.

86. Epis S, Porretta D, Mastrantonio V, Comandatore F, Sassera D, Rossi P, et al. ABC transporters are involved in defense against permethrin insecticide in the malaria vector Anopheles stephensi. Parasit Vectors. 2014; 7(1):349. doi: 10.1186/1756-3305-7-349 25073980.

87. Tian L, Song T, He R, Zeng Y, Xie W, Wu Q, et al. Genome-wide analysis of ATP-binding cassette (ABC) transporters in the sweetpotato whitefly, Bemisia tabaci. BMC Genomics. 2017; 18(1):330. doi: 10.1186/s12864-017-3706-6 28446145.

88. Bretschneider A, Heckel DG, Vogel H. Know your ABCs: Characterization and gene expression dynamics of ABC transporters in the polyphagous herbivore Helicoverpa armigera. Insect Biochem Mol Biol. 2016; 72:1–9. doi: 10.1016/j.ibmb.2016.03.001 26951878.

89. Aittomäki S, Valanne S, Lehtinen T, Matikainen S, Nyman TA, Rämet M, et al. Proprotein convertase Furin1 expression in the Drosophila fat body is essential for a normal antimicrobial peptide response and bacterial host defense. Faseb J. 2017; 31(11):4770–4782. doi: 10.1096/fj.201700296R 28705811.

90. Hu C, Aksoy S. Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans. Mol Microbiol, 2010; 60(5):1194–1204. doi: 10.1111/j.1365-2958.2006.05180.x 16689795.

91. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, et al. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol. 2006; 15(5):645–656. doi: 10.1111/j.1365-2583.2006.00682.x 17069638.

92. Mwangi S, Murungi E, Jonas M, Christoffels A. Evolutionary genomics of Glossina morsitans immune-related CLIP domain serine proteases and serine protease inhibitors. Infect Genet Evol. 2011;11(4):740–745. doi: 10.1016/j.meegid.2010.10.006 21055483.

93. Garrett M, Fullaondo A, Troxler L, Micklem G, Gubb D. Identification and analysis of serpin-family genes by homology and synteny across the 12 sequenced Drosophilia genomes. BMC Genomics. 2009; 10(1):489–490. doi: 10.1186/1471-2164-10-489 19849829.

94. Zou Z, Evans JD, Lu Z, Zhao P, Williams M, Sumathipala N, et al. Comparative genomic analysis of the Tribolium immune system. Genome Biol. 2007; 8(8):R177. doi: 10.1186/gb-2007-8-8-r177 17727709.

95. Zou Z, Picheng Z, Weng H, Mita K, Jiang H. A comparative analysis of serpin genes in the silkworm genome. Genomics. 2009; 93(4):367–75. doi: 10.1016/j.ygeno.2008.12.010 19150649.

96. Lin H, Lin X, Zhu J, Yu XQ, Xia X, Yao F, et al. Characterization and expression profiling of serine protease inhibitors in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). BMC Genomics, 2017; 18(1):162. doi: 10.1186/s12864-017-3583-z 28196471.

97. He Y, Wang Y, Zhao P, Rayaprolu S, Wang X, Cao X, et al. Serpin-9 and -13 regulate hemolymph proteases during immune responses of Manduca sexta. Insect Biochem Mol Biol. 2017; 90:71–81. doi: 10.1016/j.ibmb.2017.09.015 28987647.

98. Yuan C, Xing L, Wang M, Wang X, Yin M, Wang Q, et al. Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera. PLoS Pathog. 2017; 13(9):e1006645. doi: 10.1371/journal.ppat.1006645 28953952.

99. Zhao S, Wang X, Cai S, Zhang S, Luo H, Wu C, et al. A novel peptidoglycan recognition protein involved in the prophenoloxidase activation system and antimicrobial peptide production in Antheraea pernyi. Dev Comp Immunol. 2018; 86:78–85. doi: 10.1016/j.dci.2018.04.009 29734021.

100. Meister S, Agianian B, Turlure F, Relógio A, Morlais I, Kafatos FC, et al. Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog. 2009; 5(8):e1000542. doi: 10.1371/journal.ppat.1000542 19662170.

101. Ping Z, Fei X, Liang J, Guo H, Xu G, Sun Q, et al. Enhanced antiviral immunity against, Bombyx mori, cytoplasmic polyhedrosis virus via overexpression of peptidoglycan recognition protein S2 in transgenic silkworms. Dev Comp Immunol. 2018; 87:84–89. doi: 10.1016/j.dci.2018.05.021 29902708.

102. Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T, et al. Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc Natl Acad Sci USA. 2002; 99(21):13705–13710. doi: 10.1073/pnas.212301199 12359879.

103. Gendrin M, Turlure F, Rodgers FH, Cohuet A, Morlais I, Christophides GK. The peptidoglycan recognition proteins PGRPLA and PGRPLB regulate Anopheles immunity to bacteria and affect infection by Plasmodium. J Innate Immun. 2017; 9(4):333–342. doi: 10.1159/000452797 28494453.

104. Werner T, Liu G, Kang D, Ekengren S, Steiner H, Hultmark D. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci USA. 2000; 97(25):13772–13777. doi: 10.1073/pnas.97.25.13772 11106397.

105. Koyama H, Kato D, Minakuchi C, Tanaka T, Yokoi K, Miura K. Peptidoglycan recognition protein genes and their roles in the innate immune pathways of the red flour beetle, Tribolium castaneum. J Invertebr Pathol. 2015; 132:86–100. doi: 10.1016/j.jip.2015.09.003 26385528.

106. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, et al. Immunity-related genes and gene families in Anopheles gambiae. Sci. 2002; 298(5591):159–165. doi: 10.1126/science.1077136 12364793.

107. Mohamed AA, Zhang L, Dorrah MA, Elmogy M, Yousef HA, Bassal TT, et al. Molecular characterization of a c-type lysozyme from the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). Dev Comp Immunol. 2016; 61:60–69. doi: 10.1016/j.dci.2016.03.018 26997372.

108. Vogel H, Altincicek B, Glöckner G, Vilcinskas A. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011;12(1):308. doi: 10.1186/1471-2164-12-308 21663692.

109. Altincicek B, Knorr E, Vilcinskas A. Beetle immunity: Identification of immune-inducible genes from the model insect Tribolium castaneum. Dev Comp Immunol. 2008; 32(5):585–95. doi: 10.1016/j.dci.2007.09.005 17981328.

110. Mitaka Y, Kobayashi K, Matsuura K. Caste-, sex-, and age-dependent expression of immune-related genes in a Japanese subterranean termite, Reticulitermes speratus. PLoS ONE. 2017; 12(4):e0175417. doi: 10.1371/journal.pone.0175417 28410430.

111. He Y, Cao X, Li K, Hu Y, Chen YR, Blissard G, et al. A genome-wide analysis of antimicrobial effector genes and their transcription patterns in Manduca sexta. Insect Biochem Mol Biol. 2015; 62:23–37. doi: 10.1016/j.ibmb.2015.01.015 25662101.

112. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, et al. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 2010; 11(2):R21. doi: 10.1186/gb-2010-11-2-r21 20178569.

113. Vilcinskas A, Mukherjee K, Vogel H. Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc Biol Sci. 2013; 280(1750):20122113. doi: 10.1098/rspb.2012.2113 23173204.

114. Chapelle M, Girard PA, Cousserans F, Volkoff NA, Duvic B. Lysozymes and lysozyme-like proteins from the fall armyworm, Spodoptera frugiperda. Mol Immunol. 2009; 47(2–3):261–269. doi: 10.1016/j.molimm.2009.09.028 19828200.

115. Bulet P, Stöcklin R. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept Lett. 2005; 12(1):3–11. doi: 10.2174/0929866053406011 15638797.

116. Mulnix AB, Dunn PE. Structure and induction of a lysozyme gene from the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol. 1994; 24(3):271–281. doi: 10.1016/0965-1748(94)90007-8 7517269.

117. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, et al. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol. 2008; 38(12):1087–1110. doi: 10.1016/j.ibmb.2008.09.001 18835443.

118. Gandhe AS, Janardhan G, Nagaraju J. Immune upregulation of novel antibacterial proteins from silkmoths (Lepidoptera) that resemble lysozymes but lack muramidase activity. Insect Biochem Mol Biol. 2007; 37(7):655–666. doi: 10.1016/j.ibmb.2007.03.013 17550822.

119. Daffre S, Kylsten P, Samakovlis C, Hultmark D. The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Mol Gen Genet. 1994; 242(2):152–62. doi: 10.1007/bf00391008 8159165.

120. Rivera-Perez C. Marine invertebrate lipases: Comparative and functional genomic analysis. Comp Biochem Physiol Part D Genomics Proteomics. 2015; 15:39–48. doi: 10.1016/j.cbd.2015.06.001 26114431.

121. Horne I, Haritos VS, Oakeshott JG. Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol. 2009; 39(8):547–567. doi: 10.1016/j.ibmb.2009.06.002 19540341.

122. Majerowicz D, Calderón-Fernández GM, Alves-Bezerra M, De Paula IF, Cardoso LS, Juárez MP, et al. Lipid metabolism in Rhodnius prolixus: Lessons from the genome. Gene. 2017; 596:27–44. doi: 10.1016/j.gene.2016.09.045 27697616.

123. Hossain MS, Liu Y, Zhou S, Li K, Tian L, Li S. 20-Hydroxyecdysone-induced transcriptional activity of FoxO upregulates brummer and acid lipase-1 and promotes lipolysis in Bombyx fat body. Insect Biochem Mol Biol. 2013; 43(9):829–838. doi: 10.1016/j.ibmb.2013.06.007 23811219.

124. Grönke S, Mildner A, Fellert S, Tennagels N, Petry S, Müller G, et al. Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 2005; 1(5):323–30. doi: 10.1016/j.cmet.2005.04.003 16054079.

125. Attardo GM, Benoit JB, Michalkova V, Yang G, Roller L, Bohova J, et al. Analysis of lipolysis underlying lactation in the tsetse fly, Glossina morsitans. Insect Biochem Mol Biol. 2012; 42(5):360–370. doi: 10.1016/j.ibmb.2012.01.007 22509523.

126. Pistillo D, Manzi A, Tino A, Boyl PP, Graziani F, Malva C. The Drosophila melanogaster lipase homologs: a gene family with tissue and developmental specific expression. J Mol Biol. 1998; 276(5):877–885. doi: 10.1006/jmbi.1997.1536 9566193.

127. Tan QQ, Liu W, Zhu F, Lei CL, Wang XP. Fatty acid synthase 2 contributes to diapause preparation in a beetle by regulating lipid accumulation and stress tolerance genes expression. Sci Rep. 2017; 7:40509. doi: 10.1038/srep40509 28071706.

128. Chung H, Loehlin DW, Dufour HD, Vaccarro K, Millar JG, Carroll SB. A single gene affects both ecological divergence and mate choice in Drosophila. Sci. 2014; 343(6175):1148–1151. doi: 10.1126/science.1249998 24526311.

129. Zuo W, Li C, Luan Y, Zhang H, Tong X, Han M, et al. Genome-wide identification and analysis of elongase of very long chain fatty acid genes in the silkworm, Bombyx mori. Genome. 2018; 61(3):167–176. doi: 10.1139/gen-2017-0224 29505281.

130. Jakobsson A, Westerberg R, Jacobsson A. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res. 2006; 45(3):237–249. doi: 10.1016/j.plipres.2006.01.004 16564093.

131. Ng WC, Chin JS, Tan KJ, Yew JY. The fatty acid elongase Bond is essential for Drosophila sex pheromone synthesis and male fertility. Nat Commun. 2015; 6:8263. doi: 10.1038/ncomms9263 26369287.

132. Urbanski JM, Benoit JB, Michaud MR, Denlinger DL, Armbruster P. The molecular physiology of increased egg desiccation resistance during diapause in the invasive mosquito, Aedes albopictus. Proc Biol Sci. 2010; 277(1694):2683–2692. doi: 10.1098/rspb.2010.0362 20410035.

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