Identification of putative Type-I sex pheromone biosynthesis-related genes expressed in the female pheromone gland of Streltzoviella insularis

Autoři: Yuchao Yang aff001;  Jing Tao aff001;  Shixiang Zong aff001
Působiště autorů: Beijing Key Laboratory for Forest Pest Control, School of Forestry, Beijing Forestry University, Beijing, China aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Species-specific sex pheromones play key roles in moth sexual communication. Although the general pathway of Type-I sex pheromone biosynthesis is well established, only a handful of genes encoding enzymes involved in this pathway have been characterized. Streltzoviella insularis is a destructive wood-boring pest of many street trees in China, and the female sex pheromone of this species comprises a blend of (Z)-3-tetradecenyl acetate, (E)-3-tetradecenyl acetate, and (Z)-5-dodecenyl acetate. This organism therefore provides an excellent model for research on the diversity of genes and molecular mechanisms involved in pheromone production. Herein, we assembled the pheromone gland transcriptome of S. insularis by next-generation sequencing and identified 74 genes encoding candidate key enzymes involved in the fatty acid biosynthesis, β-oxidation, and functional group modification. In addition, tissue expression patterns further showed that an acetyl-CoA carboxylase and two desaturases were highly expressed in the pheromone glands compared with the other tissues, indicating possible roles in S. insularis sex pheromone biosynthesis. Finally, we proposed putative S. insularis biosynthetic pathways for sex pheromone components and highlighted candidate genes. Our findings lay a solid foundation for understanding the molecular mechanisms underpinning S. insularis sex pheromone biosynthesis, and provide potential targets for disrupting chemical communication that could assist the development of novel pest control methods.

Klíčová slova:

Alcohols – Biosynthesis – Dehydrogenases – Fatty acids – Moths and butterflies – Pheromones – Sex pheromones – Transcriptome analysis


1. Ando T, Inomata S, Yamamoto M. Lepidopteran sex pheromones. Top Curr Chem. 2004; 239: 51–96. doi: 10.1007/b95449 22160231

2. Witzgall P, Kirsch P, Cork A. Sex pheromones and their impact on pest management. J Chem Ecol. 2010; 36: 80–100. doi: 10.1007/s10886-009-9737-y 20108027

3. McNeil JN. Behavioral ecology of pheromone-mediated communication in moths and its importance in the use of pheromone traps. Annu Rev Entomol. 1991; 36: 407–430.

4. 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. doi: 10.1016/s0965-1748(99)00016-8 10406089

5. Löfstedt C, Wahlberg N, Millar JG. Evolutionary patterns of pheromone diversity in lepidoptera. In: Allison JD, Cardé RT, editors. Pheromone communication in moths: evolution, behavior and application. Berkeley: University of California Press. 2016. pp. 43–78.

6. Löfstedt C, Hansson BS, Petersson E, Valeur P, Richards A. Pheromonal secretions from glands on the 5th abdominal sternite of hydropsychid and rhyacophilid caddisflies (Trichoptera). J Chem Ecol. 1994; 20:153–170. doi: 10.1007/BF02065998 24241706

7. Kozlov MV, Zhu JW, Philipp P, Francke W, Zvereva EL, Hansson BS, et al. Pheromone specificity in Eriocrania semipurpurella (Stephens) and E. sangii (Wood) (Lepidoptera: Eriocraniidae) based on chirality of semiochemicals. J Chem Ecol. 1996; 22: 431–454. doi: 10.1007/BF02033647 24227484

8. Raina AK, Wergin WP, Murphy CA, Erbe EF. Structural organization of the sex pheromone gland in Helicoverpa zea in relation to pheromone production and release. Arthropod Struct Dev. 2000; 29: 343–353. 18088939

9. Jurenka R. Insect pheromone biosynthesis. Top Curr Chem. 2004; 239: 97–132. doi: 10.1007/b95450 22160232

10. Matsumoto S. Molecular mechanisms underlying sex pheromone production in moths. Biosci Biotechnol Biochem. 2010; 74: 223–231. doi: 10.1271/bbb.90756 20139627

11. 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 USA. 2004; 101: 8631–8636. doi: 10.1073/pnas.0402056101 15173596

12. Park HY, Kim MS, Paek A, Jeong SE, Knipple DC. An abundant acyl-CoA (Δ9) desaturase transcript in pheromone glands of the cabbage moth, Mamestra brassicae, encodes a catalytically inactive protein. Insect Biochem Mol Biol. 2008; 38: 581–595. doi: 10.1016/j.ibmb.2008.02.001 18405835

13. Volpe JJ, Vagelos PR. Saturated fatty acid biosynthesis and its regulation. Annu Rev Biochem. 1973; 42: 21–60. doi: 10.1146/ 4147183

14. 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: 104–109. doi: 10.1016/0003-9861(88)90013-6 2904242

15. Bjostad LB, Roelofs WL. Biosynthesis of sex pheromone components and glycerolipid precursors from sodium [1–14C] acetate in redbanded leafroller moth. J Chem Ecol. 1984; 10: 681–691. doi: 10.1007/BF00994228 24318604

16. Foster SP, Roelofs WL. Sex pheromone biosynthesis in the tortricid moth, Ctenopseustis herana (Felder & Rogenhofer). Arch Insect Biochem Physiol. 1996; 32: 135–147.

17. Wang HL, Liénard MA, Zhao CH, Wang CZ, 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: 742–751. doi: 10.1016/j.ibmb.2010.07.009 20691782

18. 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: 903–915. doi: 10.1007/BF01018782 24276140

19. Foster SP, Roelofs WL. Sex pheromone biosynthesis in the leafroller moth Planotortix excessana by Δ10 desaturation. Arch Insect Biochem Physiol. 1988; 8: 1–9.

20. Bjostad LB, Roelofs WL. Sex pheromone biosynthesis from radiolabeled fatty acids in the redbanded leafroller moth. J Biol Chem. 1981; 256: 7936–7940. 7021542

21. Zhao CH, Löfstedt C, Wang XY. 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: 57–65.

22. Knipple DC, Rosenfield CL, Nielsen R, You KM, Jeong SE. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics. 2002; 162: 1737–1752. 12524345

23. Houten SM, Wanders RJA. A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. J Inherited Metab Dis. 2010; 33: 469–477. doi: 10.1007/s10545-010-9061-2 20195903

24. 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 USA. 2003; 100: 9156–9161. doi: 10.1073/pnas.1531993100 12871998

25. Chen DS, Dai JQ, Han SC. Identification of the pheromone biosynthesis genes from the sex pheromone gland transcriptome of the diamondback moth, Plutella xylostella. Sci Rep. 2017; 7: 16255. doi: 10.1038/s41598-017-16518-8 29176628

26. Zhang YN, Zhang LW, Chen DS, Sun L, Li ZQ, Ye ZF, et al. Molecular identification of differential expression genes associated with sex pheromone biosynthesis in Spodoptera exigua. Mol Genet Genomics. 2017; 292: 795–809. doi: 10.1007/s00438-017-1307-3 28349297

27. Teal PEA, Tumlinson JH. Properties of cuticular oxidases used for sex pheromone biosynthesis by Heliothis zea. J Chem Ecol. 1988; 14: 2131–2145. doi: 10.1007/BF01014254 24277148

28. Fang N, Teal PEA, Tumlinson JH. Correlation between glycerolipids and pheromone aldehydes in the sex pheromone gland of female tobacco hornworm moths, Manduca sexta (L.). Arch Insect Biochem Physiol. 1995; 30: 321–336.

29. Bestmann HJ, Herrig M, Attygalle AB. Terminal acetylation in pheromone biosynthesis by Mamestra brassicae L. (Lepidoptera: Noctuidae). Experientia. 1987; 43: 1033–1034.

30. Teal PEA, Tumlinson JH. The role of alcohols in pheromone biosynthesis by two noctuid moths that use acetate pheromone components. Arch Insect Biochem Physiol. 1987; 4: 261–269.

31. Zhu JW, Zhao CH, Lu F, Bengtsson M, Löfstedt C. Reductase specificity and the ratio regulation of E/Z isomers in the pheromone biosynthesis of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Insect Biochem Mol Biol. 1996; 26: 171–176.

32. Gao RT, Qin XX. Preliminary study on Holcocerus insularis. For Pest Dis. 1983: 1, 3–5.

33. Liu HX, Liu ZX, Zheng HX, Jin ZR, Zhang JT, Zhang PQ. Sensilla on the antennae and ovipositor of the carpenterworm, Streltzoviella insularis (Staudinger, 1892) (Lepidoptera, Cossidae). Oriental Insects. 2018; 52: 420–433.

34. Xu LL, Pei JH, Wang T, Ren LL, Zong SX. The larval sensilla on the antennae and mouthparts of five species of Cossidae (Lepidoptera). Can J Zool. 2017; 95: 611–622.

35. Zhang JT, Meng XZ. Electrophysiological responses of Holcocerus insularis Staudinger to the female sex pheromone extracts and standard compounds. Scientia Silvae Sinicae. 2000; 36: 123–126.

36. Zhang JT, Meng XZ. Synthesis and filed tests of sex attractant for Holcocerus insularis Staudinger (Lepidoptera: Cossidae). Scientia Silvae Sinicae. 2001; 37: 71–74.

37. 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. doi: 10.1186/1471-2164-11-29 20074338

38. 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: 644–652. doi: 10.1038/nbt.1883 21572440

39. 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: 3674–3676. doi: 10.1093/bioinformatics/bti610 16081474

40. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science. 1997; 278: 631–637. doi: 10.1126/science.278.5338.631 9381173

41. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: An automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007; 35: W182–W185. doi: 10.1093/nar/gkm321 17526522

42. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnol. 2010; 28: 511–515.

43. 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: 2731–2739. doi: 10.1093/molbev/msr121 21546353

44. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4: 406–425. doi: 10.1093/oxfordjournals.molbev.a040454 3447015

45. Rambaut A. FigTree 1.4.2 software. Institute of Evolutionary Biology, Univ. Edinburgh. 2014; Available from:

46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001; 25: 402–408. doi: 10.1006/meth.2001.1262 11846609

47. Raina AK, Jaffe H, Kempe TG, Keim P, Blacher RW, Fales HM, et al. Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science. 1989; 244: 796–798. doi: 10.1126/science.244.4906.796 17802237

48. Rafaeli A, Bober R, Becker L, Choi MY, Fuerst EJ, Jurenka RA. Spatial distribution and differential expression of the PBAN receptor in tissues of adult Helicoverpa spp. (Lepidoptera: Noctuidae). Insect Mol Biol. 2007; 16: 287–293. doi: 10.1111/j.1365-2583.2007.00725.x 17328713

49. Jurenka RA, Fabrias G, Roelofs WL. Hormonal control of female sex pheromone biosynthesis in the redbanded leafroller moth, Argyrotaenia velutinana. Insect Biochem. 1991; 21: 81–89.

50. Choi MY, Jurenka RA. Role of extracellular Ca2+ and calcium channel activated by a G protein-coupled receptor regulating pheromone production in Helicoverpa zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am. 2006; 99: 905–909.

51. Choi MY, Fuerst EJ, Rafaeli A, Jurenka RA. Identification of a G protein-coupled receptor for pheromone biosynthesis activating neuropeptide from pheromone glands of the moth Helicoverpa zea. Proc Natl Acad Sci USA. 2003; 100: 9721–9726. doi: 10.1073/pnas.1632485100 12888624

52. Hull JJ, Ohnishi A, Moto K, Kawasaki Y, Kurata R, Suzuki MG, et al. Cloning and characterization of the pheromone biosynthesis activating neuropeptide receptor from the silkmoth, Bombyx mori—Significance of the carboxyl terminus in receptor internalization. J Biol Chem. 2004; 279: 51500–51507. doi: 10.1074/jbc.M408142200 15358772

53. 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: 268–275. doi: 10.1016/j.peptides.2007.12.001 18243415

54. Lee JM, Hull JJ, Kawai T, Goto C, Kurihara M, Tanokura M, et al. Re-evaluation of the PBAN receptor molecule: characterization of PBANR variants expressed in the pheromone glands of moths. Front Endocrinol. 2012; 3: 6.

55. Hull JJ, Ohnishi A, Matsumoto S. Regulatory mechanisms underlying pheromone biosynthesis activating neuropeptide (PBAN)-induced internalization of the Bombyx mori PBAN receptor. Biochem Biophys Res Commun. 2005; 334: 69–78. doi: 10.1016/j.bbrc.2005.06.050 15992769

56. Moore CA, Milano SK, Benovic JL. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol. 2007; 69: 451–482. doi: 10.1146/annurev.physiol.69.022405.154712 17037978

57. Marchese A, Paing MM, Temple BR, Trejo J. G protein—coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol. 2008; 48: 601–629. doi: 10.1146/annurev.pharmtox.48.113006.094646 17995450

58. Ding BJ, Löfstedt C. Analysis of the Agrotis segetum pheromone gland transcriptome in the light of sex pheromone biosynthesis. BMC Genomics. 2015; 16: 711. doi: 10.1186/s12864-015-1909-2 26385554

59. 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: 636. doi: 10.1186/1471-2164-14-636 24053512

60. 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: 331–340. doi: 10.1111/imb.12025 23551811

61. Fodor J, Hull JJ, Köblös G, Jacquin-Joly E, Szlanka T, Fónagy A. Identification and functional characterization of the pheromone biosynthesis activating neuropeptide receptor isoforms from Mamestra brassicae. Gen Comp Endocrinol. 2018; 258: 60–69. doi: 10.1016/j.ygcen.2017.05.024 28579335

62. Golz A, Focke M, Lichtenthaler HK. Inhibitors of de novo fatty acid biosynthesis in higher plants. J Plant Physiol. 1994; 143: 426–433.

63. Sasaki Y, Konishi T, Nagano Y. The compartmentation of acetyl-coenzyme A carboxylase in plants. Plant Physiol. 1995; 108: 445–449. doi: 10.1104/pp.108.2.445 12228484

64. Harwood JL. Fatty acid metabolism. Annu Rev Plant Physiol Plant Mol Biol. 1988; 39: 101–138.

65. Eliyahu D, Applebaum S, Rafaeli A. Moth sex-pheromone biosynthesis is inhibited by the herbicide diclofop. Pestic Biochem Phys. 2003; 77: 75–81.

66. Tang JD, Charlton RE, Jurenka RA, Wolf WA, Phelan PL, Sreng L, et al. Regulation of pheromone biosynthesis by a brain hormone in two moth species. Proc Natl Acad Sci USA. 1989; 86: 1806–1810. doi: 10.1073/pnas.86.6.1806 16594018

67. Jurenka RA, Jacquin E, Roelofs WL. Stimulation of pheromone biosynthesis in the moth Helicoverpa zea: Action of a brain hormone on pheromone glands involves Ca2+ and cAMP as second messengers. Proc Natl Acad Sci USA. 1991; 88: 8621–8625. doi: 10.1073/pnas.88.19.8621 11607216

68. 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: 439–451. doi: 10.1007/s10886-014-0433-1 24817326

69. Hashimoto K, Yoshizawa AC, Okuda S, Kuma K, Goto S, Kanehisa M. The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes. J Lipid Res. 2008; 49: 183–191. doi: 10.1194/jlr.M700377-JLR200 17921532

70. 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: 1311–1325. 3968063

71. Kunau WH, Dommes V, Schulz H. β-Oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: A century of continued progress. Prog Lipid Res. 1995; 34: 267–342. doi: 10.1016/0163-7827(95)00011-9 8685242

72. Uchida Y, Izai K, Orii T, Hashimoto T. Novel fatty acid β-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: 1034–1041. 1730633

73. Sofer W, Martin PF. Analysis of alcohol dehydrogenase gene expression in Drosophila. Annu Rev Genet. 1987; 21: 203–227. doi: 10.1146/ 3327463

74. Bohren KM, Bullock B, Wermuth B, Gabbay KH. The aldo-keto reductase superfamily. cDNAs and deduced amino acid sequences of human aldehyde and aldose reductases. J Biol Chem. 1989; 264: 9547–9551. 2498333

75. Jurenka RA, Roelofs WL. Characterization of the acetyltransferase used in pheromone biosynthesis in moths: specificity for the Z isomer in Tortricidae. Insect Biochem. 1989; 19: 639–644.

76. Morse D, Meighen E. Biosynthesis of the acetate ester precursor of the spruce budworm sex pheromone by an acetyl CoA: fatty alcohol acetyltransferase. Insect Biochem. 1987; 17: 53–59.

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