Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade


Autoři: Jun Xu aff001;  Wei Liu aff002;  Dehong Yang aff001;  Shuqing Chen aff001;  Kai Chen aff001;  Zulian Liu aff001;  Xu Yang aff001;  Jing Meng aff001;  Guanheng Zhu aff004;  Shuanglin Dong aff004;  Yong Zhang aff005;  Shuai Zhan aff001;  Guirong Wang aff002;  Yongping Huang aff001
Působiště autorů: Key Laboratory of Insect Developmental and Evolutionary Biology, Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China aff001;  State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China aff002;  Shanghai First Maternity and Infant Hospital, Tongji University School of Medicine, Shanghai, China aff003;  Education Ministry Key Laboratory of Integrated Management of Crop Disease and Pests, College of Plant Protection, Nanjing Agricultural University, Nanjing, China aff004;  Department of Biology, University of Nevada, Reno, Nevada, United States of America aff005
Vyšlo v časopise: Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008622
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008622

Souhrn

Insect courtship and mating depend on integration of olfactory, visual, and tactile cues. Compared to other insects, Bombyx mori, the domesticated silkworm, has relatively simple sexual behaviors as it cannot fly. Here by using CRISPR/Cas9 and electrophysiological techniques we found that courtship and mating behaviors are regulated in male silk moths by mutating genes in the sex determination cascade belonging to two conserved pathways. Loss of Bmdsx gene expression significantly reduced the peripheral perception of the major pheromone component bombykol by reducing expression of the product of the BmOR1 gene which completely blocked courtship in adult males. Interestingly, we found that mating behavior was regulated independently by another sexual differentiation gene, Bmfru. Loss of Bmfru completely blocked mating, but males displayed normal courtship behavior. Lack of Bmfru expression significantly reduced the perception of the minor pheromone component bombykal due to the down regulation of BmOR3 expression; further, functional analysis revealed that loss of the product of BmOR3 played a key role in terminating male mating behavior. Our results suggest that Bmdsx and Bmfru are at the base of the two primary pathways that regulate olfactory-based sexual behavior.

Klíčová slova:

Animal antennae – Gene expression – Gene regulation – Mating behavior – Moths and butterflies – Pheromones – Sex determination – Silkworms


Zdroje

1. Williams TM, Carroll SB. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat Rev Genet 2009; 10:797–804. doi: 10.1038/nrg2687 19834484

2. Murray SM, Yang SY, Van Doren M. Germ cell sex determination: a collaboration between soma and germline. Curr Opin Cell Biol 2010; 22:722–729. doi: 10.1016/j.ceb.2010.09.006 21030233

3. Gempe T, Beye M. Function and evolution of sex determination mechanisms, genes and pathways in insects. Bioessays 2011; 33: 52–60. doi: 10.1002/bies.201000043 21110346

4. Graham PL, Yanowitz JL, Penn JK, Deshpande G, Schedl P. The translation initiation factor eIF4E regulates the sex-specific expression of the master switch gene Sxl in Drosophila melanogaster. PLoS Genet 2011; 7: e1002185. doi: 10.1371/journal.pgen.1002185 21829374

5. Hashiyama K, Hayashi Y, Kobayashi S. Drosophila Sex lethal gene initiates female development in germline progenitors. Science 2011; 333: 885–888. doi: 10.1126/science.1208146 21737698

6. Siera SG, Cline TW. Sexual back talk with evolutionary implications: stimulation of the Drosophila sex-determination gene sex-lethal by its target transformer. Genetics 2008; 180: 1963–1981. doi: 10.1534/genetics.108.093898 18845845

7. Valcárcel J, Singh R, Zamore PD, Green MR. The protein Sex-lethal antagonizes the splicing factor U2AF to regulate alternative splicing of transformer pre-mRNA. Nature 1993; 362: 171–175. doi: 10.1038/362171a0 7680770

8. Mattox W, Baker BS. Autoregulation of the splicing of transcripts from the transformer-2 gene of Drosophila. Genes Dev 1991; 5: 786–796. doi: 10.1101/gad.5.5.786 2026327

9. Heinrichs V, Ryner LC, Baker BS. Regulation of sex-specific selection of fruitless 5’ splice sites by transformer and transformer-2. Mol Cell Biol 1998; 18: 450–458. doi: 10.1128/mcb.18.1.450 9418892

10. Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H, Arai Y, et al. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature 2014; 509: 633–636. doi: 10.1038/nature13315 24828047

11. Sakai H, Sumitani M, Chikami Y, Yahata K, Uchino K, Kiuchi T, et al. Transgenic Expression of the piRNA-Resistant Masculinizer Gene Induces Female-Specific Lethality and Partial Female-to-Male Sex Reversal in the Silkworm, Bombyx mori. PLoS Genet 2016; 12: e1006203. doi: 10.1371/journal.pgen.1006203 27579676

12. Xu J, Chen S, Zeng B, James AA, Tan A, Huang Y. Bombyx mori P-element Somatic Inhibitor (BmPSI) is a key auxiliary factor for silkworm male sex determination. PLoS Genet 2017; 13: e1006576. doi: 10.1371/journal.pgen.1006576 28103247

13. Xu J, Zhan S, Chen S, Zeng B, Li Z, James AA, et al. Sexually dimorphic traits in the silkworm, Bombyx mori, are regulated by doublesex. Insect Biochem Mol Biol 2017; 80: 42–51. doi: 10.1016/j.ibmb.2016.11.005 27867075

14. Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T. Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev 2005; 7: 58–68. doi: 10.1111/j.1525-142X.2005.05007.x 15642090

15. Xu J, Wang Y, Li Z, Ling L, Zeng B, James AA, et al. Transcription activator-like effector nuclease (TALEN)-mediated female-specific sterility in the silkworm, Bombyx mori. Insect Mol Biol 2014; 23: 800–807. doi: 10.1111/imb.12125 25125145

16. Duan J, Xu H, Ma S, Guo H, Wang F, Zhang L, et al. Ectopic expression of the male BmDSX affects formation of the chitin plate in female Bombyx mori. Mol Reprod Dev 2014; 81: 240–247. doi: 10.1002/mrd.22290 24420266

17. Burtis KC, Coschigano KT, Baker B., Wensink PC. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J 1991; 10: 2577–2582. 1907913

18. Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 2008; 134: 610–623. doi: 10.1016/j.cell.2008.06.052 18724934

19. Tanaka K, Barmina O, Sanders LE, Arbeitman MN, Kopp A. Evolution of sex-specific traits through changes in HOX-dependent doublesex expression. PLoS Biol 2011; 9: e1001131. doi: 10.1371/journal.pbio.1001131 21886483

20. Luo SD, Baker BS. Constraints on the evolution of a doublesex target gene arising from doublesex’s pleiotropic deployment. Proc Natl Acad Sci U S A 2015; 112: E852–861. doi: 10.1073/pnas.1501192112 25675536

21. Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 2010; 13: 458–466. doi: 10.1038/nn.2515 20305646

22. von Philipsborn AC, Jörchel S, Tirian L, Demir E, Morita T, Stern DL, Dickson BJ. Cellular and behavioral functions of fruitless isoforms in Drosophila courtship. Curr Biol 2014; 24: 242–251. doi: 10.1016/j.cub.2013.12.015 24440391

23. Demir E, Dickson BJ. fruitless splicing specifies male courtship behavior in Drosophila. Cell 2005; 121: 785–794. doi: 10.1016/j.cell.2005.04.027 15935764

24. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS. Sexual dimorphism in the fly brain. Curr Biol 2010; 20: 1589–1601. doi: 10.1016/j.cub.2010.07.045 20832311

25. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005; 436: 395–400. doi: 10.1038/nature03859 15959468

26. Pan Y, Baker BS. Genetic identification and separation of innate and experience-dependent courtship behaviors in Drosophila. Cell 2014; 156: 236–248. doi: 10.1016/j.cell.2013.11.041 24439379

27. Ellendersen BE, von Philipsborn AC. Neuronal modulation of D. melanogaster sexual behaviour. Curr Opin Insect Sci 2017; 24: 21–28. doi: 10.1016/j.cois.2017.08.005 29208219

28. Auer TO, Benton R. Sexual circuitry in Drosophila. Curr Opin Neurobiol 2016; 38: 18–26. doi: 10.1016/j.conb.2016.01.004 26851712

29. Nojima T, Neville MC, Goodwin SF. Fruitless isoforms and target genes specify the sexually dimorphic nervous system underlying Drosophila reproductive behavior. Fly (Austin) 2014; 8: 95–100. doi: 10.4161/fly.29132 25483248

30. Gailey DA, Billeter JC, Liu JH, Bauzon F, Allendorfer JB, Goodwin SF. Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Mol Biol Evol 2006; 23: 633–643. doi: 10.1093/molbev/msj070 16319090

31. Salvemini M, Robertson M, Aronson B, Atkinson P, Polito LC, Saccone G. Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for female sex determination. Int J Dev Biol 2009; 53: 109–120. doi: 10.1387/ijdb.082681ms 19123132

32. Salvemini M, D’Amato R, Petrella V, Aceto S, Nimmo D, Neira M, Alphey L, Polito LC, Saccone G. The orthologue of the fruitfly sex behaviour gene fruitless in the mosquito Aedes aegypti: evolution of genomic organisation and alternative splicing. PLoS One 2013; 8: e48554. doi: 10.1371/journal.pone.0048554 23418412

33. Bertossa RC, van de Zande L, Beukeboom LW. The Fruitless gene in Nasonia displays complex sex-specific splicing and contains new zinc finger domains. Mol Biol Evol 2009; 26: 1557–1569. doi: 10.1093/molbev/msp067 19349644

34. Meier N, Käppeli SC, Hediger Niessen M, Billeter JC, Goodwin SF, Bopp D. Genetic control of courtship behavior in the housefly: evidence for a conserved bifurcation of the sex-determining pathway. PLoS One 2013; 8: e62476. doi: 10.1371/journal.pone.0062476 23630634

35. Clynen E, Ciudad L, Bellés X, Piulachs MD. Conservation of fruitless’ role as master regulator of male courtship behaviour from cockroaches to flies. Dev Genes Evol 2011; 221: 43–48. doi: 10.1007/s00427-011-0352-x 21340608

36. Kaissling KE, Kasang G, Bestmann H, Stransky W, Vostrowsky O. A new pheromone of the silkworm moth Bombyx mori. Naturwissenschaften 1978; 65: 382–384.

37. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, et al. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 2004; 101: 16653–16658. doi: 10.1073/pnas.0407596101 15545611

38. Nakagawa T, Sakurai T, Nishioka T, Touhara K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 2005; 307: 1638–1642. doi: 10.1126/science.1106267 15692016

39. 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: 547–555. doi: 10.1093/chemse/bjj059 16679489

40. Sakurai T, Mitsuno H, Mikami A, Uchino K, Tabuchi M, Zhang F, et al. Targeted disruption of a single sex pheromone receptor gene completely abolishes in vivo pheromone response in the silkmoth. Sci Rep 2015; 5: 11001. doi: 10.1038/srep11001 26047360

41. Shiota Y, Sakurai T, Daimon T, Mitsuno H, Fujii T, Matsuyama S, et al. In vivo functional characterisation of pheromone binding protein-1 in the silkmoth, Bombyx mori. Sci Rep 2018; 8: 13529. doi: 10.1038/s41598-018-31978-2 30202026

42. Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T. Analysis of the biological functions of a doublesex homologue in Bombyx mori. Dev Genes Evol 2003; 213: 345–354. doi: 10.1007/s00427-003-0334-8 12733073

43. Liu Q, Liu W, Zeng B, Wang G, Hao D, Huang Y. Deletion of the Bombyx mori odorant receptor co-receptor (BmOrco) impairs olfactory sensitivity in silkworms. Insect Biochem Mol Biol 2017; 86: 58–67. doi: 10.1016/j.ibmb.2017.05.007 28577927

44. Daimon T, Fujii T, Fujii T, Yokoyama T, Katsuma S, Shinoda T, et al. Reinvestigation of the sex pheromone of the wild silkmoth Bombyx mandarina: the effects of bombykal and bombykyl acetate. J Chem Ecol 2012; 38: 1031–1035. doi: 10.1007/s10886-012-0164-0 22836825

45. Wanner KW, Anderson AR, Trowell SC, Theilmann DA, Robertson HM, Newcomb RD. Female-biased expression of odourant receptor genes in the adult antennae of the silkworm, Bombyx mori. Insect Mol Biol 2007; 16: 107–119. doi: 10.1111/j.1365-2583.2007.00708.x 17257213

46. Katsuma S, Kiuchi T, Kawamoto M, Fujimoto T, Sahara K. Unique sex determination system in the silkworm, Bombyx mori: current status and beyond. Proc Jpn Acad Ser B Phys Biol Sci 2018; 94: 205–216. doi: 10.2183/pjab.94.014 29760316

47. Sawanth SK, Gopinath G, Sambrani N, Arunkumar KP. The autoregulatory loop: A common mechanism of regulation of key sex determining genes in insects. J Biosci 2016; 41: 283–294. doi: 10.1007/s12038-016-9609-x 27240989

48. Sakurai T, Mitsuno H, Haupt SS, Uchino K, Yokohari F, Nishioka T, et al. A single sex pheromone receptor determines chemical response specificity of sexual behavior in the silkmoth Bombyx mori. PLoS Genet 2011; 7: e1002115. doi: 10.1371/journal.pgen.1002115 21738481

49. Tabuchi M, Sakurai T, Mitsuno H, Namiki S, Minegishi R, Shiotsuki T, et al. Pheromone responsiveness threshold depends on temporal integration by antennal lobe projection neurons. Proc Natl Acad Sci U S A 2013; 110: 15455–15460. doi: 10.1073/pnas.1313707110 24006366

50. Tanaka K, Uda Y, Ono Y, Nakagawa T, Suwa M, Yamaoka R, et al. Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr Biol 2009; 19: 881–890. (Erratum in 2011, 21: 623.) doi: 10.1016/j.cub.2009.04.035 19427209

51. Heinrichs V, Ryner LC, Baker BS. Regulation of sex-specific selection of fruitless 5’ splice sites by transformer and transformer-2. Mol Cell Biol 1998; 18: 450–458. doi: 10.1128/mcb.18.1.450 9418892

52. Ohbayashi F. Structural and functional analyses on the Bombyx mori genes homologous to Drosophila doublesex and fruitless. Ph.D. thesis, The University of Tokyo; 2001.

53. Wang Q, Taliaferro JM, Klibaite U, Hilgers V, Shaevitz JW, Rio DC. The PSI-U1 snRNP interaction regulates male mating behavior in Drosophila. Proc Natl Acad Sci U S A 2016; 113: 5269–5274. doi: 10.1073/pnas.1600936113 27114556

54. Wang Y, Li Z, Xu J, Zeng B, Ling L, You L, et al. The CRISPR/Cas System mediates efficient genome engineering in Bombyx mori. Cell Res 2013; 23: 1414–1416. doi: 10.1038/cr.2013.146 24165890

55. Naito Y, Hino K, Bono H, Ui-Tei K. CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics 2015; 31: 1120–1123. doi: 10.1093/bioinformatics/btu743 25414360

56. Zhu GH, Xu J, Cui Z, Dong XT, Ye ZF, Niu DJ, et al. Functional characterization of SlitPBP3 in Spodoptera litura by CRISPR/Cas9 mediated genome editing. Insect Biochem Mol Biol 2016; 75: 1–9. doi: 10.1016/j.ibmb.2016.05.006 27192033

57. Xu J, Yu Y, Chen K, Huang Y. Intersex regulates female external genital and imaginal disc development in the silkworm. Insect Biochem Mol Biol 2019; 108: 1–8. doi: 10.1016/j.ibmb.2019.02.003 30831220

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Genetika Reprodukční medicína

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PLOS Genetics


2020 Číslo 6

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