Hormonal control of fruitless expression and male sexual orientation in Drosophila

Xiaoxiao Ji; Lin Wang; Xiaolong Li; Sheng Li; Suning Liu; Yufeng Pan

doi:10.59717/j.xinn-life.2024.100060

The Innovation Life > 2024 Vol. 2 > No. 1 > 100060

Next Article Previous Article

REPORT Open Access

Cite PDF

Hormonal control of fruitless expression and male sexual orientation in Drosophila

1.
The Key Laboratory of Developmental Genes and Human Disease, School of Life Science and Technology, Southeast University, Nanjing 210096, China
2.
Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology and School of Life Sciences, South China Normal University, Guangzhou 510631, China
3.
Guangmeiyuan R & D Center, Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, South China Normal University, Meizhou 514779, China
4.
Co-innovation Center of Neuroregeneration, Nantong University, Nantong 226019, China

More Information

Corresponding authors: pany@seu.edu.cn (Y.P.); liusuning@scnu.edu.cn (S.L.)
Received Date: January 22, 2024

Accepted Date: February 20, 2024

Published Online: March 12, 2024

The Innovation Life 2(1), https://doi.org/10.59717/j.xinn-life.2024.100060 | Cite this article

GRAPHICAL ABSTRACT

GRAPHICAL ABSTRACT

DownLoad: Full size image

PUBLIC SUMMARY

PUBLIC SUMMARY
1. Ecdysone promotes larval and pupal expression of fruitless (fru), a master gene for male courtship in flies.
  
  Juvenile hormone suppresses larval fru expression by inhibiting ecdysone signaling.
  
  Ecdysone regulates the morphology and activity of courtship command-like neurons to alter male sexual orientation.
  
  Fly hormones and vertebrate sex hormones play conserved and diversified roles in sexual development and behaviors.

ABSTRACT

ABSTRACT

Sex determination genes control the differentiation of gonads that synthesize and secret sex hormones to remotely control sexual development and behaviors in mammals. In contrast, sex determination genes in insects directly control sexual development and behaviors in a cell-autonomous way, which is largely independent of hormones. In this study, we find that two important hormones, juvenile hormone (JH) and 20-hydroxyecdysone (20E), oppositely regulate the dynamic expression of Fru^M, the male-specific product of the sex determination gene fruitless in Drosophila. 20E signaling is essential to the high-level expression of Fru^M proteins in the pupal stage, while JH suppresses larval Fru^M expression through inhibiting 20E signaling. We further show that 20E signaling regulates both the development and physiological function of the male-specific P1 neurons to mediate sexual orientation in male flies. Our results demonstrate both conserved and diversified functions of hormones in sexual development and behaviors in flies and mice.

FullText(HTML)

REFERENCES

[1]	Gubbay, J., Collignon, J., Koopman, P., et al. (1990). A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346: 245−250. DOI: 10.1038/346245a0. View in Article CrossRef Google Scholar
[2]	Christiansen, A.E., Keisman, E.L., Ahmad, S.M., et al. (2002). Sex comes in from the cold: the integration of sex and pattern. Trends. Genet. 18: 510−516. DOI: 10.1016/s0168-9525(02)02769-5. View in Article CrossRef Google Scholar
[3]	Yamamoto, D. and Koganezawa, M. (2013). Genes and circuits of courtship behaviour in Drosophila males. Nat. Rev. Neurosci. 14: 681−692. DOI: 10.1038/nrn3567. View in Article CrossRef Google Scholar
[4]	Chen, J., Jin, S., Chen, D., et al. (2021). Fruitless tunes functional flexibility of courtship circuitry during development. Elife 10: e59224. DOI: 10.7554/eLife.59224. View in Article CrossRef Google Scholar
[5]	Peng, Q., Chen, J., and Pan, Y. (2021). From fruitless to sex: On the generation and diversification of an innate behavior. Genes Brain Behav. 20: e12772. DOI: 10.1111/gbb.12772. View in Article CrossRef Google Scholar
[6]	Shukla, J.N. and Nagaraju, J. (2010). Doublesex: a conserved downstream gene controlled by diverse upstream regulators. J. Genet. 89: 341−356. DOI: 10.1007/s12041-010-0046-6. View in Article CrossRef Google Scholar
[7]	Salvemini, M., Polito, C., and Saccone, G. (2010). Fruitless alternative splicing and sex behaviour in insects: An ancient and unforgettable love story. J. Genet. 89(3): 287−299. DOI: 10.1007/s12041-010-0040-z. View in Article CrossRef Google Scholar
[8]	Han, C., Peng, Q., Su, X., et al. (2022). A male-specific doublesex isoform reveals an evolutionary pathway of sexual development via distinct alternative splicing mechanisms. Commun. Biol. 5: 728. DOI: 10.1038/s42003-022-03664-7. View in Article CrossRef Google Scholar
[9]	Lin, H.H., Cao, D.S., Sethi, S., et al. (2016). Hormonal modulation of pheromone detection enhances male courtship success. Neuron 90: 1272−1285. DOI: 10.1016/j.neuron.2016.05.004. View in Article CrossRef Google Scholar
[10]	Zhao, S., Deanhardt, B., Barlow, G.T., et al. (2020). Chromatin-based reprogramming of a courtship regulator by concurrent pheromone perception and hormone signaling. Sci. Adv. 6: eaba6913. DOI: 10.1126/sciadv.aba6913. View in Article CrossRef Google Scholar
[11]	Zhang, B., Sato, K., and Yamamoto, D. (2018). Ecdysone signaling regulates specification of neurons with a male-specific neurite in Drosophila. Biol. Open 7: bio029744. DOI: 10.1242/bio.029744. View in Article CrossRef Google Scholar
[12]	Bilen, J., Atallah, J., Azanchi, R., et al. (2013). Regulation of onset of female mating and sex pheromone production by juvenile hormone in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 110: 18321−18326. DOI: 10.1073/pnas.1318119110. View in Article CrossRef Google Scholar
[13]	Chen, N., Liu, Y.J., Fan, Y.L., et al. (2022). A single gene integrates sex and hormone regulators into sexual attractiveness. Nat. Ecol. Evol. 6: 1180−1190. DOI: 10.1038/s41559-022-01808-w. View in Article CrossRef Google Scholar
[14]	Dalton, J.E., Lebo, M.S., Sanders, L.E., et al. (2009). Ecdysone receptor acts in fruitless- expressing neurons to mediate Drosophila courtship behaviors. Curr. Biol. 19: 1447−1452. DOI: 10.1016/j.cub.2009.06.063. View in Article CrossRef Google Scholar
[15]	Ganter, G.K., Walton, K.L., Merriman, J.O., et al. (2007). Increased male-male courtship in ecdysone receptor deficient adult flies. Behav. Genet. 37: 507−512. DOI: 10.1007/s10519-006-9140-1. View in Article CrossRef Google Scholar
[16]	Gotoh, H., Miyakawa, H., Ishikawa, A., et al. (2014). Developmental link between sex and nutrition; doublesex regulates sex-specific mandible growth via juvenile hormone signaling in stag beetles. PLoS Genet. 10: e1004098. DOI: 10.1371/journal.pgen.1004098. View in Article CrossRef Google Scholar
[17]	Li, J., Ning, C., Liu, Y., et al. (2023). Prothoracicotropic hormone controls female sexual receptivity through the function of ecdysone in pC1 neurons of Drosophila. eLife 12: RP92545. DOI: 10.7554/elife.92545.1. View in Article CrossRef Google Scholar
[18]	Sethi, S., Lin, H.H., Shepherd, A.K., et al. (2019). Social context enhances hormonal modulation of pheromone detection in Drosophila. Curr. Biol. 29: 3887−3898.e3884. DOI: 10.1016/j.cub.2019.09.045. View in Article CrossRef Google Scholar
[19]	Dubrovsky, E.B. (2005). Hormonal cross talk in insect development. Trends Endocrinol. Metab. 16: 6−11. DOI: 10.1016/j.tem.2004.11.003. View in Article CrossRef Google Scholar
[20]	Zhang, X., Li, S., and Liu, S. (2021). Juvenile hormone studies in Drosophila melanogaster. Front. Physiol. 12: 785320. DOI: 10.3389/fphys.2021.785320. View in Article CrossRef Google Scholar
[21]	Jin, M., North, H.L., Peng, Y., et al. (2023). Adaptive evolution to the natural and anthropogenic environment in a global invasive crop pest, the cotton bollworm. The Innovation 4 : 100454. DOI: https://doi.org/10.1016/j.xinn.2023.100454. View in Article Google Scholar
[22]	Ren, C., Chen, N., and Li, S. (2023). Harnessing “little mighty” cockroaches: Pest management and beneficial utilization. The Innovation 4 : 100531. DOI: https://doi.org/10.1016/j.xinn.2023.100531. View in Article Google Scholar
[23]	Niwa, Y.S. and Niwa, R. (2014). Neural control of steroid hormone biosynthesis during development in the fruit fly Drosophila melanogaster. Genes Genet. Syst. 89: 27−34. DOI: 10.1266/ggs.89.27. View in Article CrossRef Google Scholar
[24]	Riddiford, L.M., Cherbas, P., and Truman, J.W. (2000). Ecdysone receptors and their biological actions. Vitam. Horm. 60: 1−73. DOI: 10.1016/s0083-6729(00)60016-x. View in Article CrossRef Google Scholar
[25]	Li, K., Jia, Q.Q., and Li, S. (2019). Juvenile hormone signaling - a mini review. Insect. Sci. 26: 600−606. DOI: 10.1111/1744-7917.12614. View in Article CrossRef Google Scholar
[26]	Godlewski, J., Wang, S., and Wilson, T.G. (2006). Interaction of bHLH-PAS proteins involved in juvenile hormone reception in Drosophila. Biochem. Biophys. Res. Commun. 342: 1305−1311. DOI: 10.1016/j.bbrc.2006.02.097. View in Article CrossRef Google Scholar
[27]	Ashok, M., Turner, C., and Wilson, T.G. (1998). Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc. Natl. Acad. Sci. USA 95: 2761−2766. DOI: 10.1073/pnas.95.6.2761. View in Article CrossRef Google Scholar
[28]	Wilson, T.G., and Fabian, J. (1986). A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118: 190−201. DOI: 10.1016/0012-1606(86)90087-4. View in Article CrossRef Google Scholar
[29]	He, Q., Wen, D., Jia, Q., et al. (2014). Heat shock protein 83 (Hsp83) facilitates methoprene-tolerant (Met) nuclear import to modulate juvenile hormone signaling. J. Biol. Chem. 289: 27874−27885. DOI: 10.1074/jbc.M114.582825. View in Article CrossRef Google Scholar
[30]	Minakuchi, C., Zhou, X., and Riddiford, L.M. (2008). Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech. Dev. 125: 91−105. DOI: 10.1016/j.mod.2007.10.002. View in Article CrossRef Google Scholar
[31]	Riddiford, L.M., Truman, J.W., Mirth, C.K., et al. (2010). A role for juvenile hormone in the prepupal development of Drosophila melanogaster. Development 137: 1117−1126. DOI: 10.1242/dev.037218. View in Article CrossRef Google Scholar
[32]	Liu, Y., Sheng, Z., Liu, H., et al. (2009). Juvenile hormone counteracts the bHLH-PAS transcription factors MET and GCE to prevent caspase-dependent programmed cell death in Drosophila. Development 136: 2015−2025. DOI: 10.1242/dev.033712. View in Article CrossRef Google Scholar
[33]	Stockinger, P., Kvitsiani, D., Rotkopf, S., et al. (2005). Neural circuitry that governs Drosophila male courtship behavior. Cell 121: 795−807. DOI: 10.1016/j.cell.2005.04.026. View in Article CrossRef Google Scholar
[34]	Zhang, W., Guo, C., Chen, D., et al. (2018). Hierarchical control of Drosophila sleep, courtship, and feeding behaviors by male-specific P1 neurons. Neurosci. Bull. 34: 1105−1110. DOI: 10.1007/s12264-018-0281-z. View in Article CrossRef Google Scholar
[35]	Cao, J., Li, Y., Xia, W., et al. (2011). A Drosophila metallophosphoesterase mediates deglycosylation of rhodopsin. EMBO J. 30: 3701−3713. DOI: 10.1038/emboj.2011.254. View in Article CrossRef Google Scholar
[36]	Wen, D., Rivera-Perez, C., Abdou, M., et al. (2015). Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet. 11: e1005038. DOI: 10.1371/journal.pgen.1005038. View in Article CrossRef Google Scholar
[37]	Talbot, W.S., Swyryd, E.A., and Hogness, D.S. (1993). Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73: 1323−1337. DOI: 10.1016/0092-8674(93)90359-x. View in Article CrossRef Google Scholar
[38]	Truman, J.W., Talbot, W.S., Fahrbach, S.E., et al. (1994). Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120: 219−234. DOI: 10.1242/dev.120.1.219. View in Article CrossRef Google Scholar
[39]	Bender, M., Imam, F.B., Talbot, W.S., et al. (1997). Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 91: 777−788. DOI: 10.1016/s0092-8674(00)80466-3. View in Article CrossRef Google Scholar
[40]	Schubiger, M., Wade, A.A., Carney, G.E., et al. (1998). Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125: 2053−2062. DOI: 10.1242/dev.125.11.2053. View in Article CrossRef Google Scholar
[41]	Liu, S., Li, K., Gao, Y., et al. (2018). Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. Proc. Natl. Acad. Sci. USA 115: 139−144. DOI: 10.1073/pnas.1716897115. View in Article CrossRef Google Scholar
[42]	Kimura, K., Hachiya, T., Koganezawa, M., et al. (2008). Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59: 759−769. DOI: 10.1016/j.neuron.2008.06.007. View in Article CrossRef Google Scholar
[43]	Jiang, X., and Pan, Y. (2022). Neural control of action selection among innate behaviors. Neurosci. Bull. 38: 1541−1558. DOI: 10.1007/s12264-022-00886-x. View in Article CrossRef Google Scholar
[44]	Pan, Y., Meissner, G.W., and Baker, B.S. (2012). Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc. Natl. Acad. Sci. USA. 109: 10065−10070. DOI: 10.1073/pnas.1207107109. View in Article CrossRef Google Scholar
[45]	Lee, T., Marticke, S., Sung, C., et al. (2000). Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28: 807−818. DOI: 10.1016/s0896-6273(00)00155-0. View in Article CrossRef Google Scholar
[46]	Brown, H.L., Cherbas, L., Cherbas, P., et al. (2006). Use of time-lapse imaging and dominant negative receptors to dissect the steroid receptor control of neuronal remodeling in Drosophila. Development 133: 275−285. DOI: 10.1242/dev.02191. View in Article CrossRef Google Scholar
[47]	Cherbas, L., Hu, X., Zhimulev, I., et al. (2003). EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130: 271−284. DOI: 10.1242/dev.00205. View in Article CrossRef Google Scholar
[48]	Mouillet, J.F., Henrich, V.C., Lezzi, M., et al. (2001). Differential control of gene activity by isoforms A, B1 and B2 of the Drosophila ecdysone receptor. Eur. J. Biochem. 268: 1811−1819. DOI: 10.1046/j.1432-1327.2001.02051.x. View in Article CrossRef Google Scholar
[49]	Hu, X., Cherbas, L., and Cherbas, P. (2003). Transcription activation by the ecdysone receptor (EcR/USP): Identification of activation functions. Mol. Endocrinol. 17: 716−731. DOI: 10.1210/me.2002-0287. View in Article CrossRef Google Scholar
[50]	Handler, A.M. (1982). Ecdysteroid titers during pupal and adult development in Drosophila melanogaster. Dev. Biol. 93: 73−82. DOI: 10.1016/0012-1606(82)90240-8. View in Article CrossRef Google Scholar
[51]	Yang, C.F. and Shah, N.M. (2014). Representing sex in the brain, one module at a time. Neuron 82: 261−278. DOI: 10.1016/j.neuron.2014.03.029. View in Article CrossRef Google Scholar
[52]	Schwedes, C., Tulsiani, S., and Carney, G.E. (2011). Ecdysone receptor expression and activity in adult Drosophila melanogaster. J. Insect Physiol. 57 : 899-907. DOI: 10.1016/j.jinsphys.2011.03.027. View in Article Google Scholar

Cited by

ABOUT THIS ARTICLE

Cite this article:

Ji X., Wang L., Li X., et al., (2024). Hormonal control of fruitless expression and male sexual orientation in Drosophila. The Innovation Life 2(1): 100060. https://doi.org/10.59717/j.xinn-life.2024.100060

Ji X., Wang L., Li X., et al., (2024). Hormonal control of fruitless expression and male sexual orientation in Drosophila. The Innovation Life 2(1): 100060. https://doi.org/10.59717/j.xinn-life.2024.100060

Welcome!

To request copyright permission to republish or share portions of our works, please visit Copyright Clearance Center's (CCC) Marketplace website at marketplace.copyright.com.

Standard PDF

Extended PDF

Figures(4)

Article Metrics

Article views(7353) PDF downloads(3265)

Hormonal control of fruitless expression and male sexual orientation in Drosophila

GRAPHICAL ABSTRACT

PUBLIC SUMMARY

ABSTRACT

REFERENCES

ABOUT THIS ARTICLE

Cite this article:

Welcome!

Share

Article Metrics

Relative Articles

Cited by

Catalog

{{newsColumn.name}}

Official Account

{{newsColumn.name}}

Stay connected

{{newsColumn.name}}

Hormonal control of fruitless expression and male sexual orientation in Drosophila

GRAPHICAL ABSTRACT

PUBLIC SUMMARY

ABSTRACT

REFERENCES

ABOUT THIS ARTICLE

Cite this article:

Welcome!

Share

Article Metrics

Relative Articles

Cited by

Catalog

Export File

Citation

Format

Content

{{newsColumn.name}}

Official Account

{{newsColumn.name}}

Stay connected

{{newsColumn.name}}