Identification and Functional Analysis of the Gene in a Hemimetabolous Insect,

Overview

Journal Insects

Specialty Biology

Date 2024 Apr 26

PMID 38667392

Authors

Biyun Wang

Zeping Mao

Youyuan Chen

Jinjun Ying

Haiqiang Wang

Zongtao Sun

Junmin Li

Chuanxi Zhang

Jichong Zhuo

Affiliations

Soon will be listed here.

Abstract

The () gene functions as a crucial "tuner" in male insect courtship behavior through distinct expression patterns. In , our previous research showed () influencing male courtship songs, causing mating failures with virgin females. However, the impact of on mating remains unexplored. In this study, the homolog () in yielded four spliceosomes: , , and , encoding proteins of 374aa, 377aa, and 433aa, respectively. Notably, only exhibited male bias, while the others were non-sex-specific. All NlFRU proteins featured the BTB conserved domain, with NlFRU-374 and NlFRU-377 possessing the ZnF domain with different sequences. RNAi-mediated or its isoforms' knockdown in nymph stages blocked wing-flapping behavior in mating males, while embryonic knockdown via maternal RNAi resulted in over 80% of males losing wing-flapping ability, and female receptivity was reduced. expression was -regulated, and yet courtship signals and mating success were unaffected. Remarkably, RNAi-mediated knockdown up-regulated the expression of in macropterous males, which regulated muscle stiffness and delayed force response, suggesting 's involvement in muscle development regulation. Collectively, our results indicate that functions in exhibit a combination of conservation and species specificity, contributing insights into evolution, particularly in Hemiptera species.

Citing Articles

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PMID: 39057242 PMC: 11277001. DOI: 10.3390/insects15070509.

References

Salvemini M, Polito C, Saccone G . Fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story?. J Genet. 2010; 89(3):287-99. DOI: 10.1007/s12041-010-0040-z. View

Siwicki K, Kravitz E . Fruitless, doublesex and the genetics of social behavior in Drosophila melanogaster. Curr Opin Neurobiol. 2009; 19(2):200-6. PMC: 2716404. DOI: 10.1016/j.conb.2009.04.001. View

Anand A, Villella A, Ryner L, Carlo T, Goodwin S, Song H . Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics. 2001; 158(4):1569-95. PMC: 1461753. DOI: 10.1093/genetics/158.4.1569. View

Shirangi T, McKeown M . Sex in flies: what 'body--mind' dichotomy?. Dev Biol. 2007; 306(1):10-9. DOI: 10.1016/j.ydbio.2007.03.022. View

Heinrichs V, Ryner L, Baker B . Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Mol Cell Biol. 1998; 18(1):450-8. PMC: 121514. DOI: 10.1128/MCB.18.1.450. View

Peng Q, Chen J, Pan Y . From fruitless to sex: On the generation and diversification of an innate behavior. Genes Brain Behav. 2021; 20(8):e12772. DOI: 10.1111/gbb.12772. View

Zollman S, Godt D, Prive G, Couderc J, Laski F . The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A. 1994; 91(22):10717-21. PMC: 45093. DOI: 10.1073/pnas.91.22.10717. View

Dauwalder B . The roles of fruitless and doublesex in the control of male courtship. Int Rev Neurobiol. 2011; 99:87-105. DOI: 10.1016/B978-0-12-387003-2.00004-5. View

Greenspan R, Ferveur J . Courtship in Drosophila. Annu Rev Genet. 2000; 34:205-232. DOI: 10.1146/annurev.genet.34.1.205. View

10.

Pan Y, Baker B . Genetic identification and separation of innate and experience-dependent courtship behaviors in Drosophila. Cell. 2014; 156(1-2):236-48. PMC: 4677784. DOI: 10.1016/j.cell.2013.11.041. View

11.

Goodwin S, Taylor B, Villella A, Foss M, Ryner L, Baker B . Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics. 2000; 154(2):725-45. PMC: 1460956. DOI: 10.1093/genetics/154.2.725. View

12.

Ito H, Fujitani K, Usui K, Tanaka S, Yamamoto D . Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci U S A. 1996; 93(18):9687-92. PMC: 38490. DOI: 10.1073/pnas.93.18.9687. View

13.

Ustinova J, Mayer F . Alternative starts of transcription, several paralogues, and almost-fixed interspecific differences of the gene fruitless in a hemimetabolous insect. J Mol Evol. 2006; 63(6):788-800. DOI: 10.1007/s00239-005-6230-2. View

14.

Saccone G . A history of the genetic and molecular identification of genes and their functions controlling insect sex determination. Insect Biochem Mol Biol. 2022; 151:103873. DOI: 10.1016/j.ibmb.2022.103873. View

15.

Zhou H, Whitworth C, Pozmanter C, Neville M, Van Doren M . Doublesex regulates fruitless expression to promote sexual dimorphism of the gonad stem cell niche. PLoS Genet. 2021; 17(3):e1009468. PMC: 8041189. DOI: 10.1371/journal.pgen.1009468. View

16.

Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, Nakata H . Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol. 2000; 2(8):500-6. DOI: 10.1038/35019537. View

17.

Just J, Laslo M, Lee Y, Yarnell M, Zhang Z, Angelini D . Distinct developmental mechanisms influence sexual dimorphisms in the milkweed bug . Proc Biol Sci. 2023; 290(1992):20222083. PMC: 9890105. DOI: 10.1098/rspb.2022.2083. View

18.

Salvemini M, Robertson M, Aronson B, Atkinson P, Polito L, 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(1):109-20. DOI: 10.1387/ijdb.082681ms. View

19.

Wheeler D, Fields W, Hall J . Spectral analysis of Drosophila courtship songs: D. melanogaster, D. simulans, and their interspecific hybrid. Behav Genet. 1988; 18(6):675-703. DOI: 10.1007/BF01066850. View

20.

Zhuo J, Xue J, Lu J, Huang H, Xu H, Zhang C . Effect of RNAi-mediated knockdown of NlTOR gene on fertility of male Nilaparvata lugens. J Insect Physiol. 2017; 98:149-159. DOI: 10.1016/j.jinsphys.2017.01.002. View