期刊论文详细信息
BMC Developmental Biology
The gene transformer-2 of Sciara (Diptera, Nematocera) and its effect on Drosophila sexual development
Lucas Sánchez2  María F Ruiz1  Iker Martín1 
[1] Centro de Investigaciones Biológicas (C.S.I.C.), Ramiro de Maeztu 9, 28040 Madrid, Spain;NEIKER-TEKNALIA, Berreaga 1, 48160-Derio, Vizcaya, Spain
关键词: transformer-2 gene;    sex determination;    Sciara;   
Others  :  1126142
DOI  :  10.1186/1471-213X-11-19
 received in 2010-11-02, accepted in 2011-03-15,  发布年份 2011
PDF
【 摘 要 】

Background

The gene transformer-2, which is involved in sex determination, has been studied in Drosophila, Musca, Ceratitis, Anastrepha and Lucilia. All these members of Diptera belong to the suborder Brachycera. In this work, it is reported the isolation and characterisation of genes transformer-2 of the dipterans Sciara ocellaris and Bradysia coprophila (formerly Sciara coprophila), which belong to the much less extensively analysed Sciaridae Family of the Suborder Nematocera, which is paraphyletic with respect to Suborder Brachycera.

Results

The transformer-2 genes of the studied Sciara species were found to be transcribed in both sexes during development and adult life, in both the soma and germ lines. They produced a single primary transcript, which follows the same alternative splicing in both sexes, giving rise to different mRNAs isoforms. In S. ocellaris the most abundant mRNA isoform encoded a full-length protein of 251 amino acids, while that of B. coprophila encoded a protein of 246 amino acids. Both showed the features of the SR protein family. The less significant mRNA isoforms of both species encoded truncated, presumably non-functional Transformer-2 proteins. The comparison of the functional Sciara Transformer-2 proteins among themselves and those of other insects revealed the greatest degree of conservation in the RRM domain and linker region. In contrast, the RS1 and RS2 domains showed extensive variation with respect to their number of amino acids and their arginine-serine (RS) dipeptide content. The expression of S. ocellaris Transformer-2 protein in Drosophila XX pseudomales lacking the endogenous transformer-2 function caused their partial feminisation.

Conclusions

The transformer-2 genes of both Sciaridae species encode a single protein in both sexes that shares the characteristics of the Transformer-2 proteins of other insects. These proteins showed conserved sex-determination function in Drosophila; i.e., they were able to form a complex with the endogenous Drosophila Transformer protein that controls the female-specific splicing of the Drosophila doublesex pre-mRNA. However, it appears that the complex formed between the Drosophila Transformer protein and the Sciara Transformer-2 protein is less effective at inducing the female-specific splicing of the endogenous Drosophila doublesex pre-mRNA than the DrosophilaTransformer-Transformer2 complex. This suggests the existence of species-specific co-evolution of the Transformer and Transformer-2 proteins.

【 授权许可】

   
2011 Martín et al; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150218075542565.pdf 1208KB PDF download
Figure 6. 42KB Image download
Figure 5. 63KB Image download
Figure 4. 303KB Image download
Figure 3. 56KB Image download
Figure 2. 31KB Image download
Figure 1. 62KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】
  • [1]Sánchez L, Gorfinkiel N, Guerrero I: Sex determination and the development of the genital disc. In Comprehensive Molecular Insect Science. Volume 1. Edited by Gilbert LI, Iatrou K, Gill SS. Oxford: Elsevier Pergamon; 2005::1-38.
  • [2]Bell LR, Maine EM, Schedl P, Cline TW: Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similar to RNA binding proteins. Cell 1988, 55:1037-1046.
  • [3]Bell LR, Horabin JI, Schedl P, Cline TW: Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 1991, 65:229-239.
  • [4]Boggs RT, Gregor P, Idriss S, Belote JM, McKeown M: Regulation of sexual differentiation in Drosophila melanogaster via alternative splicing of RNA from the transformer gene. Cell 1987, 50:739-747.
  • [5]Belote JM, McKeown M, Boggs RT, Ohkawa R, Sosnowski BA: The molecular genetics of transformer, a genetic switch-controlling sexual differentiation in Drosophila. Devel Genet 1989, 10:143-154.
  • [6]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.
  • [7]Hedley M, Maniatis T: Sex-specific splicing and polyadenylation of dsx pre-mRNA requires a sequence that binds specifically to tra-2 protein in vitro. Cell 1991, 65:579-586.
  • [8]Hertel KJ, Lynch KW, Hsiao EC, Liu EHT, Maniatis T: Structural and functional conservation of the Drosophila doublesex splicing enhancer repeat elements. RNA 1996, 2:969-981.
  • [9]Ryner LC, Baker BS: Regulation of doublesex pre-mRNA processing occurs by 3'-splice site activation. Genes Dev 1991, 5:2071-2085.
  • [10]Tian M, Maniatis T: A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell 1993, 74:105-114.
  • [11]Burtis KC, Baker BS: Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 1989, 56:997-1010.
  • [12]Hoshijima K, Inoue K, Higuchi I, Sakamoto H, Shimura Y: Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 1991, 252:833-836.
  • [13]Sánchez L: Sex-determining mechanisms in insects. Int J Dev Biol 2008, 52:1059-1075.
  • [14]Gempe T, Beye M: Function and evolution of sex determination mechanisms, genes and pathways in insects. BioEssays 2010, 33:52-60.
  • [15]Verhulst EC, van de Zande L, Beukeboom LW: Insect sex determination: it all evolves around transformer. Curr Opin Gene Devel 2010, 20:1-8.
  • [16]Ruiz MF, Goday C, González P, Sánchez L: Molecular analysis and developmental expression of the Sex-lethal gene of Sciara ocellaris (Diptera Order, Nematocera Suborder). Gene Expr Patt 2003, 3:341-346.
  • [17]Serna E, Gorab E, Ruiz MF, Goday C, Eirín-López JM, Sánchez L: The gene Sex-lethal of the Sciaridae family (Order Diptera, Suborder Nematocera) and its phylogeny in dipteran insects. Genetics 2004, 168:907-921.
  • [18]Chandler D, McGuffin M, Piskur J, Yao J, Baker B, Mattox W: Evolutionary conservation of regulatory strategies for the sex determination factor transformer-2. Mol Cell Biol 1997, 17:2908-2919.
  • [19]Burghardt G, Hediger M, Siegenthaler C, Moser M, Dübendorfer A, Bopp D: The transformer-2 gene in Musca domestica is required for selecting and maintaining the female pathway of development. Dev Genes Evol 2005, 215:165-176.
  • [20]Gomulski LM, Dimopoulos G, Xi Z, Soares MB, Bonaldo MF, Malacrida AR, Gasperi G: Gene discovery in an invasive tephritid model pest species, the Mediterranean fruit fly, Ceratitis capitata. BMC Genetics 2008, 9:243.
  • [21]Salvemini M, Robertson M, Aronson B, Atkinson P, Polito C, 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.
  • [22]Sarno F, Ruiz MF, Eirín-López JM, Perondini ALP, Selivon D, Sánchez L: The gene transformer-2 of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. BMC Evolutionary Biology 2010, 10:140. BioMed Central Full Text
  • [23]Concha C, Scott MJ: Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 2009, 182:785-789.
  • [24]Niu BL, Meng ZQ, Tao YZ, Lu SL, Weng HB, He LH, Shen WF: Cloning and alternative splicing analysis of Bombyx mori transformer-2 gene using silkworm EST database. Acta Biochim Biophys 2005, 37:728-736.
  • [25]Hediger M, Henggeler C, Meier N, Pérez R, Saccone G, Bopp D: Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 2010, 184:155-170.
  • [26]Dübendorfer A, Hediger M, Burghardt G, Bopp D: Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 2002, 46:75-79.
  • [27]Amrein H, Maniatis T, Nöthiger R: Alternatively spliced transcripts of the sex determining gene tra-2 of Drosophila encode functional proteins of different size. EMBO J 1990, 9:3619-3629.
  • [28]Mattox W, Palmer MJ, Baker BS: Alternative splicing of the sex determination gene transformer-2 is sex-specific in the germ line but not in the soma. Genes Dev 1990, 4:789-805.
  • [29]Dauwalder B, Amaya-Manzanares F, Mattox W: A human homologue of the Drosophila sex determination factor transformer-2 has conserved splicing regulatory functions. Proc Natl Acad Sci USA 1996, 93:9004-9009.
  • [30]McAllister BF, McVean GAT: Neutral evolution of the sex-determining gene transformer in Drosophila. Genetics 2000, 154:1711-1720.
  • [31]Qi J, Su S, McGuffin ME, Mattox W: Concentration dependent selection of targets by an SR splicing regulator results in tissue-specific RNA processing. Nucl Acids Res 2006, 34:6256-6263.
  • [32]St Pierre SE, Galindo MI, Couso JP, Thor S: Control of Drosophila imaginal disc development by rotund and roughened eye: differentially expressed transcripts of the same encoding functionally distinct zinc finger proteins. Development 2002, 129:1273-1281.
  • [33]Ramos-Onsins S, Segarra C, Rozas J, Aguadé M: Molecular and chromosomal phylogeny in the obscura group of Drosophila inferred from sequences of the rp49 gene region. Mol Phylo Evol 1998, 9:33-41.
  • [34]Black DL: Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 2003, 72:291-336.
  • [35]Ruiz MF, Sánchez L: Effect of the gene transformer of Anastrepha on the somatic sexual development of Drosophila. Int J Dev Biol 2010, 54:627-633.
  • [36]Lindsley DL, Zimm G: The genome of Drosophila melanogaster. San Diego, California. Academic Press; 1992.
  • [37]Cho Ng, Kopp A: Sex combs are important for male mating success in Drosophila melanogaster. Behav Genet 2008, 38:195-201.
  • [38]McGuire SE, Le PH, Osborn AJ, Matsumoto K, Davis RL: Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003, 302:1765-1768.
  • [39]Maniatis T, Fritsch F, Sambrook J: Molecular cloning. New York: Cold Spring Harbor Laboratory; 1982.
  文献评价指标  
  下载次数:207次 浏览次数:21次