Organ-specific transcripts as a source of gene multifunctionality: lessons learned from the Drosophila melanogaster sbr (Dm nxf1) gene

  • Ludmila Mamon Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation
  • Viktoria Ginanova Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation
  • Sergey Kliver Theodosius Dobzhansky Center for Genome Bioinformatics, Saint Petersburg State University, Sredniy Pr., 41, Saint Petersburg, 199004, Russian Federation
  • Mariya Toropko Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation
  • Elena Golubkova Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation


Analysis of the transcriptomes of different organisms has demonstrated that a single gene can have multiple transcripts. The sources of transcriptional variability are the alternative promoters, polyadenylation sites, splicing, and RNA editing. A comparison of the organisms of different taxa has demonstrated that the complexity of organization during evolution arises not due to an increase in the number of protein-coding genes. The greatest variability of transcripts is specific to the nervous and germinal systems. A variety of mechanisms providing for the complexity of the transcriptome ensures a precise and coordinated regulation of organ-specific functions through a combination of cis-acting elements and trans-acting factors. The D. melanogaster sbr (Dm nxf1) gene has proven to be an excellent model for investigating mechanisms potentially leading to the emergence of multiple products with various functions.


nxf (nuclear export factor), D. melanogaster, alternative splicing, intron retention, transcriptional variability, alternative polyadenylation


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An, J. J., Gharami, K., Liao, G.-Y., Woo, N. H., Lau, A. G., Vanevski, F., Torre, E. R., Jones, K. R., Feng, Y., Lu, B., and Xu, B. 2008. Distinct role of long 3′UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134(1):175–187.

Barnard, D. C., Cao, Q., and Richter, J. D. 2005. Differential phosphorylation controls Maskin association with eukaryotic translation initiation factor 4E and localization on the mitotic apparatus. Molecular and Cellular Biology 25(17):7605–7615.

Beaudoing, E., Freier, S., Wyatt, J.R., Claverie, J.-M., and Gautheret, D. 2000. Patterns of variant polyadenylation signal usage in human genes. Genome Research 10:1001–1010.

Berkovits, B. D. and Mayr, C. 2015. Alternative 3´ UTRs act as scaffolds to regulate membrane protein localization. Nature 522:363–367.

Bicknell, A. A., Cenik, C., Chua, H. N., Roth, F. P., and Moore, M. J. 2012. Intron in UTRs: why we should stop ignoring them. Bioessays 34:1025–1034.

Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annual Review of Biochemistry 72:291–336.

Braunschweig, U., Barbosa-Morais, N. L., Pan, Q., Nachman, E. N., Alipanahi, B., Gonatopoulos-Pournatzis, T., Frey, B., Irimia, M., and Blencowe, B. J. 2014. Widespread intron retention in mammals functionally tunes transcriptomes. Genome Research 24:1774–1786.

Brown, J. B., Boley, N., Eisman, R., May, G. E., Stoiber, M. H., Duff, M. O., Booth, B. W., Wen, J., Park, S., Suzuki, A. M., Wan, K. H., Yu, C., Zhang, D., Carlson, J. W., Cherbas, L., Eads, B. D., Miller, D., Mockaitis, K., Roberts, J., Davis, C. A., Frise, E., Hammonds, A. S., Olson, S., Shenker, S., Sturgill, D., Samsonova, A. A., Weiszmann, R., Robinson, G., Hernandez, J., Andrews, J., Bickel, P. J., Carninci, P., Cherbas, P., Gingeras, T. R., Hoskins, R. A., Kaufman, T. C., Lai, E. C., Oliver, B., Perrimon, N., Graveley, B. R., and Celniker, S. E. 2014. Diversity and dynamics of the Drosophila transcriptome. Nature 512:393–399.

Child, S. J., Miller, M. K., and Geballe, A. P. 1999. Translational control by an upstream open reading frame in the HER-2/neu transcript. Journal of Biological Chemistry 274:24335–24341.

Colgan, D. F. and Manley, J. L. 1997. Mechanism and regulation of mRNA polyadenylation. Genes and Development 11:2755–2766.

Coll, O., Villalba, A., Bussotti, G., Notredame, C., and Gebauer, F. 2010. A novel, canonical mechanism of cytoplasmic polyadenylation operates in Drosophila embryogenesis. Genes and Development 24:129–134.

Cui, J., Sartain, C. V., Pleiss, J., and Wolfner, M. F. 2013. Cytoplasmic polyadenylation is a major mRNA regulator during oogenesis and egg activation in Drosophila. Developmental Biology 383:121–131.

Dass, B., Tardif, S., Park, J. Y., Tian, B., Weitlauf, H. M., Hess, R. A., Carnes, K., Griswold, M. D., Small, C. L., and MacDonald, C. C. 2007. Loss of polyadenylation protein τCstF-64 causes spermatogenic defects and male infertility. Proceeding of the National Academy of Science of USA 104:20374–20379.

Derti, A., Garrett-Engele, P., Maclsaac, K. D., Stevens, R. C., Sriram, S., Chen, R., Rohl, C. A., Johnson, J. M., and Babak, T. 2012. A quantitative atlas of polyadenylation in five mammals. Genome Research 22(6):1173–1183.

Detivaud, L., Pascreau, G., Karaiskou, A., Osborne, H. B., and Kubiak, J. Z. 2003. Regulation of EDEN-dependent deadenylation of Aurora A/Eg2-derived mRNA via phosphorylation and dephosphorylation in Xenopus laevis egg extracts. Journal of Cell Science 116:2697–2705.

Du, L. and Richter, J. D. 2005. Activity-dependent polyadenylation in neurons. RNA 11:340–1347.

Elkon, R., Drost, J., van Haaften, G., Jenal, M., Schrier, M., Oude Vrielink, J.A., and Agami, R. 2012. E2F mediates enhanced alternative polyadenylation in proliferation. Genome Biology 13:R59.

Erson-Bensan, A. E. 2016. Alternative polyadenylation and RNA-binding proteins. Journal of Molecular Endocrinology 57:F29–F34.

Evsikov, A. V. and de Evsikova, C. M. 2009. Gene expression during the oocyte-to-embryo transition in mammals. Molecular Reproduction and Development 76(9):805–818.

Evsikov, A. V., Graber, J. H., Brockman, J. M., Hampl, A., Holbrook, A. E., Singh, P., Eppig, J. J., Solter, D., and Knowles, B. B. 2006. Cracking the egg: molecular dynamics and evolutionary aspects of the transition from the fully grown oocyte to embryo. Genes and Development 20:2713–2727.

Flynt, A. S. and Lai, E. C. 2008. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nature Reviews Genetics 9:831–842.

Ginanova, V., Golubkova, E., Kliver, S., Bychkova, E., Markoska, K., Ivankova, N., Tretyakova, I., Evgen'ev, M., and Mamon, L. 2016. Testis-specific products of the Drosophila melanogaster sbr gene, encoding nuclear export factor 1, are necessary for male fertility. Gene 577:153–160.

Ginanova V. 2017. Variety and tissue-specific isoforms of the Nxf1 (nuclear export factor 1), a main factor of nuclear export of mRNA in Drosophila melanogaster. PhD thesis. St.-Petersburg.

Golubkova, E. V., Atsapkina, A. A., and Mamon, L. A. 2015. The role of sbr / Dm nxf1 gene in syncytial development in Drosophila melanogaster. Cell and Tissue Biology 9(4):271–283.

Golubkova, E. V. and Mamon, L. A. 2012. The role of Dm NXF1 in controlling early embryonic mitoses in Drosophila melanogaster. Encyclopedia of Cell Biology Research 543–549. Nova Science Publishers. Inc.

Graveley, B. R. 2001. Alternative splicing: increasing diversity in the proteomic world. Trends in Genetics 17:100–107.

Graveley, B. R. 2005. Mutually exclusive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures. Cell 123:65–73.

Guo, X., Gourronc, F., Audic, Y., Lyons-Levy, G., Mitchell, T., and Hartley, R. S. 2008. ElrA and AUF1 differentially bind cyclin B2 mRNA. Biochemical and Biophysical Research Communications 377:653–657.

Hawthorne, S. K., Busanelli, R. R., and Kleen, K. C. 2006. The 5´ UTR and 3´ UTR of the sperm mitochondria-associated cysteine-rich protein mRNA regulate translation in spermatids by multiple mechanisms in transgenic mice. Developmental Biology 297:118–126.

Herold, A., Klymenko, T., and Izaurralde, E. 2001. NXF1/ p15 heterodimers are essential for mRNA nuclear export in Drosophila. RNA 7:1768–1780.

Hilgers, V. 2015. Alternative polyadenylation coupled to transcription initiation: Insights from ELAV-mediated 3' UTR extension. RNA Biology 12(9):918–921.

Hilgers, V., Lemke, S. B., and Levine, M. 2012. ELAV mediates 3’ UTR extension in the Drosophila nervous system. Genes and Development 26:2259–2264.

Hilgers, V., Perry, M. W. Hednrix, D., Stark, A., Levine, M., and Haley, B. 2011. Neural-specific elongation of 3′ UTRs during Drosophila development. Proceeding of the National Academy of Science of USA 108:15864–15869.

Iguchi, N., Tobias, J. W., and Hecht, N. B. 2006. Expression profiling reveals meiotic male germ cell mRNAs that are translationally up- and down-regulated. Proceeding of the National Academy of Science of USA 103:7712–7717.

Ivankova, N., Tretyakova, I., Lyozin, G., Avanesyan, E., Zolotukhin, A., Zatsepina, O. G., Evgen’ev, M. B., and Mamon, L. A. 2010. Alternative transcripts expressed by small bristles, the Drosophila melanogaster nxf1 gene. Gene 458:11–19.

Iwakawa, H. O. and Tomari, Y. 2015. The functions of microRNAs: mRNA decay and translational repression. Trends in Cell Biology 25:651–665.

Jacob, A. G. and Smith, C. W. 2017. Intron retention as a component of regulated gene expression programs. Human Genetics 136:1043–1057.

Johnson, J. M., Castle, J., Garrett-Engele, P., Kan, Z., Loerch, P. M., Armour, C. D., Santos, R., Schadt, E. E., Stoughton, R., and Shoemaker, D. D. 2003. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302:2141–2144.

Jun, L., Frints, S., Duhamel, H., Herold, A., Abad-Rodrigues, J., Dotti, C., Izaurralde, E., Marynen, P., and Froyen, G. 2001. NXF5, a novel member of the nuclear RNA export factor family, is lost in a male patient with a syndromic form of mental retardation. Current Biology 11(18):1381–1391.

Kadonaga, J. T. 2012. Perspectives on the RNA polymerase II core promoter. Wiley Interdisciplinary Reviews-Developmental Biology 1(1):40–51.

Kadonaga, J. T. 2002. The DPE, a core promoter element for transcription by RNA polymerase II. Experimental and Molecular Medicine 34:259–264.

Kashiwabara, S., Zhuang, T., Yamagata, K., Noguchi, J., Fukamizu, A., and Baba, T. 2000. Identification of a novel isoform of poly(A) polymerase, TPAP, specifically present in the cytoplasm of spermatogenic cells. Developmental Biology 228:106–115.

Kashiwabara, S, Noguchi, J, Zhuang, T, Ohmura, K, Honda, A, Sugiura, S, Miyamoto, K, Takahashi, S, Inoue, K, Ogura, A, and Baba, T. 2002. Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science 298:1999–2002.

Kiseleva, E., Rutherford, S., Cotter, L. M., Allen, T. D., and Goldberg, M. W. 2001. Step of nuclear pore complex disassembly and reassembly during mitosis in early Drosophila embryos. Journal of Cell Science 114:3607–3618.

Kleene, K. C. 2001. A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mechanisms of Development 106:3–23.

Kleene, K. C. 2003. Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenetic and Genome Research 103:217–224.

Kopytova, D., Popova, V., Kurshakova, M., Shidlovskii, Y., Nabirochkina, E., Brechalov, A., Georgiev, G., and Georgieva, S. 2016. ORC interacts with THSC/TREX-2 and its subunits promote Nxf1 association with mRNP and mRNA export in Drosophila. Nucleic Acids Research 44:4920–4933.

Kumar, A. 2009. An overview of nested genes in eukaryotic genomes. Eukaryotic Cell 8:1321–1329.

Kundel, M., Jones, K. J., Shin, C. Y., and Wells, D. G. 2009. Cytoplasmic polyadenylation element binding protein regulates neurotrophin 3-dependent β-catenin mRNA translation in developing hippocampal neurons. Journal of Neuroscience 29:13630–13639.

Li, J. and Gilmour, D.S. 2013. Distinct mechanisms of transcriptional pausing orchestrated by GAGA factor and M1BP, a novel transcription factor. The EMBO Journal 32:1829–1841.

Li, W., Park, J.Y. Zheng, D., Hoque, M. Yehia, G., and Tian, B. 2016. Alternative cleavage and polyadenylation in spermatogenesis connects chromatin regulation with post-transcriptional control. BMC Biology 14:6.

Li, Y., Bor, Y. C., Fitzgerald, M. P., Lee, K. S., Rekosh, D., and Hammarskjold, M. L. 2016. An NXF1 mRNA with a retained intron is expressed in hippocampal and neocortical neurons and is translated into a protein that functions as an Nxf1 cofactor. Molecular Biology of the Cell 27:3903–3912.

Li, Y., Bor, Y. C., Misawa, Y., Xue, Y., Rekosh, D., and Hammarskjöld, M. L. 2006. An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature 443:234–237.

Liu, D., Brockman, J. M., Dass, B., Hutchins, L. N., Singh, P., McCarrey, J. R., MacDonald, C. C., and Graber, J. H. 2007. Systematic variation in mRNA 3'-processing signals during mouse spermatogenesis. Nucleic Acids Research 35:234–246.

Lόpez de Salines, I., Zhan, M., Lal, A., Yang, X., and Gorospe, M. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proceeding of the National Academy of Science of USA 101:2987–2992.

Lund, E., Liu, M., Hartley, R. S., Sheets, M. D., and Dahlberg, J. S. 2009. Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos. RNA 15:2351–2363.

MacDonald, C. C. and McMahon, K. W. 2010. Tissue-specific mechanisms of alternative polyadenylation: testis, brain, and beyond. Wiley Interdisciplinary Reviews-RNA 1:494–501.

MacDonald, C. C., Wilusz, J., and Shenk, T. 1994. The 64-kilodalton subunit of the CstF polyadenylation factor binds to pre-mRNAs downstream of the cleavage site and influences cleavage site location. Molecular and Cellular Biology 14:6647–6654.

Mamon, L. A., Kliver, S. F., and Golubkova, E. V. 2013. Evolutionarily conserved features of the retained intron in alternative transcripts of the nxf1 (Nuclear eXport Factor) genes in different organisms. Open Journal of Genetics 3:159–170.

Mamon, L. A., Kliver, S. F., Prosovskaya, A. O., Ginanova, V. R., and Golubkova, Ye. V. 2014. The intron-containing transcript: an evolutionarily conserved characteristic of the genes orthologous to nxf1 (nuclear export factor 1). Russian Journal of Genetics and Applied Research 4(5):434–443.

Mamon, L. A., Ginanova, V. R., Kliver, S. F., Yakimova, A. O., Atsapkina, A. A., and Golubkova, E. V. 2017. RNA-binding proteins of the NXF (nuclear export factor) family and their connection with the cytoskeleton. Cytoskeleton 74:161–169.

Medenbach, J., Seiler, M., and Hentze, M. W. 2011. Translational control via protein-regulated upstream open reading frames. Cell 145:902–913.

Mitra, M., Johnson, E. L., and Coller, H. A. 2015. Alternative polyadenylation can regulate post-translational membrane localization. Trends in Cell and Molecular Biology 10:37–47.

Miura, P., Sanfilippo, P., Shenker, S., and Lai, E. C. 2014. Alternative polyadenylation in the nervous system: to what lengths with 3´ UTR extensions take us? BioEssays 36:766–777.

Miura, P., Shenker, S., Andreu-Agullo, C., Westholm, J. O., and Lai, E. C. 2013. Widespread and extensive lengthening of 3´ UTRs in the mammalian brain. Genome Research 23:812–825.

Neilson, J. R. and Sandberg, R. 2010. Heterogeneity in mammalian RNA 3′ end formation. Experimental Cell Research 316:1357–1364.

Neve, J., Patel, R., Wang, Z., Louey, A., and Furger, A. M. 2017. Cleavage and polyadenylation: Ending the message expands gene regulation: Ending the message expands gene regulation. RNA Biology 14:865–890.

Nilsen, T. W. and Graveley, B. R. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457–463.

Oktaba, K., Zhang, W., Lotz, T. S., Jun, D. J., Lemke, S. B., Ng, S. P., Esposito, E., Levine, M., and Hilgers, V. 2015. ELAV links paused Pol II to alternative polyadenylation in the Drosophila nervous system. Molecular Cell 57(2):341–348.

Perales, R. and Bentley, D. 2009. “Co-transcriptionality” – the transcription elongation complex as a nexus for nuclear transactions. Molecular Cell 36:178–191.

Proudfoot, N. J. 2011. Ending the message: poly(A) signals then and now. Genes and Development 25:1770–1782.

Richter, J. D. 1996. Dynamics of poly(A) addition and removal during development. pp 481-503 in J.W.B. Hershey, M.B. Mathews, and N. Sonenberg (eds) “Translational control”. Cold Spring Harbor Laboratory Press. Plainview. NY.

Richter, J. D. and Sonenberg, N. 2005. Regulation of cap-dependent translation by elF4E inhibitory proteins. Nature 433:477–480.

Sanfilippo, P., Wen, J., and Lai, E. C. 2017. Landscape and evolution of tissue-specific alternative polyadenylation across Drosophila species. Genome Biology 18:229.

Sasaki, M., Takeda, E., and Takano, K. 2005. Molecular cloning and functional characterization of mouse Nxf family gene products. Genomics 85:641–653.

Schmitz, U., Pinello, N., Jia, F., Alasmari, S., Ritchie, W., Keightley, M.-C., Shini, S., Lieschke, G. J., Wong, J. J.-L., and Rasko, J. E. J. 2017. Intron retention enhances gene regulatory complexity in vertebrates. Genome Biology 18:216.

Schmucker, D., Clemens, J. C., Shu, H., Worby, C. A., Xiao, J., Muda, M., Dixon, J. E., and Zipursky, S. L. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–684.

Schultz, R. M., Stein, P., and Svoboda, P. 2018. The oocyte to embryo transition in mouse: past, present, and future. Biology of Reproduction 99:160–174.

Smibert, P., Miura, P., Westholm, J. O., Shenker, S., May, G., Duff, M. O., Zhang, D., Eads, B. D., Carlson, J., Brown, J. B., Eisman, R. C., Andrews, J., Kaufman, T., Cherbas, P., Celniker, S. E., Graveley, B. R., and Lai, E. C. 2012. Global patterns of tissue-specific alternative polyadenylation in Drosophila. Cell Reports 1:277–289.

Sridharan V., Heimiller J., Robida M. D., and Singh, R. 2016. High throughput sequencing identifies misregulated genes in the Drosophila polypyrimidine tract-binding protein (hephaestus) mutant defective in spermatogenesis. PLoS One 11(3):e0150768.

Stafstrom, J. P. and Staehelin, L. A. 1984. Dynamics of the nuclear envelope and of nuclear pore complexes during mitosis in the Drosophila embryo. European Journal of Cell Biology 34:179–189.

Svoboda, P., Franke, V., and Schultz, R. M. 2015. Chapter Nine - Sculpting the Transcriptome During the Oocyte-to-Embryo Transition in Mouse. Current Topics in Developmental Biology 113:305–349.

Szostak, E. and Gebauer, F. 2012. Translational control by 3´ -UTR-binding proteins. Briefings Functional Genomics 12:58–65.

Tadros, W. and Lipshitz, H. D. 2009. The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042.

Tay, J. and Richter, J. D. 2001. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Developmental Cell 1:201–213.

Tian, B., Hu, J., Zhang, H., and Lutz, C. S. 2005. A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Research 33:201–212.

Tretyakova, I., Zolotukhin, A. S., Tan, W., Bear, J., Propst, F., Rothler, G., and Fleber, B. K. 2005. Nuclear export factor family protein participates in cytoplasmic mRNA trafficking. Journal of Biological Chemistry 280(36):31981–31990.

Tuck, A. C. and Tollervey, D. 2011. RNA in pieces. Trends in Genetics 27:422–432.

Vacik, T. and Raska, I. 2017. Alternative intronic promoters in development and disease. Protoplasma 254:1201–1206.

Voeltz, G. K. and Steitz, J. A. 1998. AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Molecular and Cellular Biology 18:7537–7545.

Wallace, A. M., Dass, B., Ravnik, S. E., Tonk, V., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., and MacDonald, C. C. 1999. Two distinct forms of the 64,000 Mr protein of the cleavage stimulation factor are expressed in mouse male germ cells. Proceeding of the National Academy of Science of USA 96:6763–6768.

Wang, B., Rekosh, D., and Hammarskjold, M.-L. 2015. Evolutionary conservation of machinery for export and expression of mRNAs with retained introns. RNA 21:1–12.

Wang, E. T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P., and Burge, C. B. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476.

Wells, S. E., Hillner, P. E., Vale, R. D., and Sachs, A. B. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Molecular Cell 2:135–140.

White, E. J. F., Brewer, G., and Wilson, G. M. 2013. Post-transcriptional control of gene expression by AUF1: Mechanisms, physiological targets, and regulation. Biochimica et Biophysica Acta 1829:680–688.

Xu, M., Gonzalez-Hurtado, E., and Martinez, E. 2016. Core promoter-specific gene regulation: TATA box selectivity and Initiator-dependent bi-directionality of serum response factor activated transcription. Biochimica et Biophysica Acta 1859:553–563.

Yang, J., Bogert, H. P., Wang, P. J., Page, D. C., and Cullen B. R. 2001. Two closely related human nuclear export factors utilize entirely distinct export pathways. Molecular Cell 8:397–406.

Zhou, J., Pan, J., Eckardt, S., Leu, N. A., McLaughlin, K. J., and Wang, P. J. 2011. Nxf3 is expressed in Sertoli cells, but is dispensable for spermatogenesis. Molecular Reproduction and Development 78(4):241–249.

How to Cite
Mamon, L., Ginanova, V., Kliver, S., Toropko, M., & Golubkova, E. (2019). Organ-specific transcripts as a source of gene multifunctionality: lessons learned from the <em>Drosophila melanogaster sbr</em> (<em>Dm nxf1</em&gt;) gene. Biological Communications, 64(2), 146–157.
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