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The β2Tubulin, Rad50-ATPase and enolase cis-regulatory regions mediate male germline expression in Tribolium castaneum

  • 1.

    Pretty, J. & Bharucha, Z. P. Integrated pest management for sustainable intensification of agriculture in Asia and Africa. Insects 6, 152–182. https://doi.org/10.3390/insects6010152 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 2.

    Klassen, W. & Curtis, C. F. History of the sterile insect technique. In Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (eds Dyck, V. A. et al.) 3–36 (Springer, 2005).

    Chapter 

    Google Scholar 

  • 3.

    Papathanos, P. A. et al. Sex separation strategies: Past experience and new approaches. Malar. J. https://doi.org/10.1186/1475-2875-8-s2-s5 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 4.

    Benedict, M. Q. & Robinson, A. S. The first releases of transgenic mosquitoes: An argument for the sterile insect technique. Trends Parasitol. 19, 349–355. https://doi.org/10.1016/s1471-4922(03)00144-2 (2003).

    Article 
    PubMed 

    Google Scholar 

  • 5.

    Alphey, L. et al. Sterile-insect methods for control of mosquito-borne diseases: An analysis. Vector-Borne Zoonotic Dis. 10, 295–311. https://doi.org/10.1089/vbz.2009.0014 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 6.

    Kandul, N. P. et al. Transforming insect population control with precision guided sterile males with demonstration in flies. Nat. Commun. https://doi.org/10.1038/s41467-018-07964-7 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 7.

    Ahmed, H. M. M., Hildebrand, L. & Wimmer, E. A. Improvement and use of CRISPR/Cas9 to engineer a sperm-marking strain for the invasive fruit pest Drosophila suzukii. BMC Biotechnol. https://doi.org/10.1186/s12896-019-0588-5 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 8.

    Yan, Y. & Scott, M. J. A transgenic embryonic sexing system for the Australian sheep blow fly Lucilia cuprina. Sci. Rep. https://doi.org/10.1038/srep16090 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 9.

    Papathanos, P. A., Windbichler, N., Menichelli, M., Burt, A. & Crisanti, A. The vasa regulatory region mediates germline expression and maternal transmission of proteins in the malaria mosquito Anopheles gambiae: A versatile tool for genetic control strategies. Bmc Mol. Biol. https://doi.org/10.1186/1471-2199-10-65 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Schroder, R. vasa mRNA accumulates at the posterior pole during blastoderm formation in the flour beetle Tribolium castaneum. Dev. Genes Evol. 216, 277–283. https://doi.org/10.1007/s00427-005-0054-3 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 11.

    Michiels, F., Gasch, A., Kaltschmidt, B. & Renkawitzpohl, R. A 14-bp promoter element directs the testis specificity of the Drosophila-beta-2 tubulin gene. Embo J. 8, 1559–1565. https://doi.org/10.1002/j.1460-2075.1989.tb03540.x (1989).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    Smith, R. C., Walter, M. F., Hice, R. H., O’Brochta, D. A. & Atkinson, P. W. Testis-specific expression of the beta 2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker. Insect Mol. Biol. 16, 61–71. https://doi.org/10.1111/j.1365-2583.2006.00701.x (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 13.

    Xu, J. et al. Transgenic characterization of two testis-specific promoters in the silkworm, Bombyx mori. Insect Mol. Biol. 24, 183–190. https://doi.org/10.1111/imb.12144 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 14.

    Schetelig, M. F. & Handler, A. M. A transgenic embryonic sexing system for Anastrepha suspensa (Diptera: Tephritidae). Insect Biochem. Mol. 42, 790–795. https://doi.org/10.1016/j.ibmb.2012.07.007 (2012).

    CAS 
    Article 

    Google Scholar 

  • 15.

    Kemphues, K. J., Kaufman, T. C., Raff, R. A. & Raff, E. C. The testis specific beta tubulin subunit I Drosophila melanogaster has multiple functions in spermatogenesis. Cell 31, 655–670. https://doi.org/10.1016/0092-8674(82)90321-x (1982).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 16.

    Fackenthal, J. D., Turner, F. R. & Raff, E. C. Tissue-specific microtubule functions in Drosophila spermatogenesis require the β2-tubulin isotype-specific carboxy terminus. Dev. Biol. 158, 213–227 (1983).

    Article 

    Google Scholar 

  • 17.

    Kemphues, K. J., Raff, E. C., Raff, R. A. & Kaufman, T. C. Mutation in a testis-specific β-tubulin in Drosophila: Analysis of its effects on meiosis and map location of the gene. Cell 21, 445–451. https://doi.org/10.1016/0092-8674(80)90481-x (1980).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 18.

    Whitworth, C., Jimenez, E. & Van Doren, M. Development of sexual dimorphism in the Drosophila testis. Spermatogenesis 2, 129–136 (2012).

    Article 

    Google Scholar 

  • 19.

    Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell 134, 25–36. https://doi.org/10.1016/j.cell.2008.06.030 (2008).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 20.

    Yamamoto, D. S. et al. A synthetic male-specific sterilization system using the mammalian pro-apoptotic factor in a malaria vector mosquito. Sci. Rep. https://doi.org/10.1038/s41598-019-44480-0 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 21.

    Harvey-Samuel, T., Ant, T. & Alphey, L. Towards the genetic control of invasive species. Biol. Invas. 19, 1683–1703. https://doi.org/10.1007/s10530-017-1384-6 (2017).

    Article 

    Google Scholar 

  • 22.

    Scott, M. J., Concha, C., Welch, J. B., Phillips, P. L. & Skoda, S. R. Review of research advances in the screwworm eradication program over the past 25 years. Entomol. Exp. Appl. 164, 226–236. https://doi.org/10.1111/eea.12607 (2017).

    Article 

    Google Scholar 

  • 23.

    Scolari, F. et al. Fluorescent sperm marking to improve the fight against the pest insect Ceratitis capitata (Wiedemann; Diptera: Tephritidae). New Biotechnol. 25, 76–84. https://doi.org/10.1016/j.nbt.2008.02.001 (2008).

    CAS 
    Article 

    Google Scholar 

  • 24.

    Scolari, F. et al. Polyandry in the medfly—Shifts in paternity mediated by sperm stratification and mixing. BMC Genet. 15, S10. https://doi.org/10.1186/1471-2156-15-s2-s10 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25.

    Hunt, T. et al. A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science 318, 1913–1916. https://doi.org/10.1126/science.1146954 (2007).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 26.

    Slipinski, S. A., Leschen, R. A. B. & Lawrence, J. F. Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148, 1–237 (2011).

    Article 

    Google Scholar 

  • 27.

    Herndon, N. et al. Enhanced genome assembly and a new official gene set for Tribolium castaneum. BMC Genomics. https://doi.org/10.1186/s12864-019-6394-6 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 28.

    Richards, S. et al. The genome of the model beetle and pest Tribolium castaneum. Nature 452, 949–955. https://doi.org/10.1038/nature06784 (2008).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 29.

    Doenitz, J., Gerischer, L., Hahnke, S., Pfeiffer, S. & Bucher, G. Expanded and updated data and a query pipeline for iBeetle-Base. Nucleic Acids Res. 46, D831–D835. https://doi.org/10.1093/nar/gkx984 (2018).

    CAS 
    Article 

    Google Scholar 

  • 30.

    Schmitt-Engel, C. et al. The iBeetle large-scale RNAi screen reveals gene functions for insect development and physiology. Nat. Commun. https://doi.org/10.1038/ncomms8822 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 31.

    Johnathan, C. et al. Expanding the genetic toolkit of Tribolium castaneum. PLoS ONE 13, e0195977. https://doi.org/10.1371/journal.pone.0195977 (2018).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Lai, Y. T. et al. Enhancer identification and activity evaluation in the red flour beetle, Tribolium castaneum. Development. https://doi.org/10.1242/dev.160663 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 33.

    Gilles, A. F., Schinko, J. B. & Averof, M. Efficient CRISPR-mediated gene targeting and transgene replacement in the beetle Tribolium castaneum. Development 142, 2832. https://doi.org/10.1242/dev.125054 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 34.

    Brown, S. J. et al. The red flour beetle, Tribolium castaneum (Coleoptera): a model for studies of development and pest biology. Cold Spring Harb. Protoc. 2009(8), pdb.emo126. https://doi.org/10.1101/pdb.emo126 (2009).

  • 35.

    Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343. https://doi.org/10.1038/nmeth.1318 (2009).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 36.

    Horn, C. & Wimmer, E. A. A versatile vector set for animal transgenesis. Dev. Genes. Evol. 210, 630–637. https://doi.org/10.1007/s004270000110 (2000).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 37.

    Handler, A. M. & Harrell, R. A. Germline transformation of Drosophila melanogaster with the piggyBac transposon vector. Insect Mol. Biol. 8, 449–457. https://doi.org/10.1046/j.1365-2583.1999.00139.x (1999).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 38.

    Ochman, H., Gerber, A. S. & Hartl, D. L. Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621–623 (1988).

    CAS 
    Article 

    Google Scholar 

  • 39.

    Khan, S. A., Eggleston, H., Myles, K. M. & Adelman, Z. N. Differentially and co-expressed genes in embryo, germ-line and somatic tissues of Tribolium castaneum. G3: Genes Genomes Genet. 9, 2363. https://doi.org/10.1534/g3.119.400340 (2019).

    CAS 
    Article 

    Google Scholar 

  • 40.

    Williams, G. J. et al. ABC ATPase signature helices in Rad50 link nucleotide state to Mre11 interface for DNA repair. Nat. Struct. Mol. Biol. 18, 423–431 (2011).

    CAS 
    Article 

    Google Scholar 

  • 41.

    Gerlt, J. A., Babbitt, P. C. & Rayment, I. Divergent evolution in the enolase superfamily: The interplay of mechanism and specificity. Arch. Biochem. Biophys. 433, 59–70. https://doi.org/10.1016/j.abb.2004.07.034 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 42.

    Lorenzen, M. D. et al. piggyBac-mediated germline transformation in the beetle Tribolium castaneum. Insect Mol. Biol. 12, 433–440. https://doi.org/10.1046/j.1365-2583.2003.00427.x (2003).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Beeman, R. W., Haas, S. & Friesen, K. Stored Product Insect and Engineering Research (2019). http://www.ars.usda.gov/Research/docs.htm?docid=12892. Accessed 15 May 2021.

  • 44.

    Catteruccia, F., Benton, J. P. & Crisanti, A. An Anopheles transgenic sexing strain for vector control. Nat. Biotechnol. 23, 1414–1417. https://doi.org/10.1038/nbt1152 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 45.

    Salazar, K., Dias, G., Boucher, S., Lino-Neto, J. & Serrao, J. E. Morpho-anatomy of the male reproductive tract and spermatogenesis of the South American Spasalus silvarum Kuwert (Coleoptera: Passalidae). Zoomorphology 135, 487–497. https://doi.org/10.1007/s00435-016-0321-z (2016).

    Article 

    Google Scholar 

  • 46.

    Handel, K., Basal, A., Fan, X. & Roth, S. Tribolium castaneum twist: Gastrulation and mesoderm formation in a short-germ beetle. Dev. Genes Evol. 215, 13–31. https://doi.org/10.1007/s00427-004-0446-9 (2005).

    Article 
    PubMed 

    Google Scholar 

  • 47.

    Wolff, C., Schroder, R., Schulz, C., Tautz, D. & Klingler, M. Regulation of the Tribolium homologues of caudal and hunchback in Drosophila: Evidence for maternal gradient systems in a short germ embryo. Development 125, 3645–3654 (1998).

    CAS 
    Article 

    Google Scholar 

  • 48.

    Eckert, C., Aranda, M., Wolff, C. & Tautz, D. Separable stripe enhancer elements for the pair-rule gene hairy in the beetle Tribolium. Embo Rep. 5, 638–642. https://doi.org/10.1038/sj.embor.7400148 (2004).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 49.

    Schroder, R., Eckert, C., Wolff, C. & Tautz, D. Conserved and divergent aspects of terminal patterning in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. U.S.A. 97, 6591–6596. https://doi.org/10.1073/pnas.100005497 (2000).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Schinko, J. B., Hillebrand, K. & Bucher, G. Heat shock-mediated misexpression of genes in the beetle Tribolium castaneum. Dev. Genes Evol. 222, 287–298. https://doi.org/10.1007/s00427-012-0412-x (2012).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 51.

    Siebert, K. S., Lorenzen, M. D., Brown, S. J., Park, Y. & Beeman, R. W. Tubulin superfamily genes in Tribolium castaneum and the use of a Tubulin promoter to drive transgene expression. Insect Biochem. Mol. 38, 749–755. https://doi.org/10.1016/j.ibmb.2008.04.007 (2008).

    CAS 
    Article 

    Google Scholar 

  • 52.

    Lorenzen, M. D., Brown, S. J., Denell, R. E. & Beeman, R. W. Transgene expression from the Tribolium castaneum Polyubiquitin promoter. Insect Mol. Biol. 11, 399–407. https://doi.org/10.1046/j.1365-2583.2002.00349.x (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 53.

    Kemphues, K. J., Raff, E. C., Raff, R. A. & Kaufman, T. C. Mutation in a Testis-specific beta tubulin in Drosophila analysis of its effect of meiosis and map location of gene. Cell 21, 445–451. https://doi.org/10.1016/0092-8674(80)90481-x (1980).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 54.

    Kemphues, K. J., Kaufman, T. C., Raff, R. A. & Raff, E. C. The testis specific beta tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell 31, 655–670. https://doi.org/10.1016/0092-8674(82)90321-x (1982).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 55.

    Gelbart, W. M. & Emmert, D. B. FlyBase High Throughput Expression Pattern Data (2013).

  • 56.

    Hopfner, K. P. et al. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789–800. https://doi.org/10.1016/s0092-8674(00)80890-9 (2000).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 57.

    Hu, M. H. et al. Decreased expression of MRE11 and RAD50 in testes from humans with spermatogenic failure. J. Assist. Reprod. Genet. 37, 331–340. https://doi.org/10.1007/s10815-019-01686-5 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 58.

    Lange, J. et al. The landscape of mouse meiotic double-strand break formation, processing, and repair. Cell 167, 695. https://doi.org/10.1016/j.cell.2016.09.035 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 59.

    Gunes, S., Al-Sadaan, M. & Agarwal, A. Spermatogenesis, DNA damage and DNA repair mechanisms in male infertility. Reprod. Biomed. Online 31, 309–319. https://doi.org/10.1016/j.rbmo.2015.06.010 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 60.

    Sun, C., Xu, B., Liu, X., Zhang, Z. & Su, Z. Crystal structure of enolase from Drosophila melanogaster. Acta Crystallogr. Sect. F Struct. Biol. Commun. 73, 228–234. https://doi.org/10.1107/s2053230x17004022 (2017).

    CAS 
    Article 

    Google Scholar 

  • 61.

    Kikuchi, A. et al. Identification of functional enolase genes of the silkworm Bombyx mori from public databases with a combination of dry and wet bench processes. BMC Genomics. https://doi.org/10.1186/s12864-016-3455-y (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 62.

    Yan, Y., Schwirz, J. & Schetelig, M. F. Characterization of the Drosophila suzukii β2-tubulin gene and the utilization of its promoter to monitor sex separation and insemination. Gene 771, 145366. https://doi.org/10.1016/j.gene.2020.145366 (2021).

    CAS 
    Article 
    PubMed 

    Google Scholar 

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