Iranian Journal of Plant Protection Science

Iranian Journal of Plant Protection Science

Generation of transgenic lines for studying of the brain development in Tribolium castaneum (Coleoptera: Tenebrionidae)

Document Type : Research Paper

Authors
Mahdiyeh Bigham 1
Vahid Hosseininaveh 2
Hossein Allahyari 2
1 Ph.D. Student , Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
2 Associate Professor, Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran
10.22059/ijpps.2015.57376
Abstract
Germ-line transformation of insects is now widely used for analyzing gene function and for the development of genetically modified strains for various purposes. There is not enough information on the embryonic development of some brain parts in insects. In order to study the genetic control of embryonic brain development, we established some transgenic lines to identify some genes involved in embryonic brain development. The genome has been sequenced and transgenic approaches are established for this model organism. Transposable element piggyBac was used as a vector for the transformation of T. castaneum. Tc-vermilion line- a Tribolium eye-color mutant- was also used for the microinjection of the donor vector. The donor vector contained the Tc-vermilion gene under the control of 3xP3 promoter, resulting in black eyes as a marker of their identity. In the present study, several transgenic lines bearing the regulatory regions of some importantgenes were generated. Additionally, transgenic lines for tracing of neuroblast development from the onset to the respective fully developed structure in the brain were established. Taken together, valuable tools which allow investigations of the complex genetic network needed for embryonic brain development in T. castaneum were established.Furthermore, the system will allow identification of genes and their functions in Tribolium brain formation.
 
 
 
Keywords
transposable elements
insect transgenesis
germ-line transformation
microinjection

  1.  

    1. Atkinson, P.W., Pinkerton, A.C. & O’Brochta, D.A. (2001). Genetic transformation systems in insects. Annual Review of Entomology, 46, 317-46.
    2. Badisco, L., Huybrechts, J., Simonet, G., Verlinden, H., Marchal, E., Huybrechts, R., Schoofs, L., De Loof, A. & Vanden Broeck, J. (2011). Transcriptome Analysis of the Desert Locust Central Nervous System: Production and Annotation of a Schistocerca gregaria EST Database. PLoS One 6, e17274.
    3. Beall, E. L. & Rio, D. C. (1997). Drosophila P-element transposase is a novel site-specific endonuclease. Genes & Development, 11(16), 2137-2151.
    4. Bentley, D. & Toroian-Raymond, A. (1981). Embryonic and postembryonic morphogenesis of a grasshopper interneuron. Journal of Comparative Neurology, 201, 507-18.
    5. Berghammer, A.J., Klingler, M. & Wimmer, E.A. (1999). A universal marker for transgenic insects. Nature. 402, 370-71.
    6. Berghammer, A.J., Weber, M., Trauner, J. & Klingler, M. (2009). Red flour beetle (Tribolium) germline transformation and insertional mutagenesis. Cold Spring Harb Protoc, pdb.prot5259.
    7. Boquet, I., Hitier, R., Dumas, M., Chaminade, M. & Preat, T. (2000). Central brain postembryonic development in Drosophila: implication of genes expressed at the interhemispheric junction. Journal of Neurobiology, 42, 33-48.
    8. Boyan, G., Herbert, Z. & Williams, L. (2010). Cell death shapes embryonic lineages of the Central Complex in the grasshopper Schistocerca gregaria. Journal of Morphology, 271, 949-959.
    9. Boyan, G.S. & Williams, J.L.D. (1997). Embryonic development of the pars intercerebralis/ Central Complex of the grasshopper. Development Genes and Evolution, 207, 317-329.
    10. Brown, S.J., Shippy, T.D., Miller, S., Bolognesi, R., Beeman, R.W., Lorenzen, M.D., Bucher, G., Wimmer, E.A. & Klingler, M. (2009). The Red Flour Beetle, Tribolium castaneum (Coleoptera): A Model for Studies of Development and Pest Biology. Cold Spring Harbor Protocols, 4(8),1-9.
    11. Bucher, G., Scholten, J. & Klingler, M. (2002). Parental RNAi in Tribolium (Coleoptera). Current Biology, 12, R85.
    12. Burt, A. & Koufopanou V. (2004). Homing endonuclease genes: the rise and fall and rise again of a selfish element. Current Opinion in Genetics & Development, 14, 609-15.
    13. Coates, C.J., Jasinskiene, N., Morgan, D., Tosi, L.R., Beverley, SM. & James, A.A. (2000). Purified mariner (Mos1) transposase catalyzes the integration of marked elements into the germ-line of the yellow fever mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology, 30, 1003-8.
    14. Cowden, J. & Levine, M. (2003). Ventral dominance governs sequential patterns of gene expression across the dorsal–ventral axis of the neuroectoderm in the Drosophila embryo. Developmental Biology, 262, 335-349.
    15. de Velasco, B., Erclik, T., Shy, D., Sclafani, J., Lipshitz, H., McInnes, R. & Hartenstein, V. (2007). Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Developmental Biology, 302, 309-323.
    16. Doak, T.G., Doerder, F.P., Jahn, C.L. & Herrick, G. (1994). A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D35E” motif. In: Proceedings of the National Academy of Sciences, 91, 942-46.
    17. Dominguez, M. & Campuzano, S. (1993). Asense, a member of the Drosophila achaete scutecomplex, is a proneural and neural differentiation gene. The EMBO Journal, 2(5), 20149-2060.
    18. Dong, Y. & Friedrich, M. (2010). Enforcing biphasic eye development in a directly developing insect by transient knockdown of single eye selector genes. Journal of experimental zoology. Part B, Molecular and Developmental Evolution, 314B, 104-114.
    19. Dreyer, D., Vitt, H., Dippel, S., Goetz, B., El Jundi, B., Kollmann, M., Huetteroth, W. & Schachtner, J. (2010). 3D Standard Brain of the Red Flour Beetle Tribolium Castaneum: A Tool to Study Metamorphic Development and Adult Plasticity. Frontiers in Systems Neuroscience 4, 3.
    20. Emery, J.F. & Bier, E. (1995). Specificity of CNS and PNS regulatory sub elements comprising pan-neural enhancers of the deadpan and scratch genes is achieved by repression. Development, 121, 3549-3560.
    21. Erclik, T., Hartenstein, V., Lipshitz, H. D. & McInnes, R. R. (2008). Conserved Role of the Vsx Genes Supports a Monophyletic Origin for Bilaterian Visual Systems. Current Biology, 18, 1278-1287.
    22. Fraser, J. M.J. (2012). Insect Transgenesis: Current Applications and Future Prospects. Annual Review of Entomology, 57, 267-89.
    23. Fraser, M. (2000). The TTAA-specific family of transposable elements: identification, functional characterization, and utility for transformation of insects. In Insect Transgenesis: Methods and Applications.
    24. Handler, A. M., Gomez, S. P. & O'Brochta, D. A. (1993). A functional analysis of the P-element gene transfer vector in insects. Archives of Insect Biochemistry and Physiology, 22(3-4), 373-384.
    25. Handler, A. M. & James, A. A. (2000). Insect Transgenesis:Methods and Applications (CRC, Boca Raton, Florida).
    26. Heinze, S. & Homberg, U. (2007). Maplike representation of celestial E-vector orientations in the brain of an insect. Science, 315, 995-7.
    27. Horn, C., Schmid, B. G. M., Pogoda, F. S. & Wimmer, E. A. (2002). Fluorescent transformation markers forinsect transgenesis. Insect Biochemistry and Molecular Biology,32, 1221-1235.
    28. Ilius, M., Wolf, R. & Heisenberg, M. (1994). The central complex of Drosophila melanogaster is involved in flight control: studies on mutants and mosaics of the gene ellipsoid body open. Journal of Neurogenetics, 9, 189-206.
    29. Kato, T., Kajikawa, M., Maenaka, K. & Park, EY. (2010). Silkworm expression system as a platform technology in life science. Applied Microbiology and Biotechnology, 85, 459-70.
    30. Kurylas, A. E., Rohlfing, T., Krofczik, S., Jenett, A. & Homberg, U. (2008). Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell and Tissue Research, 333, 125-45.
    31. Levine, E. M., Hitchcock, P. F., Glasgow, E. & Schechter, N. (1994). Restricted expression of a new pairedclass homeobox gene in normal and regenerating adult goldfish retina. Journal of Comparative Neurology, 348, 596-606.
    32. Liu, I. S. C., Chen, J., Ploder, L., Vidgen, D., Van der Kooy, D., Kalnins, V. I. & Mclnnes, R. R. (1994). Developmental expression of a novel murine homeobox gene (Chx10): Evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron, 13, 377-393.
    33. Martin, J. R., Raabe, T. & Heisenberg, M. (1999). Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. Journal of Comparative Physiology A, 185, 277-88.
    34. Mathur, G., Sanchez-Vargas, I., Alvarez, D., Olson, K.E., Marinotti, O. & James AA. (2010). Transgene mediated suppression of dengue viruses in the salivary glands of the yellow fever mosquito, Aedes aegypti. Insect Biochemistry and Molecular Biology, 19, 753-63.
    35. Nemirov, A. (2012). Simply Cloning-Cracking Gel from www.youtube.com/watch?v=BfQ-UIabquk.
    36. O’Brochta, D. A. & Atkinson, P. W. (1998). Building the better bug. Scientific American, 279, 90-95.
    37. O’Brochta, D.A., Subramanian, R.A., Orsetti, J., Peckham, E., Nolan, N., Arensburger, P., Atkinson, PW. & Charlwood, DJ. (2006). hAT element population genetics in Anopheles gambiae s.l. in Mozambique. Genetica, 127, 185-98.
    38. Popov, A. V., Sitnik, N. A., Savvateeva-Popova, E. V., Wolf, R. & Heisenberg, M. (2003). The role of central parts of the brain in the control of sound production during courtship in Drosophila melanogaster. Neuroscience and Behavioral Physiology, 33, 53-65.
    39. Posnien, N., Koniszewski, N. D. B., Hein, H. J. & Bucher, G. (2011b). Candidate Gene Screen in the Red Flour Beetle Tribolium Reveals Six3 as Ancient Regulator of Anterior Median Head and Complex Development. PLoS Genetics, 7, e1002416.
    40. Posnien, N., Schinko, J., Grossmann, D., Shippy, T.D., Konopova, B. & Bucher, G. (2009). RNAi in the red flour beetle (Tribolium). Cold Spring Harb Protoc, pdb.prot5256.
    41. Rein, K., Zockler, M., Mader, M. T., Grubel, C. & Heisenberg, M. (2002). The Drosophila standard brain. Current Biology, 12, 227-31.
    42. Robertson, H. M. (1995). The Tcl-mariner superfamily of transposons in animals. Journal of Insect Physiology, 41(2), 99-105.
    43. Robinson, A.S., Franz, G. & Atkinson, P.W. (2004). Insect transgenesis and its potential role in agriculture and human health. Insect Biochemistry and Molecular Biology, 34, 113-20.
    44. Rubin, G. M. & Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science, 218, 348-353.
    45. Rull, J., Brunel, O. & Mendez, M.E. (2005). Mass rearing history negatively affects mating success of male Anastrepha ludens (Diptera: Tephritidae) reared for sterile insect technique programs. Journal of Economic Entomology, 98, 1510-16.
    46. Schinko, J.B., Weber, M., Viktorinova, I., Kiupakis, A., Averof, M., Klingler, M., Wimmer, E.A. & Bucher, G. (2010). Functionality of the GAL4/UAS system in Tribolium requires the use of endogenous core promoters. Developmental Biology. 10:53 doi: 10.1186/1471-213X-10-53.
    47. Scolari, F., Schetelig, M.F., Bertin, S., Malacrida, A.R., Gasperi, G. & Wimmer, E.A. (2008). Fluorescent sperm marking to improve the fight against the pest insect Ceratitis capitata (Wiedemann; Diptera: Tephritidae). Nature Biotechnology, 25, 76-84.
    48. Scolari, F., Siciliano, P., Gabrieli, P., Gomulski, L.M., Bonomi, A., Gasperi, G. & Malacrida, A.R. (2011). Safe and fit genetically modified insects for pest control: from lab to field applications. Genetica, 139, 41-52.
    49. Sokoloff, A. (1974). The` biology of Tribolium: with special emphasis on genetic aspects. Clarendon Press.
    50. Sprecher, S.G., Urbach, R., Technau, G.M., Rijli, F.M., Reichert, H. & Hirth, F. (2006). The columnar gene vnd is required for tritocerebral neuromere formation during embryonic brain development of Drosophila. Development, 133, 4331-4339.
    51. Sundararajan, P., Atkinson, P.W. & O’Brochta, D.A. (1999). Transposable element interactions in insects: crossmobilization of hobo and Hermes. Insect Biochemistry and Molecular Biology, 8, 359-68.
    52. Tamura, T., Thibert, C., Royer, C., Kanda, T., Abraham, E., Kamba, M., Komoto, N., Thomas, J.L., Mauchamp, B., Chavancy, G., Shirk, P., Fraser, M., Prudhomme, J.C. & Couble, P. (2000). Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nature Biotechnology, 18, 81-84.
    53. Thomas, J.L., Da Rocha, M., Besse, A., Mauchamp, B. & Chavancy, G. (2002). 3xP3-EGFP marker facilitates screening for transgenic silkworm Bombyx mori L. from the embryonic stage onwards. Insect Biochemistry and Molecular Biology, 32, 247-53.
    54. Tomita, M. (2011). Transgenic silkworms that weave recombinant proteins into silk cocoons. Biotechnology Letters, 33, 645-54.
    55. Tomita, M., Munetsuna, H., Sato, T., Adachi, T., Hino, R., Hayashi, M., Shimizu,K., Nakamura, N., Tamura, T. & Yoshizato, K. (2003). Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nature Biotechnology, 21, 52-56.
    56. Tomoyasu, Y. & Denell, R.E. (2004). Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Development Genes and Evolution, 214, 575-78.
    57. Wegerhoff, R. & Breidbach, O. (1992). Structure and development of the larval central complex in a holometabolous insect, the beetle Tenebrio molitor. Cell and Tissue Research, 268, 341-358.
    58. Wheeler, S.R., Carrico, M.L., Wilson, B.A. & Skeath, J.B. (2005). The Tribolium columnar genes reveal conservation and plasticity in neural precursor patterning along the embryonic dorsal–ventral axis. Developmental Biology, 279, 491-500.
    59. Wheeler, S.R., Carrico, M.L., Wilson, B.A., Brown, SJ. & Skeath, J.B. (2003). The expression and function of the achaete-scute genes in Tribolium castaneum reveals conservation and variation in neural pattern formation and cell fate specification. Development, 130, 4373-4381.
    60. Williams, J.L.D., Guentner, M. & Boyan, G.S. (2005). Building the Central Complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w,x, y, z tracts. Arthropod Structure & Development, 34, 97-110.
    61. Wimmer, E. A. (2003). Applications of insect transgenesis. Nature Reviews Genetics, 4(3), 225-32.
    62. Wu, C. L., Xia, S., Fu, T. F., Wang, H., Chen, Y. H., Leong, D., Chiang, A. S. & Tully, T. (2007). Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Neuroscience and Behavioral Physiology, 10, 1578-86.
    63. Young, J.M. & Armstrong, J.D. (2010). Building the Central Complex in Drosophila: The generation and development of distinct neural subsets. Journal of Comparative Neurology, 518, 1525-541.
    64. Zhu, S., Wildonger, J., Barshow, S., Younger, S., Huang, Y. & Lee T. (2012). The bHLH Repressor Deadpan Regulates the Selfrenewal and Specification of Drosophila Larval Neural Stem Cells Independently of Notch. PLoS ONE. 7(10): e46724. doi:10.1371/journal.pone.0046724 1-15.

     

     

     

Iranian Journal of Plant Protection Science
Volume 46, Issue 2 - Serial Number 2
Autumn & Winter
October 2015
Pages 207-218

  • Receive Date 15 August 2015
  • Revise Date 08 November 2015
  • Accept Date 08 December 2015