Abstract
Hypomorphic mutations have been investigated of the genes spineless (ss), Distal-less (Dll), leg-arista-wing complex/TBP-related factor 2 (lawc/Trf2), CG5017, and hsp70 in order to explore the effects of their expression level on the formation of distal structures of antenna and legs of Drosophila melanogaster. We demonstrated the effect of the CG5017, hsp70, Dll, and lawc gene transcription level on phenotypic manifestation of the ss gene mutation and the involvement of these genes into morphogenesis regulation of Drosophila melanogaster limbs. The total decrease in the level of the CG5017, hsp70, Dll, and lawc gene expression level was shown to promote a loss of the segmented pattern of distal structures of legs and antennae and a reversion of Drosophila limb morphogenesis to the evolutionarily earlier progenitors of insects. A hypothesis is proposed considering limb morphogenesis of insects as an evolutionary ancient process of formation of amorphous-crystal chitin structures with catalytically modifying participation of gene expression products.
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Abu-Shaar, M. and Mann, R.S., Generation of Multiple Antagonistic Domains along the Proximodistal Axis during Drosophila Leg Development, Development, 1998, vol. 125, no. 19, pp.3821–3830.
Balkashinea, I., Ein Fall der Erbhomoosis (Die Genovariation “Aristapedia”) Bei Drosophila Melanogaster, W. Roux Arch. Entw. Org., 1929, vol. 115, pp.448–465.
Brand, A.H. and Perrimon, N., Targeted Gene Expression as a Means of Altering Cell Fates and Generating Dominant Phenotypes, Development, 1993, vol. 118, pp.401–9415.
Brook, W.J. and Cohen, S.M., Antagonistic Interactions between Wingless and Decapentaplegic Responsible for Dorsal-Ventral Pattern in the Drosophila Leg, Science, 1996, vol. 273, pp.1373–1377.
Chen, B., Shilova, V.Y., Zatsepina, O.G., et al., Location of P Element Insertions in the Proximal Promoter Region of Hsp70A Is Consequential for Gene Expression and Correlated with Fecundity in Drosophila melanogaster, Cell Stress Chaperones, 2008, vol. 13, no. 1, pp.11–17.
Cohen, S.M. and Jürgens, G., Proximal-Distal Pattern Formation in Drosophila: Cell Autonomous Requirement for Distal-Less Gene Activity in Limb Development, EMBO J., 1989, vol. 8, no. 7, pp.2045–2055.
Crew, S. and Brenman, E., Spineless Provides a Little Backbone for Dendritic Morphogenesis, Gen. Dev., 2006, vol. 20, pp.2773–2778.
Dubnau, J., Chiang, A., Grady, L., et al., The Staufen/Pumilio Pathway Is Involved in Drosophila Long-Term Memory, Curr. Biol., 2003, vol. 13, pp.286–296.
Duncan, D., Burgess, E., and Duncan, I., Control of Distal Antennal Identity and Tarsal Development in Drosophila by Spineless-Aristapedia, a Homolog of the Mammalian Dioxin Receptor, Gen. Dev., 1998, vol. 12, pp.1290–1303.
Emmons, R., Duncan, D., Estes, P., et al., The Spineless-Aristapedia and Tango bHLH-PAS Proteins Interact to Control Antennal and Tarsal Development in Drosophila, Development, 1999, vol. 126, pp.3937–3945.
Gorovoi, L.F. and Kosyakov, V.N., Sorptive Properties of Chitin, in Khitin i khitozan (Chitin and Chitosan), Moscow: Nauka, 2002, pp.217–246.
Grigliatti, T. and Suzuki, D., Temperature Sensitive Mutations in Drosophila melanogaster. VII. The Homeotic Mutant ssa40a, Proc. Natl. Acad. Sci. USA, 1971, vol. 68, pp.1307–1311.
Kim, M., Jan, L., and Jan, Y., The bHLH-PAS Protein Spineless Is Necessary for the Diversification of Dendrite Morphology of Drosophila Dendritic Arborisation Neurons, Gen. Dev., 2006, vol. 20, pp.2806–2819.
Kopytova, D.V., Krasnov, A.N., Simonova, O.B., et al., Study of the lawc-trf2 Gene of Drosophila melanogaster and the Protein Product of This Gene, Doklady Biochem. Biophys., 2005, vol. 405, no. 1, pp.380–382.
Kuzin, B.A., Doszhanov, K.T., Simonova, O.B., et al., A New Allele Variant of ssa and Its Participation in Regulating the Proliferation of the Stem Elements of the Leg and Antenna Imaginal Disks in Drosophila melanogaster, Ontogenez, 1991, vol. 22, pp.212–217.
Kuzin, B., Dosdjanov, K., and Mazo, A., Interaction between spineless-aristapedia Gene and Genes from Antennapedia and Bithorax Complexes of Drosophila melanogaster, Int. J. Dev. Biol., 1997, vol. 41, pp.867–875.
Kuzin, B.A., Modestova, E.A., Vorontsova, Yu.E., et al., Interaction of the ss and CG5017 Genes in the Regulation of Morphogensis of Limbs in Drosophila melanogaster, Russ. J. Dev. Biol., 2010, vol. 41, no. 5, pp.312–317.
Lambert, J.B., Gurusamy-Thangavelu, S.A., and Ma, K., The Silicate-Mediated Formose Reaction: Bottom-Up Synthesis of Sugar Silicates, Science, 2010, vol. 327, pp.984–986.
Lecuit, T. and Cohen, S., Proximal-Distal Axis Formation in the Drosophila Leg, Nature, 1997, vol. 388, pp.139–145.
Park, Y.J. and Luger, K., The Structure of Nucleosome Assembly Protein 1, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, no. 5, pp.1248–1253.
Rabenstein, M.D., Zhou, S., Lis, J.T., et al., TATA Box-Binding Protein (TBP)-Related Factor 2 (TRF2), a Third Member of the TBP Family, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 9, pp.4791–4796.
Rozanov, A.Yu., Living Conditions on Early Earth after 4.0 Billion Years Ago, in Problemy proiskhozhdeniya zhizni: Sb. nauch. statei RAN (Problems of the Origin of Life: Collected Scientific Papers of the Russian Academy of Sciences), Moscow: PIN RAN, 2009, pp.185–201.
Shilova, V.Y., Garbuz, D.G., Myasyankina, E.N., et al., Remarkable Site Specificity of Local Transposition into the Hsp70 Promoter of Drosophila melanogaster, Genetics, 2006, vol. 173, no. 2, pp.809–820.
Simonova, O.B., Kuzin, B.A., Georgiev, P.G., and Gerasimova, T.I., A New Regulatory Mutation in Drosophila melanogaster, Genetika, 1992, vol. 28, no. 2, pp.164–167.
Simonova, O.B., A New trans-Regulatory Locus of Drosophila, Russ. J. Genet., 2000, vol. 36, no. 11, pp.1464–1474.
Struhl, G., spineless-aristapedia: A Homeotic Gene that Does Control the Development of Specific Compartment in Drosophila, Genetics, 1982, vol. 102, no. 4, pp.737–749.
Vorontsova, Yu.E., Modestova, E.A., Burdina, N.V., et al., Restoring Viability of Lethal Mutants for the leg-aristawing-complex Gene in Rescue Experiments with Transgenic Constructs that Express the trf2 Gene Domains in Drosophila melanogaster, Doklady Biol. Sci., 2007, vol. 417, no. 1, pp.429–431.
Wu, J. and Cohen, S.M., Proximodistal Axis Formation in the Drosophila Leg: Subdivision into Proximal and Distal Domains by Homothorax and Distal-Less, Development, 1999, vol. 126, pp.109–117.
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Original Russian Text © Yu.E. Vorontsova, R.O. Cherezov, O.G. Zatsepina, M.S. Slezinger, B.A. Kuzin, O.B. Simonova, 2012, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2012, No. 2, pp. 228–236.
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Vorontsova, Y.E., Cherezov, R.O., Zatsepina, O.G. et al. Gene expression modulation is an evolutionary resource of adaptive alterations in the morphogenesis of insect limbs. Biol Bull Russ Acad Sci 39, 186–193 (2012). https://doi.org/10.1134/S1062359012020124
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DOI: https://doi.org/10.1134/S1062359012020124