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Putative orthologues of genetically identified Drosophila melanogaster chitin producing and organising genes in Apis mellifera

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Abstract

The cuticle is a versatile coat allowing insects to survive in a variety of ecological situations. The polysaccharide chitin is a major cuticle component defining cuticle function. The key players of chitin synthesis and organisation, including chitin synthase-1 (CS-1), the chitin deacetylases vermiform (Verm) and serpentine (Serp), the extracellular obstructor-A (Obst-A) protein, the membrane-bound Knickkopf (Knk) and retroactive (Rtv) proteins, the cytoplasmic mummy (Mmy) protein and the transcription factor grainyhead (Grh) have been characterised genetically in the fruit fly Drosophila melanogaster. Here, we report on the identification of putative orthologues of these factors in Apis mellifera and on their expression at different developmental stages. Overall, differences in gene organisation and expression pattern between these two species may compile different cuticle compositions that reflect their life style and ecology. Our data will serve to elucidate the honeybee-specific mechanisms of cuticle formation.

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References

  • Altenhoff, A.M., Dessimoz, C. (2012) Inferring orthology and paralogy. Methods Mol Biol 855, 259–279

    Article  PubMed  Google Scholar 

  • Arakane, Y., Hogenkamp, D.G., Zhu, Y.C., Kramer, K.J., Specht, C.A., Beeman, R.W., Kanost, M.R., Muthukrishnan, S. (2004) Characterization of two chitin synthase genes of the red flour beetle, Tribolium castaneum, and alternate exon usage in one of the genes during development. Insect Biochem Mol Biol 34, 291–304

    Article  PubMed  CAS  Google Scholar 

  • Arakane, Y., Muthukrishnan, S., Kramer, K.J., Specht, C.A., Tomoyasu, Y., Lorenzen, M.D., Kanost, M., Beeman, R.W. (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 14, 453–463

    Article  PubMed  CAS  Google Scholar 

  • Araujo, S.J., Aslam, H., Tear, G., Casanova, J. (2005) mummy/cystic encodes an enzyme required for chitin and glycan synthesis, involved in trachea, embryonic cuticle and CNS development—analysis of its role in Drosophila tracheal morphogenesis. Dev Biol 288, 179–193

    Article  PubMed  CAS  Google Scholar 

  • Atanesyan, L., Gunther, V., Dichtl, B., Georgiev, O., Schaffner, W. (2012) Polyglutamine tracts as modulators of transcriptional activation from yeast to mammals. Biol Chem 393, 63–70

    Article  PubMed  CAS  Google Scholar 

  • Bray, S.J., Kafatos, F.C. (1991) Developmental function of Elf-1: an essential transcription factor during embryogenesis in Drosophila. Genes Dev 5, 1672–1683

    Article  PubMed  CAS  Google Scholar 

  • Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J., Wittwer, C.T. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55, 611–622

    Article  PubMed  CAS  Google Scholar 

  • Chaudhari, S.S., Arakane, Y., Specht, C.A., Moussian, B., Boyle, D.L., Park, Y., Kramer, K.J., Beeman, R.W., Muthukrishnan, S. (2011) Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. Proc Natl Acad Sci U S A 108, 17028–17033

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chaudhari, S.S., Arakane, Y., Specht, C.A., Moussian, B., Kramer, K.J., Muthukrishnan, S., Beeman, R.W. (2013) Retroactive maintains cuticle integrity by promoting the trafficking of Knickkopf into the procuticle of Tribolium castaneum. PLoS Genet 9, e1003268

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dixit, R., Arakane, Y., Specht, C.A., Richard, C., Kramer, K.J., Beeman, R.W., Muthukrishnan, S. (2008) Domain organization and phylogenetic analysis of proteins from the chitin deacetylase gene family of Tribolium castaneum and three other species of insects. Insect Biochem Mol Biol 38, 440–451

    Article  PubMed  CAS  Google Scholar 

  • Elias-Neto, M., Soares, M.P., Bitondi, M.M. (2009) Changes in integument structure during the imaginal molt of the honey bee. Apidologie 40, 29–39

    Article  Google Scholar 

  • Gangishetti, U., Veerkamp, J., Bezdan, D., Schwarz, H., Lohmann, I., Moussian, B. (2012) The transcription factor Grainy head and the steroid hormone ecdysone cooperate during differentiation of the skin of Drosophila melanogaster. Insect Mol Biol 21, 283–295

    Article  PubMed  CAS  Google Scholar 

  • Guan, X., Middlebrooks, B.W., Alexander, S., Wasserman, S.A. (2006) Mutation of TweedleD, a member of an unconventional cuticle protein family, alters body shape in Drosophila. Proc Natl Acad Sci U S A 103, 16794–16799

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hogenkamp, D.G., Arakane, Y., Zimoch, L., Merzendorfer, H., Kramer, K.J., Beeman, R.W., Kanost, M.R., Specht, C.A., Muthukrishnan, S. (2005) Chitin synthase genes in Manduca sexta: characterization of a gut-specific transcript and differential tissue expression of alternately spliced mRNAs during development. Insect Biochem Mol Biol 35, 529–540

    Article  PubMed  CAS  Google Scholar 

  • Huang, L., Cheng, T., Xu, P., Fang, T., Xia, Q. (2012) Bombyx mori transcription factors: genome-wide identification, expression profiles and response to pathogens by microarray analysis. J Insect Sci 12, 40

    PubMed  PubMed Central  Google Scholar 

  • Irion, U. (2012) Drosophila muscleblind codes for proteins with one and two tandem zinc finger motifs. PLoS One 7, e34248

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson, B.R., Borowiec, M.L., Chiu, J.C., Lee, E.K., Atallah, J., Ward, P.S. (2013) Phylogenomics resolves evolutionary relationships among ants, bees, and wasps. Curr Biol 23, 2058–2062

    Article  PubMed  CAS  Google Scholar 

  • Kucharski, R., Maleszka, J., Maleszka, R. (2007) Novel cuticular proteins revealed by the honey bee genome. Insect Biochem Mol Biol 37, 128–134

    Article  PubMed  CAS  Google Scholar 

  • Locke, M. (2001) The Wigglesworth Lecture: Insects for studying fundamental problems in biology. J Insect Physiol 47, 495–507

    Article  PubMed  CAS  Google Scholar 

  • Luschnig, S., Batz, T., Armbruster, K., Krasnow, M.A. (2006) serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr Biol 16, 186–194

    Article  PubMed  CAS  Google Scholar 

  • Merzendorfer, H. (2006) Insect chitin synthases: a review. J Comp Physiol B 176, 1–15

    Article  PubMed  CAS  Google Scholar 

  • Moussian, B. (2008) The role of GlcNAc in formation and function of extracellular matrices. Comp Biochem Physiol B Biochem Mol Biol 149, 215–226

    Article  PubMed  Google Scholar 

  • Moussian, B. (2010) Recent advances in understanding mechanisms of insect cuticle differentiation. Insect Biochem Mol Biol 40, 363–375

    Article  PubMed  CAS  Google Scholar 

  • Moussian, B. (2013) The apical plasma membrane of chitin-synthesizing epithelia. Insect science 20, 139–146

    Article  PubMed  CAS  Google Scholar 

  • Moussian, B., Schwarz, H., Bartoszewski, S., Nusslein-Volhard, C. (2005a) Involvement of chitin in exoskeleton morphogenesis in Drosophila melanogaster. J Morphol 264, 117–130

    Article  PubMed  CAS  Google Scholar 

  • Moussian, B., Soding, J., Schwarz, H., Nusslein-Volhard, C. (2005b) Retroactive, a membrane-anchored extracellular protein related to vertebrate snake neurotoxin-like proteins, is required for cuticle organization in the larva of Drosophila melanogaster. Dev Dyn 233, 1056–1063

    Article  PubMed  CAS  Google Scholar 

  • Moussian, B., Tang, E., Tonning, A., Helms, S., Schwarz, H., Nusslein-Volhard, C., Uv, A.E. (2006) Drosophila Knickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization. Development 133, 163–171

    Article  PubMed  CAS  Google Scholar 

  • Munoz-Torres, M.C., Reese, J.T., Childers, C.P., Bennett, A.K., Sundaram, J.P., Childs, K.L., Anzola, J.M., Milshina, N., Elsik, C.G. (2011) Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 39, D658–662

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pare, A., Kim, M., Juarez, M.T., Brody, S., McGinnis, W. (2012) The functions of grainy head-like proteins in animals and fungi and the evolution of apical extracellular barriers. PLoS One 7, e36254

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Petkau, G., Wingen, C., Jussen, L.C., Radtke, T., Behr, M. (2012) Obstructor-A is required for epithelial extracellular matrix dynamics, exoskeleton function, and tubulogenesis. J Biol Chem 287, 21396–21405

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qu, M., Yang, Q. (2011) A novel alternative splicing site of class A chitin synthase from the insect Ostrinia furnacalis—gene organization, expression pattern and physiological significance. Insect Biochem Mol Biol 41, 923–931

    Article  PubMed  CAS  Google Scholar 

  • Qu, M., Yang, Q. (2012) Physiological significance of alternatively spliced exon combinations of the single-copy gene class A chitin synthase in the insect Ostrinia furnacalis (Lepidoptera). Insect Mol Biol 21, 395–404

    Article  PubMed  CAS  Google Scholar 

  • Rezende, G.L., Martins, A.J., Gentile, C., Farnesi, L.C., Pelajo-Machado, M., Peixoto, A.A., Valle, D. (2008) Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Dev Biol 8, 82

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103(Suppl 1), S96–119

    Article  PubMed  Google Scholar 

  • Schimmelpfeng, K., Strunk, M., Stork, T., Klambt, C. (2006) Mummy encodes an UDP-N-acetylglucosamine-dipohosphorylase and is required during Drosophila dorsal closure and nervous system development. Mech Dev 123, 487–499

    Article  PubMed  CAS  Google Scholar 

  • Soares, M.P., Silva-Torres, F.A., Elias-Neto, M., Nunes, F.M., Simoes, Z.L., Bitondi, M.M. (2011) Ecdysteroid-dependent expression of the tweedle and peroxidase genes during adult cuticle formation in the honey bee, Apis mellifera. PLoS One 6, e20513

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Soding, J., Biegert, A., Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33, W244–248

    Article  PubMed  PubMed Central  Google Scholar 

  • Suske, G. (1999) The Sp-family of transcription factors. Gene 238, 291–300

    Article  PubMed  CAS  Google Scholar 

  • Tonning, A., Helms, S., Schwarz, H., Uv, A.E., Moussian, B. (2006) Hormonal regulation of mummy is needed for apical extracellular matrix formation and epithelial morphogenesis in Drosophila. Development 133, 331–341

    Article  PubMed  CAS  Google Scholar 

  • Uv, A.E., Harrison, E.J., Bray, S.J. (1997) Tissue-specific splicing and functions of the Drosophila transcription factor Grainyhead. Mol Cell Biol 17, 6727–6735

    PubMed  CAS  PubMed Central  Google Scholar 

  • Van Leeuwen, T., Demaeght, P., Osborne, E.J., Dermauw, W., Gohlke, S., Nauen, R., Grbic, M., Tirry, L., Merzendorfer, H., Clark, R.M. (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci U S A 109, 4407–4412

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Liu, X., Zhang, J., Li, D., Sun, Y., Guo, Y., Ma, E., Zhu, K.Y. (2010) Silencing of two alternative splicing-derived mRNA variants of chitin synthase 1 gene by RNAi is lethal to the oriental migratory locust, Locusta migratoria manilensis (Meyen). Insect Biochem Mol Biol 40, 824–833

    Article  PubMed  CAS  Google Scholar 

  • Zhang, X., Zhang, J., Park, Y., Zhu, K.Y. (2012) Identification and characterization of two chitin synthase genes in African malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 42, 674–682

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Correspondence to Bernard Moussian.

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Manuscript editor: Marina Meixner

Orthologues putatifs des gènes identifiés chez Drosophila melanogaster impliqués dans la synthese et l'organisation de la chitine chez Apis mellifera

cuticule / chitine / synthase de la chitine

Mutmaßliche Orthologe der bei Drosophila melanogaster identifizierten, zur Produktion und Organisation von Chitin benötigten gene bei Apis mellifera.

Kutikula / Chitin / Chitin Synthase / Chitin-Organisation

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Wang, Y., Odemer, R., Rosenkranz, P. et al. Putative orthologues of genetically identified Drosophila melanogaster chitin producing and organising genes in Apis mellifera . Apidologie 45, 733–747 (2014). https://doi.org/10.1007/s13592-014-0292-3

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  • DOI: https://doi.org/10.1007/s13592-014-0292-3

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