Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Oenocyte development in the red flour beetle Tribolium castaneum


Oenocytes are a specialized cell type required for lipid processing, pheromone secretion, and developmental signaling. Their development has been well characterized in Drosophila melanogaster, but it remains unknown whether the developmental program is conserved in other insect species. In this study, we compare and contrast the specification and development of larval oenocytes between Drosophila and the red flour beetle, Tribolium castaneum. First, we identify several useful reagents to label larval oenocytes, including both a Tribolium GFP enhancer trap line and a simple flurophore-conjugated streptavidin staining method that recognizes oenocytes across insect species. Second, we use these tools to describe oenocyte development in Tribolium embryos, and our findings provide evidence for conserved roles of MAP kinase signaling as well as the Spalt, Engrailed, hepatocyte nuclear factor-4, and ventral veins lacking factors in producing abdominal-specific oenocyte cells. However, Tribolium embryos produce four times as many oenocytes per abdominal segment as Drosophila, and unlike in Drosophila, these cells rapidly downregulate the expression of the Spalt transcription factor. Thus, these results provide new insight into the molecular pathways regulating oenocyte specification across insect species.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7


  1. Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461:987–991

  2. Brodu V, Elstob PR, Gould AP (2002) Abdominal A specifies one cell type in Drosophila by regulating one principal target gene. Development 129:2957–2963

  3. Brodu V, Elstob PR, Gould AP (2004) EGF receptor signaling regulates pulses of cell delamination from the Drosophila ectoderm. Dev Cell 7:885–895

  4. Chapman RF (1998) The insects: structure and function, 4th edn. Cambridge University Press, Cambridge

  5. Eastham LES (1929) The post-embryonic development of Phaenoserphus viator Hal. (Proctotrypoidea), a parasite of the larva of Pterostichus niger (Carabidae), with notes on the anatomy of the larva. Parasitology 21:1–21

  6. Elstob PR, Brodu V, Gould AP (2001) Spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor. Development 128:723–732

  7. Fernandez MP, Chan YB, Yew JY, Billeter JC, Dreisewerd K, Levine JD, Kravitz EA (2010) Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol 8:e1000541

  8. Fletcher K, Myant NB (1960) Biotin in the synthesis of fatty acid and cholesterol by mammalian liver. Nature 188:585

  9. Gabay L, Seger R, Shilo BZ (1997) In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277:1103–1106

  10. Gebelein B, Mann RS (2007) Compartmental modulation of abdominal Hox expression by engrailed and sloppy-paired patterns the fly ectoderm. Dev Biol 308:593–605

  11. Gould AP, Elstob PR, Brodu V (2001) Insect oenocytes: a model system for studying cell-fate specification by Hox genes. J Anat 199:25–33

  12. Gutierrez E, Wiggins D, Fielding B, Gould AP (2007) Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 445:275–280

  13. Gutzwiller LM, Witt LM, Gresser AL, Burns KA, Cook TA, Gebelein B (2010) Proneural and abdominal Hox inputs synergize to promote sensory organ formation in the Drosophila abdomen. Dev Biol 348:231–243

  14. Inbal A, Levanon D, Salzberg A (2003) Multiple roles for u-turn/ventral veinless in the development of Drosophila PNS. Development 130:2467–2478

  15. Jackson A, Locke M (1989) The formation of plasma membrane reticular systems in the oenocytes of an insect. Tissue Cell 21:463–473

  16. Kornberg T (1981) Engrailed: a gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci U S A 78:1095–1099

  17. Lage P, Jan YN, Jarman AP (1997) Requirement for EGF receptor signalling in neural recruitment during formation of Drosophila chordotonal sense organ clusters. Curr Biol: CB 7:166–175

  18. Levine M (2010) Transcriptional enhancers in animal development and evolution. Curr Biol: CB 20:R754–R763

  19. Li-Kroeger D, Witt LM, Grimes HL, Cook TA, Gebelein B (2008) Hox and senseless antagonism functions as a molecular switch to regulate EGF secretion in the Drosophila PNS. Dev Cell 15:298–308

  20. Mahadevan LC, Willis AC, Barratt MJ (1991) Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65:775–783

  21. Palanker L, Tennessen JM, Lam G, Thummel CS (2009) Drosophila HNF4 regulates lipid mobilization and beta-oxidation. Cell Metab 9:228–239

  22. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Bucher G, Friedrich M, Grimmelikhuijzen CJ et al (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–955

  23. Roth S, Hartenstein V (2008) Development of Tribolium castaneum. Dev Genes Evol 218:115–118

  24. Rusten TE, Cantera R, Urban J, Technau G, Kafatos FC, Barrio R (2001) Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS of Drosophila promoting the development of oenocytes. Development 128:711–722

  25. Schroder R, Beermann A, Wittkopp N, Lutz R (2008) From development to biodiversity—Tribolium castaneum, an insect model organism for short germband development. Dev Genes Evol 218:119–126

  26. Shilo BZ (2005) Regulating the dynamics of EGF receptor signaling in space and time. Development 132:4017–4027

  27. Shippy TD, Brown SJ, Denell RE (1998) Molecular characterization of the Tribolium abdominal-A ortholog and implications for the products of the Drosophila gene. Dev Genes Evol 207:446–452

  28. Snodgrass RE (1993) Principles of insect morphology. Cornell University Press, Ithaca

  29. Tomoyasu Y, Wheeler SR, Denell RE (2005) Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433:643–647

  30. Trauner J, Schinko J, Lorenzen MD, Shippy TD, Wimmer EA, Beeman RW, Klingler M, Bucher G, Brown SJ (2009) Large-scale insertional mutagenesis of a coleopteran stored grain pest, the red flour beetle Tribolium castaneum, identifies embryonic lethal mutations and enhancer traps. BMC Biol 7:73

  31. Wheeler WM (1892) Concerning the blood tissue of insects. Psyche 6:216–258

  32. Witt LM, Gutzwiller LM, Gresser AL, Li-Kroeger D, Cook TA, Gebelein B (2010) Atonal, senseless, and abdominal-A regulate rhomboid enhancer activity in abdominal sensory organ precursors. Dev Biol 344:1060–1070

  33. Xie B, Charlton-Perkins M, McDonald E, Gebelein B, Cook T (2007) Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134:4243–4253

  34. Zara FJ, Caetano FH (2004) Ultramorphology and histochemistry of fat body cells from last instar larval of the Pachycondyla (=Neoponera) villosa (Fabricius) (Formicidae: Ponerinae). Braz J Biol 64:725–735

  35. Ziegler R, Engler DL, Davis NT (1995) Biotin-containing proteins of the insect nervous system, a potential source of interference with immunocytochemical localization procedures. Insect Biochem Mol Biol 25:569–574

Download references


We thank Alex Gould, GEKU, the Bloomington Drosophila Stock Center, and the Developmental Studies Hybridoma Bank (University of Iowa) for the reagents. We thank Tingjia Lao and Padmapriyadarshini Ravisankar for technical assistance. This work was supported by an NIH grant GM079428A to B.G and an NSF grant (IOS0950964) to Y.T.

Author information

Correspondence to Brian Gebelein.

Additional information

Communicated by S. Roth

Electronic supplementary material

Below is the link to the electronic supplementary material.


(DOC 1,925 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Burns, K.A., Gutzwiller, L.M., Tomoyasu, Y. et al. Oenocyte development in the red flour beetle Tribolium castaneum . Dev Genes Evol 222, 77–88 (2012). https://doi.org/10.1007/s00427-012-0390-z

Download citation


  • Oenocytes
  • Epidermal growth factor
  • Spalt
  • Tribolium