Development Genes and Evolution

, Volume 218, Issue 3–4, pp 153–167 | Cite as

Sites of Fgf signalling and perception during embryogenesis of the beetle Tribolium castaneum

Original Article

Abstract

The development of multicellular embryos depends on coordinated cell-to-cell signalling events. Among the numerous cell-signalling pathways, fibroblast growth factors (FGFs) are involved in important processes during embryogenesis, such as mesoderm formation during gastrulation and growth. In vertebrates, the Fgf superfamily consists of 22 family members, whereas only few FGFs are contained in the less complex genomes of insects and worms. In the recently sequenced genome of the beetle Tribolium, we identified four Fgf family members representing three subfamilies. Tribolium has Fgf1 genes that are absent in Drosophila but known from vertebrates. By phylogenetic analysis and microsynteny to Drosophila, we further classify Tc-fgf 8 as an ancestor of pyramus and thisbe, the fly Fgf8 genes. Tc-fgf8 expression in the growth zone suggests an involvement in mesoderm formation. In the embryonic head, expression of Tc-fgf8 subdivides the brain into a larger anterior and a smaller posterior region. The Fgf Tc-branchless is expressed in the embryonic tracheal placodes and in various gland-like structures. The expression patterns of the only Tribolium Fgf receptor and the adaptor molecule Downstream-of-Fgfr are largely congruent with Tc-Fgf8 and Tc-bnl. Thus, in contrast to Drosophila, only one Fgf receptor canalises Fgf signalling in different tissues in Tribolium. Our findings significantly advance our understanding of the evolution of Fgf signalling in insects.

Keywords

Tribolium Fgf signalling Gastrulation Brain regionalisation Evolution 

Notes

Acknowledgements

We thank R. Reuter for constant encouraging support, T. Mader for technical help and F. Beermann for comments on the manuscript. Our work is financed by the German Research Council (DFG) grant SCHR 435/3 1-3).

References

  1. Beiman M, Shilo BZ, Volk T (1996) Heartless, a Drosophila FGF receptor homolog, is essential for cell migration and establishment of several mesodermal lineages. Genes Dev 10:2993–3002PubMedCrossRefGoogle Scholar
  2. Boulet AM, Moon AM, Arenkiel BR, Capecchi MR (2004) The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev Biol 273:361–372PubMedCrossRefGoogle Scholar
  3. Branda CS, Stern MJ (2000) Mechanisms controlling sex myoblast migration in Caenorhabditis elegans hermaphrodites. Dev Biol 226:137–151PubMedCrossRefGoogle Scholar
  4. Chi CL, Martinez S, Wurst W, Martin GR (2003) The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130:2633–2644PubMedCrossRefGoogle Scholar
  5. Cohen SM, Jürgens G (1989) Proximal–distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J 8:2045–2055PubMedGoogle Scholar
  6. Coulier F, Pontarotti P, Roubin R, Hartung H, Goldfarb M, Birnbaum D (1997) Of worms and men: an evolutionary perspective on the fibroblast growth factor (FGF) and FGF receptor families. J Mol Evol 44:43–56PubMedCrossRefGoogle Scholar
  7. Elsik CG, Mackey AJ, Reese JT, Milshina NV, Roos DS, Weinstock GM (2007) Creating a honey bee consensus gene set. Genome Biol 8:R13PubMedCrossRefGoogle Scholar
  8. Fambrough D, McClure K, Kazlauskas A, Lander ES (1999) Diverse signaling pathways activated by growth factor receptors induce broadly overlapping, rather than independent, sets of genes. Cell 97:727–741PubMedCrossRefGoogle Scholar
  9. Gisselbrecht S, Skeath JB, Doe CQ, Michelson AM (1996) heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo. Genes Dev 10:3003–3017PubMedCrossRefGoogle Scholar
  10. Grieshammer U, Cebrian C, Ilagan R, Meyers E, Herzlinger D, Martin GR (2005) FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 132:3847–3857PubMedCrossRefGoogle Scholar
  11. Gryzik T, Müller HA (2004) FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl and are required for mesoderm migration in the Drosophila gastrula. Curr Biol 14:659–667PubMedCrossRefGoogle Scholar
  12. Handel K, Basal A, Fan X, Roth S (2005) Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle. Dev Genes Evol 215:13–31PubMedCrossRefGoogle Scholar
  13. Harmer NJ (2006) Insights into the role of heparan sulphate in fibroblast growth factor signalling. Biochem Soc Trans 34:442–445PubMedCrossRefGoogle Scholar
  14. Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H (2003) An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 130:2365–2373PubMedCrossRefGoogle Scholar
  15. Huang P, Stern MJ (2005) FGF signaling in flies and worms: more and more relevant to vertebrate biology. Cytokine Growth Factor Rev 16:151–158PubMedCrossRefGoogle Scholar
  16. Huet C, Lenoir-Rousseaux JJ (1976) Adult leg development of Tenebrio molitor: I. Experimental analysis of the restoration process during morphogenesis. J Embryol Exp Morphol 35:303–321PubMedGoogle Scholar
  17. Imai KS, Satoh N, Satou Y (2002) Region specific gene expressions in the central nervous system of the ascidian embryo. Mech Dev 119(Suppl 1):S275–S277PubMedCrossRefGoogle Scholar
  18. Imai KS, Levine M, Satoh N, Satou Y (2006) Regulatory blueprint for a chordate embryo. Science 312:1183–1187PubMedCrossRefGoogle Scholar
  19. Itoh N, Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20:563–569PubMedCrossRefGoogle Scholar
  20. Kerber B, Fellert S, Hoch M (1998) Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev 12:1781–1786PubMedCrossRefGoogle Scholar
  21. Kim C (1959) The differentiation centre inducing the development from larval to adult leg in Pieris brassicae (Lepidoptera). J Embryol Exp Morphol 7:572–582PubMedGoogle Scholar
  22. Klämbt C, Glazer L, Shilo BZ (1992) Breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 6:1668–1678PubMedCrossRefGoogle Scholar
  23. Klingler M, Gergen JP (1993) Regulation of runt transcription by Drosophila segmentation genes. Mech Dev 43:3–19PubMedCrossRefGoogle Scholar
  24. Kuske G (1963) Untersuchungen zur Metamorphose der Schmetterlingsbeine. Roux’ Archiv für Entwicklungsmechanik 154:354–377CrossRefGoogle Scholar
  25. Kuske G, Penner M, Piepho H (1961) Zur Metamorphose des Schmetterlingsbeines. Biol Zbl 80:347–351Google Scholar
  26. Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity 94:465–477PubMedCrossRefGoogle Scholar
  27. Maqbool T, Soler C, Jagla T, Daczewska M, Lodha N, Palliyil S, Vijayraghavan K, Jagla K (2006) Shaping leg muscles in Drosophila: role of ladybird, a conserved regulator of appendicular myogenesis. PLoS ONE 1:e122PubMedCrossRefGoogle Scholar
  28. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS (1998) Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 12:3156–3161PubMedCrossRefGoogle Scholar
  29. Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2:REVIEWS3005PubMedCrossRefGoogle Scholar
  30. Parthasarathy R, Gopinathan KP (2005) Comparative analysis of the development of the mandibular salivary glands and the labial silk glands in the mulberry silkworm, Bombyx mori. Gene Expression Patterns 5:323–339PubMedCrossRefGoogle Scholar
  31. Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L (1994) Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J 13:3296–3301PubMedGoogle Scholar
  32. Popovici C, Roubin R, Coulier F, Birnbaum D (2005) An evolutionary history of the FGF superfamily. Bioessays 27:849–857PubMedCrossRefGoogle Scholar
  33. Reichert H (2005) A tripartite organization of the urbilaterian brain: developmental genetic evidence from Drosophila. Brain Res Bull 66:491–494PubMedCrossRefGoogle Scholar
  34. Reuss B, von Bohlen und Halbach O (2003) Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 313:139–157PubMedCrossRefGoogle Scholar
  35. Rhinn M, Picker A, Brand M (2006) Global and local mechanisms of forebrain and midbrain patterning. Curr Opin Neurobiol 16:5–12PubMedCrossRefGoogle Scholar
  36. Sato M, Kornberg TB (2002) FGF is an essential mitogen and chemoattractant for the air sacs of the Drosophila tracheal system. Dev Cell 3:195–207PubMedCrossRefGoogle Scholar
  37. Sato T, Joyner AL, Nakamura H (2004) How does Fgf signaling from the isthmic organizer induce midbrain and cerebellum development? Dev Growth Differ 46:487–494PubMedCrossRefGoogle Scholar
  38. Savard J, Tautz D, Richards S, Weinstock GM, Gibbs RA, Werren JH, Tettelin H, Lercher MJ (2006) Phylogenomic analysis reveals bees and wasps (Hymenoptera) at the base of the radiation of Holometabolous insects. Genome Res 16:1334–1338PubMedCrossRefGoogle Scholar
  39. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M (2000) Crystal structure of a ternary FGF–FGFR–heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6:743–750PubMedCrossRefGoogle Scholar
  40. Schröder R, Eckert C, Wolff C, Tautz D (2000) Conserved and divergent aspects of terminal patterning in the beetle Tribolium castaneum. Proc Natl Acad Sci USA 97:6591–6596PubMedCrossRefGoogle Scholar
  41. Shishido E, Higashijima S, Emori Y, Saigo K (1993) Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117:751–761PubMedGoogle Scholar
  42. Simon MA (2000) Receptor tyrosine kinases: specific outcomes from general signals. Cell 103:13–15PubMedCrossRefGoogle Scholar
  43. Stathopoulos A, Tam B, Ronshaugen M, Frasch M, Levine M (2004) Pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. Genes Dev 18:687–699PubMedCrossRefGoogle Scholar
  44. Sun X, Meyers EN, Lewandoski M, Martin GR (1999) Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev 13:1834–1846PubMedCrossRefGoogle Scholar
  45. Sun X, Mariani FV, Martin GR (2002) Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418:501–508PubMedCrossRefGoogle Scholar
  46. Sutherland D, Samakovlis C, Krasnow MA (1996) Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87:1091–1101PubMedCrossRefGoogle Scholar
  47. Takashima S, Murakami R (2001) Regulation of pattern formation in the Drosophila hindgut by wg, hh, dpp, and en. Mech Dev 101:79–90PubMedCrossRefGoogle Scholar
  48. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85PubMedCrossRefGoogle Scholar
  49. Thisse B, Thisse C (2005) Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 287:390–402PubMedCrossRefGoogle Scholar
  50. Trumpp A, Depew MJ, Rubenstein JL, Bishop JM, Martin GR (1999) Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev 13:3136–3148PubMedCrossRefGoogle Scholar
  51. Vincent S, Wilson R, Coelho C, Affolter M, Leptin M (1998) The Drosophila protein Dof is specifically required for FGF signaling. Mol Cell 2:515–525PubMedCrossRefGoogle Scholar
  52. Wilson R, Vogelsang E, Leptin M (2005) FGF signalling and the mechanism of mesoderm spreading in Drosophila embryos. Development 132:491–501PubMedCrossRefGoogle Scholar
  53. Wolff C, Sommer R, Schröder R, Glaser G, Tautz D (1995) Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121:4227–4236PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Animal Genetics, Institute for Cell BiologyUniversity of TübingenTübingenGermany

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