Skip to main content
SpringerLink
Log in

Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Mesoderm formation has been extensively analyzed in the long-germ insect Drosophila melanogaster. In Drosophila, both the invagination and specification of the mesoderm is controlled by twist. Here we present a detailed description of mesoderm formation and twist regulation for the short-germ beetle Tribolium castaneum. In contrast to Drosophila, (1) the presumptive mesodermal cells of Tribolium are part of a mitotic domain and divide prior to ventral furrow formation, (2) ventral furrow formation progresses from posterior to anterior, (3) the number of cell layers within the furrow changes from multilayered in caudal to single layered in cephalic regions, and (4) there is a continuous production of mesodermal cells after gastrulation as new segments arise from the posterior growth zone. Tribolium twist (Tc-twist) is initially expressed in all presumptive mesodermal cells; however, after invagination, expression is maintained only in particular locations, which include the anterior compartments of the cephalic segments and a patch of cells at the posterior rim of the growth zone. The growth zone is multilayered with its inner cell layer being continuous with the mesoderm of the newly forming segments where twist expression is re-initiated anterior to the emerging engrailed stripes. A genomic region of Tc-twist was identified which drives ventral expression of a reporter construct in Drosophila. The expression of this Tc-twist construct in the background of Drosophila maternal mutations suggests that the dorsoventral system regulates Tc-twist, but that differences exist in regulation of the Dm-twist and Tc-twist genes by the terminal system.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Anderson DT (1972) The development of hemimetabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, vol 1. Academic, London, pp 96–163

  • Ando H (1962) The comparative embryology of Odonata with special reference to a relic dragonfly Epiophlebia superstes Seyles. Japanese Society for the Promotion of Science, Tokyo

    Google Scholar 

  • Ando H, Kawana T (1956) Embryology of the mayfly (Epemera strigata Eaton) as studied by external observation. Kontyu 24:224–232

    Google Scholar 

  • Arendt D (2004) Comparative aspects of gastrulation. In: Stern CD (ed) Gastrulation. Cold Spring Harbor Laboratory Press, New York, pp 679–693

    Google Scholar 

  • Arora K, Nüsslein-Volhard C (1992) Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes. Development 114:1003–1024

    CAS  PubMed  Google Scholar 

  • Bate M, Rushton E, Currie DA (1991) Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113:79–90

    CAS  PubMed  Google Scholar 

  • Baylies MK, Bate M (1996) twist: a myogenic switch in Drosophila. Science 272:1481–1484

    CAS  PubMed  Google Scholar 

  • Berghammer A, Bucher G, Maderspacher F, Klingler M (1999a) A system to efficiently maintain embryonic lethal mutations in the flour beetle Tribolium castaneum. Dev Genes Evol 209:382–388

    Article  CAS  PubMed  Google Scholar 

  • Berghammer A, Klingler M, Wimmer EA (1999b) A universal marker for transgenic insects. Nature 402:370–371

    Article  CAS  PubMed  Google Scholar 

  • Brand C, Bergter A, Paululat A (2003) Cloning of a Twist orthologue from Enchytraeus coronatus (Annelida, Oligochaeta). DNA Seq 14:25–31

    CAS  PubMed  Google Scholar 

  • Brown SJ, Hilgenfeld RB, Denell RE (1994a) The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc Natl Acad Sci USA 91:12922–12926

    CAS  PubMed  Google Scholar 

  • Brown SJ, Patel NH, Denell RE (1994b) Embryonic expression of the single Tribolium engrailed homolog. Dev Genet 15:7–18

    CAS  PubMed  Google Scholar 

  • Bucher G, Scholten J, Klingler M (2002) Parental RNAi in Tribolium (Coleoptera). Curr Biol 12:R85–R86

    Article  CAS  PubMed  Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Casanova J (1991) Interaction between torso and dorsal, two elements of different transduction pathways in the Drosophila embryo. Mech Dev 36:41–45

    Article  CAS  PubMed  Google Scholar 

  • Castanon I, Baylies MK (2002) A Twist in fate: evolutionary comparison of Twist structure and function. Gene 287:11–22

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Handel K, Roth S (2000) The maternal NF-kappaB/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. Development 127:5145–5156

    CAS  PubMed  Google Scholar 

  • Costa M, Wilson ET, Wieschaus E (1994) A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation. Cell 76:1075–1089

    Article  CAS  PubMed  Google Scholar 

  • Courey AJ, Tjian R (1988) Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell 55:887–898

    Article  CAS  PubMed  Google Scholar 

  • Davis GK, Patel NH (2002) Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu Rev Entomol 47: 669–699

    Article  CAS  PubMed  Google Scholar 

  • Edgar BA, O’FARRELL PH (1989) Genetic control of cell division patterns in the Drosophila embryo. Cell 57:177–187

    Article  CAS  PubMed  Google Scholar 

  • Edgar BA, Lehman DA, O’FARRELL PH (1994) Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. Development 120:3131–3143

    CAS  PubMed  Google Scholar 

  • Falciani F, Hausdorf B, Schröder R, Akam M, Tautz D, Denell R, Brown S (1996) Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci USA 93:8479–8484

    Article  CAS  PubMed  Google Scholar 

  • Fan X (2001) Apis dorsal, gene structure, role in oogenesis, embryonic development and induction of an innate immune response. PhD Thesis, University of Tübingen, Tübingen

  • Fleig R, Sander K (1988) Honeybee morphogenesis: embryonic cell movements that shape the larval body. Development 103:535–543

    PubMed  Google Scholar 

  • Foe VE (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:1–22

    CAS  Google Scholar 

  • Fristrom D, Fristrom JW (1993) The metamorphic development of the adult epidermis. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, vol 2. Cold Spring Harbor Laboratory Press, New York, pp 843–898

  • Gitelman I (1997) Twist protein in mouse embryogenesis. Dev Biol 189: 205–214

    Article  CAS  PubMed  Google Scholar 

  • Gont LK, Steinbeisser H, Blumberg B, de Robertis EM (1993) Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip. Development 119:991–1004

    CAS  PubMed  Google Scholar 

  • Grosshans J, Wieschaus E (2000) A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101:523–531

    Article  CAS  PubMed  Google Scholar 

  • Halfon MS, Carmena A, Gisselbrecht S, Sackerson CM, Jimenez F, Baylies MK, Michelson AM (2000) Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103:63–74

    Article  CAS  PubMed  Google Scholar 

  • Handel K, Grünfelder C, Roth S, Sander K (2000) Tribolium embryogenesis: a SEM study of cell shapes and movements from blastoderm to serosal closure. Dev Genes Evol 210:167–179

    Article  CAS  PubMed  Google Scholar 

  • Harfe BD, Gomes AV, Kenyon C, Liu J, Krause M, Fire A (1998) Analysis of a Caenorhabditis elegans Twist homolog identifies conserved and divergent aspects of mesodermal patterning. Genes Dev 12:2623–2635

    CAS  PubMed  Google Scholar 

  • Hemavathy K, Meng X, Ip YT (1997) Differential regulation of gastrulation and neuroectodermal gene expression by Snail in the Drosophila embryo. Development 124:3683–3691

    CAS  PubMed  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360

    Article  CAS  PubMed  Google Scholar 

  • Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149

    Article  CAS  PubMed  Google Scholar 

  • Hopwood ND, Pluck A, Gurdon JB (1989) A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59:893–903

    CAS  PubMed  Google Scholar 

  • Imai KS, Satoh N, Satou Y (2003) A Twist-like bHLH gene is a downstream factor of an endogenous FGF and determines mesenchymal fate in the ascidian embryos. Development 130:4461–4472

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Kosman D, Ip YT, Levine M (1991) The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos. Genes Dev 5:1881–1991

    CAS  PubMed  Google Scholar 

  • Jura C (1972) Development of apterygote insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, vol 1. Academic, London, pp 49–95

  • Kanki JP, Ho RK (1997) The development of the posterior body in zebrafish. Development 124:881–893

    CAS  PubMed  Google Scholar 

  • Klingler M, Erdelyi M, Szabad J, Nüsslein-Volhard C (1988) Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature 335:275–277

    Article  CAS  PubMed  Google Scholar 

  • Knezevic V, De Santo R, Mackem S (1998) Continuing organizer function during chick tail development. Development 125:1791–1801

    CAS  PubMed  Google Scholar 

  • Konrad KD, Goralski TJ, Mahowald A (1988) Developmental analysis of fs(1) gastrulation defective, a dorsal-group gene of Drosophila melanogaster. Wilhelm Roux Arch Entwicklungsmech Org 197:75–91

    Article  Google Scholar 

  • Kusch T, Reuter R (1999) Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling. Development 126: 3991–4003

    CAS  PubMed  Google Scholar 

  • Leptin M (1991) twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev 5:1568–1576

    CAS  PubMed  Google Scholar 

  • Leptin M (2004) Gastrulation in Drosophila. In: Stern CD (ed) Gastrulation. Cold Spring Harbor Laboratory Press, New York, pp 91–104

    Google Scholar 

  • Leptin M, Grunewald B (1990) Cell shape changes during gastrulation in Drosophila. Development 110:73–84

    CAS  PubMed  Google Scholar 

  • Leptin M, Roth S (1994) Autonomy and non-autonomy in Drosophila mesoderm differentiation and morphogenesis. Development 120:853–859

    CAS  PubMed  Google Scholar 

  • Maderspacher F, Bucher G, Klingler M (1998) Pair-rule and gap gene mutants in the flour beetle Tribolium castaneum. Dev Genes Evol 208: 558–568

    Article  CAS  PubMed  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474

    Article  CAS  PubMed  Google Scholar 

  • Mata J, Curado S, Ephrussi A, Rorth P (2000) Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101:511–522

    Article  CAS  PubMed  Google Scholar 

  • Nüsslein-Volhard C, Wieschaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Wilhelm Roux Arch Entwicklungsmech Org 193:267–282

    Google Scholar 

  • Pan DJ, Huang JD, Courey AJ (1991) Functional analysis of the Drosophila twist promoter reveals a dorsal-binding ventral activator region. Genes Dev 5:1892–1901

    CAS  PubMed  Google Scholar 

  • Patel NH, Condron BG, Zinn K (1994) Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367:429–434

    Article  CAS  PubMed  Google Scholar 

  • Ray RP, Arora K, Nüsslein-Volhard C, Gelbart WM (1991) The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113:35–54

    CAS  PubMed  Google Scholar 

  • Roonwal ML (1936) Studies on the embryology of the African migratory locus, Locusta migratoria migratoroides. I. The early development, with a new theory of multiphase gastrulation among insects. Philos Trans R Soc Ser B 226:391–421

    Google Scholar 

  • Roth S (2004) Gastrulation in other insects. In: Stern CD (ed) Gastrulation. Cold Spring Harbor Laboratory Press, New York, pp 105–121

    Google Scholar 

  • Roth S, Stein D, Nüsslein-Volhard C (1989) A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59:1189–1202

    Article  CAS  PubMed  Google Scholar 

  • Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348–353

    CAS  PubMed  Google Scholar 

  • Sanchez-Salazar J, Plether MT, Bennett RL, Brown SJ, Dandamudi TJ, Denell, RE, Doctor JS (1996) The Tribolium decapentaplegic gene is similar in sequence, structure, and expression to the Drosophila dpp gene. Dev Genes Evol 206:237–246

    Article  CAS  Google Scholar 

  • Schmidt-Ott U (2000) The amnioserosa is an apomorphic character of cyclorrhaphan flies. Dev Genes Evol 210:373–376

    Article  CAS  PubMed  Google Scholar 

  • Schwalm F (1988) Insect morphogenesis. In: Monographs in developmental biology. Karger, Basel

  • Seher TC, Leptin M (2000) Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Curr Biol 10:623–629

    Article  CAS  PubMed  Google Scholar 

  • Simpson P (1983) Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics 105: 615–632

    Google Scholar 

  • Sommer RJ, Tautz D (1993) Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera). Nature 361:448–450

    Article  CAS  PubMed  Google Scholar 

  • Sommer RJ, Tautz D (1994) Expression patterns of twist and snail in Tribolium (Coleoptera) suggest a homologous formation of mesoderm in long and short germ band insects. Dev Genet 15:32–37

    CAS  PubMed  Google Scholar 

  • Spring J, Yanze N, Middel AM, Stierwald M, Groger H, Schmid V (2000) The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol 228:363–375

    Article  CAS  PubMed  Google Scholar 

  • Stathopoulos A, Levine M (2002) Dorsal gradient networks in the Drosophila embryo. Dev Biol 246:57–67

    Article  CAS  PubMed  Google Scholar 

  • Stathopoulos A, Van Drenth M, Erives A, Markstein M, Levine M (2002) Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo. Cell 111:687–701

    Article  CAS  PubMed  Google Scholar 

  • Sulston IA, Anderson KV (1996) Embryonic patterning mutants of Tribolium castaneum. Development 122:805–814

    CAS  PubMed  Google Scholar 

  • Sulston IA, Anderson KV (1998) Altered patterns of gene expression in Tribolium segmentation mutants. Dev Genet 23:56–64

    Article  CAS  PubMed  Google Scholar 

  • Sweeton D, Parks S, Costa M, Wieschaus, E. (1991) Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations. Development 112:775–789

    CAS  PubMed  Google Scholar 

  • Tapanes-Castillo A, Cox V, Baylies M (2004) Conserved and divergent roles of Twist in gastrulation. In: Stern CD (ed) Gastrulation. Cold Spring Harbor Laboratory Press, New York, pp 619–629

    Google Scholar 

  • 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 98:81–85

    Article  CAS  PubMed  Google Scholar 

  • Thisse B, Stoetzel C, Gorostiza-Thisse C, Perrin-Schmitt F (1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7:2175–2183

    CAS  PubMed  Google Scholar 

  • Thisse C, Perrin-Schmitt F, Stoetzel C, Thisse B (1991) Sequence-specific transactivation of the Drosophila twist gene by the dorsal gene product. Cell 65:1191–1201

    Article  CAS  PubMed  Google Scholar 

  • Thummel CS, Boulet AM, Lipshitz HD (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74:445–456

    Article  CAS  PubMed  Google Scholar 

  • Ullmann SL (1964) The origin and structure of the mesoderm and the formation of the coelomic sacs in Tenebrio molitor L. (Insecta, Coleoptera). Philos Trans R Soc Ser B 248:245–277

    Google Scholar 

  • Vincent S, Wilson R, Coelho C, Affolter M, Leptin M (1998) The Drosophila protein Dof is specifically required for FGF signaling. Mol Cell 2:515–525

    Article  CAS  PubMed  Google Scholar 

  • Willmann R (2003) Phylogenese und System der Insekten. In: Dathe HH (ed) Wirbellose Tiere, vol 1. Part 5 Insecta. Spektrum, Heidelberg

Download references

Acknowledgements

We thank Dr. Christoph Grünfelder for help with SEM microscopy, Dr. Angelika Stollewerk for introducing confocal microscopy to us, Dr. Nikola-Michael Prpic for assessing the twi phylogeny and Oliver Karst for technical assistance. X.F. has conducted her work on Apis in the lab of Prof. Wolf Engels at the Institute of Zoology of the University of Tübingen. She thanks Prof. W. Engels for support. We are grateful to Prof. Maria Leptin, Dr. Robert Wilson, Patrick Kalscheuer, Cornelia Mikulski and Maurijn van der Zee for discussions and critical comments on the manuscript. The work was supported by DFG grants (SPP 1027).

Author information

Author notes

  1. Klaus Handel

    Present address: Roche Diagnostics GmbH, Nonnenwald 2, 82377, Penzberg, Germany

  2. Xiang Fan

    Present address: University of Georgia Athens, 420 Biological Sciences Building, 30602-2603, Athens, GA, USA

Authors and Affiliations

  1. Institut für Entwicklungsbiologie, Universität zu Köln, Gyrhofstr. 17, 50923, Cologne, Germany

    Abidin Basal & Siegfried Roth

Authors
  1. Klaus Handel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abidin Basal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiang Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Siegfried Roth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Siegfried Roth.

Additional information

Edited by D. Tautz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Handel, K., Basal, A., Fan, X. et al. Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle. Dev Genes Evol 215, 13–31 (2005). https://doi.org/10.1007/s00427-004-0446-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-004-0446-9

Keywords

Search

Navigation