Capturing embryonic development from metamorphosis: how did the terminal patterning signalling pathway of Drosophila evolve?

https://doi.org/10.1016/j.cois.2014.04.007Get rights and content

Highlights

  • •

    The Torso activation module in insects is ancestrally involved in regulation of growth and pupation.

  • •

    The Torso activation module has been co-opted into controlling terminal patterning in Drosophila and Tribolium.

  • •

    Torso-like is highly conserved, but has a largely unknown function in embryogenesis and in the prothoracic gland.

The Torso receptor tyrosine kinase has two crucial roles in Drosophila melanogaster development. One is in the control of insect moulting, which is regulated by the neuropeptide hormone PTTH (prothoracicotropic hormone). PTTH activates ERK signalling via Torso in the prothoracic gland to stimulate ecdysone secretion. Torso also has a role in control of one of the earliest events in embryogenesis in Drosophila; patterning of the embryonic termini. Here Torso is activated by a different, but related, peptide called Trunk. During terminal patterning another protein, Torso-like, has a key role in mediating activation of Torso by Trunk. Torso-like is also expressed in the prothoracic gland and null-mutants have defective developmental timing in Drosophila. This function, however, has been recently shown to be independent of Torso and PTTH. We refer to these proteins, Trunk, PTTH, Torso and Torso-like, as the Torso-activation module. Outside Drosophila we see that the genes encoding the Torso-activation module have a complex phylogenetic history, with different origins and multiple losses of components of this signalling pathway during arthropod evolution. This, together with expression and functional data in a range of insects, leads us to propose that the terminal patterning pathway in Drosophila and Tribolium arose through co-option of PTTH/Trunk and Torso, which has a role in developmental timing, into a new context, and that Torso-like was recruited specifically in the ovary to modulate the specificity of this pathway.

Section snippets

Torso and Trunk in Drosophila

In Drosophila melanogaster the formation of anterior–posterior and dorso-ventral axes are initiated during oogenesis [1]. At the same time, a patterning process, named terminal patterning, defines both the anterior and posterior ends of the embryo 2, 3. Components of this patterning pathway have been identified through extensive mutant screens 3, 4, 5, 6, 7, 8, and include a receptor tyrosine kinase called Torso that is believed to be activated by binding of a ligand called Trunk 9, 10.

Torso and PTTH in Drosophila and Bombyx

Trunk is predicted to be homologous to the neuropeptide hormone prothoracicotropic hormone (PTTH) 9, 28••, 37, 38•• — sequence similarity reveals both proteins belonging to the cysteine knot growth factor superfamily. PTTH is released from specific neurons to stimulate the prothoracic gland in response to nutritional and environmental cues 39, 40, 41, 42. This triggers the production and release of ecdysone 41, 43 initiating larval moulting and metamorphosis 37, 43, 44. In Drosophila, these

Evolution of the Torso activation module

Torso, Trunk, PTTH, and Torso-like form the components of what we refer to as the ‘Torso-activation module’.

The patterns of conservation and diversification of the components of the Torso-activation module is complex with varied origins and multiple losses during arthropod evolution (Figure 2) [38••]. Trunk is only found in some holometabolous insects and in the chelicerate Ixodes [38••], but not in hemimetabolous insects. Trunk is also missing from the genomes of two hymenopterans; the

Conclusions and future directions

Studies of the Torso activation module in Drosophila and other insects have provided insights into the evolution of this pathway. The phylogenetic distribution of the components of this pathway is confusing, but it appears that trunk and PTTH arose from Noggin-like genes [38••]. The developmental timing function of this pathway appears older than its role in terminal patterning, as PTTH activity [53] and the PTTH gene [38••], are broadly phylogenetically distributed in insects, whereas

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by an ARC grant to J.C.W., C.W. and P.K.D. (DP140102771). This work derived from discussions supported by Genetics Otago (www.otago.ac.nz/genetics).

References (63)

  • P.K. Dearden

    Patterns of conservation and change in honey bee developmental genes

    Genome Res

    (2006)
  • M.J. Wilson et al.

    Diversity in insect axis formation: two orthodenticle genes and hunchback act in anterior patterning and influence dorsoventral organization in the honeybee (Apis mellifera)

    Development

    (2011)
  • J.A. Lynch

    Regulation and function of tailless in the long germ wasp Nasonia vitripennis

    Dev Genes Evol

    (2006)
  • A. Weisbrod

    Evolution of the insect terminal patterning system — insights from the milkweed bug, Oncopeltus fasciatus

    Dev Biol

    (2013)
  • J.A. Lynch

    Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia

    Nature

    (2006)
  • C. Nusslein-Volhard

    Determination of anteroposterior polarity in Drosophila

    Science

    (1987)
  • D. St Johnston et al.

    The origin of pattern and polarity in the Drosophila embryo

    Cell

    (1992)
  • T. Schupbach et al.

    Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations

    Genetics

    (1989)
  • T. Schupbach et al.

    Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology

    Genetics

    (1991)
  • N. Perrimon

    Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome

    Genetics

    (1989)
  • S. Luschnig

    An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster

    Genetics

    (2004)
  • A. Casali et al.

    The spatial control of Torso RTK activation: a C-terminal fragment of the Trunk protein acts as a signal for Torso receptor in the Drosophila embryo

    Development

    (2001)
  • J. Casanova

    Similarities between trunk and spätzle, putative extracellular ligands specifying body pattern in Drosophila

    Genes Dev

    (1995)
  • G. Bronner et al.

    Regulation and function of the terminal gap gene huckebein in the Drosophila blastoderm

    Int J Dev Biol

    (1996)
  • F. Pignoni

    bicoid and the terminal system activate tailless expression in the early Drosophila embryo

    Development

    (1992)
  • M. Klingler

    Function of torso in determining the terminal anlagen of the Drosophila embryo

    Nature

    (1988)
  • T.R. Strecker

    Reciprocal effects of hyper- and hypoactivity mutations in the Drosophila patterning gene torso

    Science

    (1989)
  • O. Grimm

    Torso RTK, controls Capicua degradation by changing its subcellular localization

    Development

    (2012)
  • F. Sprenger

    The Drosophila gene torso encodes a putative receptor tyrosine kinase

    Nature

    (1989)
  • J. Casanova et al.

    Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila

    Genes Dev

    (1989)
  • L.M. Stevens

    Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo

    Nature

    (1990)

    • Cited by (5)

    • RNA interference suppression of the receptor tyrosine kinase Torso gene impaired pupation and adult emergence in Leptinotarsa decemlineata

      2015, Journal of Insect Physiology
      Citation Excerpt :

      Activated Torso initiates a phosphorylation cascade including Raf/Phl, MEK/Dsor1, and ERK/Rl. This cascade disinhibits the transcriptional repression by Cic and Gro, and permits gap gene (tailless and huckebein) and subsequent pair-rule gene expression to pattern the developing embryo (Duncan et al., 2014; Sopko and Perrimon, 2013). Orthologs for Trunk, PTTH and Torso have been identified in Coleopteran species Tribolium castaneum (Grillo et al., 2012; Smith and Rybczynski, 2012).

    • Co-option of immune effectors by the hormonal signalling system triggering metamorphosis in Drosophila melanogaster

      2021, PLoS Genetics

    • Evolution of the Torso activation cassette, a pathway required for terminal patterning and moulting

      2019, Insect Molecular Biology

    • The trigger (and the restriction) of Torso RTK activation

      2018, Open Biology

    • The honeybee as a model insect for developmental genetics

      2017, Genesis
    View full text
    Copyright © 2014 Elsevier Inc. All rights reserved.