Literature DB >> 33546687

Functional analysis of sense organ specification in the Tribolium castaneum larva reveals divergent mechanisms in insects.

Marleen Klann1,2, Magdalena Ines Schacht1, Matthew Alan Benton3, Angelika Stollewerk4.   

Abstract

Insects and other arthropods utilise external sensory structures for mechanosensory, olfactory, and gustatory reception. These sense organs have characteristic shapes related to their function, and in many cases are distributed in a fixed pattern so that they are identifiable individually. In Drosophila melanogaster, the identity of sense organs is regulated by specific combinations of transcription factors. In other arthropods, however, sense organ subtypes cannot be linked to the same code of gene expression. This raises the questions of how sense organ diversity has evolved and whether the principles underlying subtype identity in D. melanogaster are representative of other insects. Here, we provide evidence that such principles cannot be generalised, and suggest that sensory organ diversification followed the recruitment of sensory genes to distinct sensory organ specification mechanism.
RESULTS: We analysed sense organ development in a nondipteran insect, the flour beetle Tribolium castaneum, by gene expression and RNA interference studies. We show that in contrast to D. melanogaster, T. castaneum sense organs cannot be categorised based on the expression or their requirement for individual or combinations of conserved sense organ transcription factors such as cut and pox neuro, or members of the Achaete-Scute (Tc ASH, Tc asense), Atonal (Tc atonal, Tc cato, Tc amos), and neurogenin families (Tc tap). Rather, our observations support an evolutionary scenario whereby these sensory genes are required for the specification of sense organ precursors and the development and differentiation of sensory cell types in diverse external sensilla which do not fall into specific morphological and functional classes.
CONCLUSIONS: Based on our findings and past research, we present an evolutionary scenario suggesting that sense organ subtype identity has evolved by recruitment of a flexible sensory gene network to the different sense organ specification processes. A dominant role of these genes in subtype identity has evolved as a secondary effect of the function of these genes in individual or subsets of sense organs, probably modulated by positional cues.

Entities:  

Keywords:  Evolution; Gene expression; RNA interference; Sense organ development; Sense organ subtypes; Tribolium castaneum

Year:  2021        PMID: 33546687      PMCID: PMC7866635          DOI: 10.1186/s12915-021-00948-y

Source DB:  PubMed          Journal:  BMC Biol        ISSN: 1741-7007            Impact factor:   7.431


  90 in total

Review 1.  Arthropod sensilla: morphology and phylogenetic considerations.

Authors:  E Hallberg; B S Hansson
Journal:  Microsc Res Tech       Date:  1999-12-15       Impact factor: 2.769

Review 2.  Proneural genes and the specification of neural cell types.

Authors:  Nicolas Bertrand; Diogo S Castro; François Guillemot
Journal:  Nat Rev Neurosci       Date:  2002-07       Impact factor: 34.870

Review 3.  Gene duplication at the achaete-scute complex and morphological complexity of the peripheral nervous system in Diptera.

Authors:  Nick Skaer; Daniela Pistillo; Jean-Michel Gibert; Pietro Lio; Corinna Wülbeck; Pat Simpson
Journal:  Trends Genet       Date:  2002-08       Impact factor: 11.639

4.  Genetic basis for the evolution of organ morphogenesis: the case of spalt and cut in the development of insect trachea.

Authors:  Cristina de Miguel; Friedemann Linsler; Jordi Casanova; Xavier Franch-Marro
Journal:  Development       Date:  2016-08-30       Impact factor: 6.868

5.  The red flour beetle, Tribolium castaneum (Coleoptera): a model for studies of development and pest biology.

Authors:  Susan J Brown; Teresa D Shippy; Sherry Miller; Renata Bolognesi; Richard W Beeman; Marcé D Lorenzen; Gregor Bucher; Ernst A Wimmer; Martin Klingler
Journal:  Cold Spring Harb Protoc       Date:  2009-08

Review 6.  The role of Atonal transcription factors in the development of mechanosensitive cells.

Authors:  Andrew P Jarman; Andrew K Groves
Journal:  Semin Cell Dev Biol       Date:  2013-03-30       Impact factor: 7.727

7.  Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera).

Authors:  Johannes B Schinko; Nina Kreuzer; Nils Offen; Nico Posnien; Ernst A Wimmer; Gregor Bucher
Journal:  Dev Biol       Date:  2008-03-15       Impact factor: 3.582

8.  The role of Notch signalling and numb function in mechanosensory organ formation in the spider Cupiennius salei.

Authors:  Katrina Gold; James A Cotton; Angelika Stollewerk
Journal:  Dev Biol       Date:  2008-12-16       Impact factor: 3.582

9.  Suppression of β1-integrin in gonadotropin-releasing hormone cells disrupts migration and axonal extension resulting in severe reproductive alterations.

Authors:  Jyoti Parkash; Irene Cimino; Nicoletta Ferraris; Filippo Casoni; Susan Wray; Hélène Cappy; Vincent Prevot; Paolo Giacobini
Journal:  J Neurosci       Date:  2012-11-21       Impact factor: 6.167

10.  Expanded and updated data and a query pipeline for iBeetle-Base.

Authors:  Jürgen Dönitz; Lizzy Gerischer; Stefan Hahnke; Stefan Pfeiffer; Gregor Bucher
Journal:  Nucleic Acids Res       Date:  2018-01-04       Impact factor: 16.971

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