Cited by 55Developmental Biology and Gene RegulationGenomics and Chromatin DynamicsNeurobiology and Insect Physiology Research

Delimiting the conserved features of hunchback function for the trunk organization of insects

Open access
Marques-Souza, Henrique, Aranda, Manuel, Tautz, Diethard·2008·Development

Abstract

The gap gene hunchback in Drosophila acts during syncytial blastoderm stage via a short-range gradient and concentration-dependent activation or repression of target genes. Orthologues of hunchback can be easily found in other insects, but it has been unclear how well its functions are conserved. The segmentation process in most insect embryos occurs under cellular conditions, which should not allow the formation of diffusion-controlled transcription factor gradients. We have studied here in detail the function of hunchback in the short germ embryo of Tribolium using parental RNAi and interaction with possible target genes. We find that hunchback is a major regulator of the trunk gap genes and Hox genes in Tribolium, but may only indirectly be required to regulate other segmentation genes. The core function of hunchback appears to be the setting of the Ultrabithoraxexpression border via a repression effect, and the activation of the Krüppel expression domain. These regulatory effects are likely to be direct and are conserved between Drosophila and Tribolium. We find no evidence for a classical gap phenotype in the form of loss of segments in the region of expression of hunchback. However, the phenotypic effects in Tribolium are highly comparable with those found for other short germ embryos, i.e. the core functions of hunchback in Tribolium appear to be the same in these other insects, although they are evolutionarily more distant to Tribolium,than Tribolium is to Drosophila. These results allow the disentanglement of the conserved role of hunchback in insects from the derived features that have been acquired in the lineage towards Drosophila. Given that the gap phenotype appears to occur only in long germ embryos and that the main role of hunchback appears to be the regionalization of the embryo, it may be appropriate to revive an alternative name for the class of gap genes, namely `cardinal genes'.

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  • Every major aspect of A/P patterning analyzed at the gene interaction level appears to include some different linkages in Drosophila compared to Tribolium.

    “Every major aspect of A/P patterning analyzed at the gene interaction level appears to include some different linkages in Drosophila compared to Tribolium.”

    From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Marques-Souza et al., 2008

    The paper identifies differences in specific gene interactions: the Regulation between gap genes section (p. 6) says a hunchback–giant interaction seen in Drosophila is not conserved, and The role of hunchback in segmentation (p. 7) describes a possible difference in gap-gene–pair-rule coupling. It does not establish that every major aspect of A/P patterning has different linkages; The conserved core elements of hunchback function (p. 7) also identifies interactions shared by the two insects. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • In both Drosophila and Tribolium, hb sets the anterior boundary of Ubx expression and provides an activating input into the kruppel regulatory system.

    “On the other hand, in both species hb sets the anterior boundary of Ubx expression and provides an activating input into the kruppel regulatory system (Marques-Souza et al., 2008).”

    From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Marques-Souza et al., 2008

  • In Tribolium, hb apparently does not directly control primary pair rule genes, and does not repress but rather activates giant.

    “Similarly it is clear that some of the GRN wiring downstream of the hunchback gene differs, for in Tribolium hb apparently does not directly control primary pair rule genes, and does not repress, but rather activates giant (Choe et al., 2006; Marques-Souza et al., 2008).”

    From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Marques-Souza et al., 2008

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Authors
Marques-Souza, H., Aranda, M., & Tautz, D.
Affiliations
  • Department of Genetics, University of Cologne, Zülpicherstrasse 47, 50674 Köln, Germany.
  • University of Cologne (DE)
  • Max Planck Society (DE)
Corresponding author
Tautz, Diethard
Venue
Development
Published
2008-03-01
Volume
135
Issue
5
Pages
881-888
ISSN
  • 0950-1991 (ISSN-L)
  • 1477-9129
OpenAlex
W1979178770
Cited by
55
References
45
Citations by year
2025: 1 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 4 · 2019: 3 · 2018: 6 · 2017: 2 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 2 · 2012: 3
FWCI
3.15
Type
journal article
Language
en
Open access
Locations
  • Development (publishedVersion)
  • PubMed (publishedVersion)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords
hunchback, gap genes, Tribolium castaneum, Hox genes, Ultrabithorax, Krüppel, syncytial blastoderm, Drosophila
MeSH terms
Animals, DNA-Binding Proteins, Drosophila, Embryo, Nonmammalian, Larva, Phenotype, Transcription Factors, Tribolium, Homeodomain Proteins, Gene Expression Regulation, Developmental, Gene Expression Profiling, RNA Interference

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