Delimiting the conserved features of hunchback function for the trunk organization of insects
Open accessAbstract
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 measuredIn 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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Cites
Tautz, D., & Pfeifle, C. (1989) · Chromosoma · doi:10.1007/bf00291041 · Cited by 2,535 · see citing works
Self-citationThe molecular basis for metameric pattern in the Drosophila embryo
Akam, M. E. (1987) · Development · doi:10.1242/dev.101.1.1 · Cited by 1,022 · see citing works
Parental RNAi in Tribolium (Coleoptera)
Bucher, G., Scholten, J., & Klingler, M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00666-8 · Cited by 531 · see citing works
Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres
Tautz, D. (1988) · Nature · doi:10.1038/332281a0 · Cited by 377 · see citing works
Self-citationdMi-2, a Hunchback-Interacting Protein That Functions in Polycomb Repression
Kehle, J. (1998) · Science · doi:10.1126/science.282.5395.1897 · Cited by 354 · see citing works
Control of Drosophila body pattern by the hunchback morphogen gradient
Struhl, G., Johnston, P., & Lawrence, P. A. (1992) · Cell · doi:10.1016/0092-8674(92)90405-2 · Cited by 298 · see citing works
Lehmann, R., & Nüsslein‐Volhard, C. (1987) · Developmental Biology · doi:10.1016/0012-1606(87)90045-5 · Cited by 294 · see citing works
Chapter 30 In Situ Hybridization to RNA
Lehmann, R., & Tautz, D. (1994) · Methods in cell biology · doi:10.1016/s0091-679x(08)60933-4 · Cited by 283 · see citing works
Self-citationHülskamp, M., Pfeifle, C., & Tautz, D. (1990) · Nature · doi:10.1038/346577a0 · Cited by 264 · see citing works
Self-citationSavard, J., Tautz, D., Richards, S., Weinstock, G. M., Gibbs, R. A., Werren, J. H., Tettelin, H., & Lercher, M. J. (2006) · Genome Research · doi:10.1101/gr.5204306 · Cited by 250 · see citing works
Self-citationThe genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium
Schröder, R. (2003) · Nature · doi:10.1038/nature01536 · Cited by 230 · see citing works
Gaul, U., Seifert, E., Schuh, R., & Jäckle, H. (1987) · Cell · doi:10.1016/0092-8674(87)90037-7 · Cited by 215 · see citing works
Choe, C. P., Miller, S. C., & Brown, S. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510440103 · Cited by 198 · see citing works
A gap gene, hunchback, regulates the spatial expression of Ultrabithorax
White, R. A., & Lehmann, R. (1986) · Cell · doi:10.1016/0092-8674(86)90453-8 · Cited by 189 · see citing works
Stauber, M., Prell, A., & Schmidt‐Ott, U. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012292899 · Cited by 178 · see citing works
Qian, S., Capovilla, M., & Pirrotta, V. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07662.x · Cited by 166 · see citing works
Hierarchical Inductions of Cell States: A Model for Segmentation in Drosophila
Meinhardt, H. (1986) · Journal of Cell Science · doi:10.1242/jcs.1986.supplement_4.20 · Cited by 162 · see citing works
Savard, J., Marques‐Souza, H., Aranda, M., & Tautz, D. (2006) · Cell · doi:10.1016/j.cell.2006.05.053 · Cited by 160 · see citing works
Self-citationSommer, R. J., & Tautz, D. (1993) · Nature · doi:10.1038/361448a0 · Cited by 155 · see citing works
Self-citationIrish, V. F., Martínez-Arias, A., & Akam, M. E. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03537.x · Cited by 153 · see citing works
Liu, P. Z., & Kaufman, T. C. (2004) · Development · doi:10.1242/dev.01046 · Cited by 153 · see citing works
Competition for Overlapping Sites in the Regulatory Region of the Drosophila Gene Krüppel
Hoch, M., Gerwin, N., Taubert, H., & Jäckle, H. (1992) · Science · doi:10.1126/science.1348871 · Cited by 139 · see citing works
The expression and regulation of Sex combs reduced protein in Drosophila embryos.Preprint
Riley, P. D., Carroll, S. B., & Scott, M. P. (1987) · Genes & Development · doi:10.1101/gad.1.7.716 · Cited by 129 · see citing works
Carroll, S. B., DiNardo, S., O’Farrell, P. H., White, R. A., & Scott, M. P. (1988) · Genes & Development · doi:10.1101/gad.2.3.350 · Cited by 118 · see citing works
Wolff, C., Sommer, R. J., Schröder, R., et al. (1995) · Development · doi:10.1242/dev.121.12.4227 · Cited by 117 · see citing works
Bucher, G., & Klingler, M. (2004) · Development · doi:10.1242/dev.01073 · Cited by 116 · see citing works
Gap genes and gradients – The logic behind the gaps
Hülskamp, M., & Tautz, D. (1991) · BioEssays · doi:10.1002/bies.950130602 · Cited by 92 · see citing works
Self-citationMito, T., Sarashina, I., Zhang, H., et al. (2005) · Development · doi:10.1242/dev.01784 · Cited by 91 · see citing works
Shimell, M., Peterson, A. J., Burr, J., Simon, J. A., & O’Connor, M. B. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9576 · Cited by 91 · see citing works
Schulz, C., & Tautz, D. (1994) · Development · doi:10.1242/dev.120.10.3043 · Cited by 88 · see citing works
Self-citationLewis, D. L., DeCamillis, M., & Bennett, R. L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4504 · Cited by 87 · see citing works
Breakdown of abdominal patterning in the Tribolium Kruppel mutant jaws
Cerny, A. C., Bucher, G., Schröder, R., & Klingler, M. (2005) · Development · doi:10.1242/dev.02154 · Cited by 86 · see citing works
Regulation of the infraabdominal regions of the bithorax complex of Drosophila by gap genes
Casares, F., & Sánchez‐Herrero, E. (1995) · Development · doi:10.1242/dev.121.6.1855 · Cited by 85 · see citing works
Insect embryogenesis - what is ancestral and what is derived?
Tautz, D., Friedrich, M., & Schröder, R. (1994) · Development · doi:10.1242/dev.1994.supplement.193 · Cited by 84 · see citing works
Self-citationA major role for zygotichunchbackin patterning theNasoniaembryo
Pultz, M. A., Westendorf, L., Gale, S. D., Hawkins, K., Lynch, J., Pitt, J. N., Reeves, N., Yao, J. C. Y., Small, S., Desplan, C., et al. (2005) · Development · doi:10.1242/dev.01939 · Cited by 83 · see citing works
Zhang, C., & Bienz, M. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.16.7511 · Cited by 80 · see citing works
Role of hunchback in segment patterning of Locusta migratoria manilensis revealed by parental RNAi
He, Z., Cao, Y., Yin, Y., et al. (2006) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2006.00881.x · Cited by 66 · see citing works
Hülskamp, M., Lukowitz, W., Beermann, A., Glaser, G., & Tautz, D. (1994) · Genetics · doi:10.1093/genetics/138.1.125 · Cited by 65 · see citing works
Self-citationWu, X., Vakani, R., & Small, S. (1998) · Development · doi:10.1242/dev.125.19.3765 · Cited by 62 · see citing works
Thoracic Patterning by the Drosophila Gap Gene hunchback
Wu, X., Vasisht, V., Kosman, D., et al. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0355 · Cited by 61 · see citing works
Implications of the Tribolium Deformed mutant phenotype for the evolution of Hox gene function
Brown, S. J., DeCamillis, M., Gonzalez-Charneco, K., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4510 · Cited by 38 · see citing works
Extensive zygotic control of the anteroposterior axis in the wasp Nasonia vitripennis
Pultz, M. A., Pitt, J. N., & Alto, N. M. (1999) · Development · doi:10.1242/dev.126.4.701 · Cited by 36 · see citing works
DeCamillis, M., Lewis, D. L., Brown, S. J., et al. (2001) · Genetics · doi:10.1093/genetics/159.4.1643 · Cited by 34 · see citing works
Identification and expression of the gap segmentation gene hunchback in drosophila melanogaster
Bender, M. T., Horikami, S. M., Cribbs, D. L., et al. (1988) · Developmental Genetics · doi:10.1002/dvg.1020090604 · Cited by 32 · see citing works
Normal and ectopic domains of the homeotic gene Sex combs reduced of Drosophila
Pelaz, S., Urquía, N., & Morata, G. (1993) · Development · doi:10.1242/dev.117.3.917 · Cited by 15 · see citing works
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Evolution of Gene Regulatory Networks Controlling Body Plan Development
Peter, I. S., & Davidson, E. H. (2011) · Cell · doi:10.1016/j.cell.2011.02.017 · Cited by 417 · see citing works
Kotkamp, K., Klingler, M., & Schoppmeier, M. (2010) · Development · doi:10.1242/dev.047043 · Cited by 41 · see citing works
- 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
- Publisher
- The Company of Biologists
- 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
- bronze
- doi.org
- 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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