Dynamic Patterning by the Drosophila Pair-rule Network Reconciles Long-germ and Short-germ Segmentation

Overview

Journal PLoS Biol

Specialty Biology

Date 2017 Sep 28

PMID 28953896

Citations 43

Authors

Erik Clark

Affiliations

Soon will be listed here.

Abstract

Drosophila segmentation is a well-established paradigm for developmental pattern formation. However, the later stages of segment patterning, regulated by the "pair-rule" genes, are still not well understood at the system level. Building on established genetic interactions, I construct a logical model of the Drosophila pair-rule system that takes into account the demonstrated stage-specific architecture of the pair-rule gene network. Simulation of this model can accurately recapitulate the observed spatiotemporal expression of the pair-rule genes, but only when the system is provided with dynamic "gap" inputs. This result suggests that dynamic shifts of pair-rule stripes are essential for segment patterning in the trunk and provides a functional role for observed posterior-to-anterior gap domain shifts that occur during cellularisation. The model also suggests revised patterning mechanisms for the parasegment boundaries and explains the aetiology of the even-skipped null mutant phenotype. Strikingly, a slightly modified version of the model is able to pattern segments in either simultaneous or sequential modes, depending only on initial conditions. This suggests that fundamentally similar mechanisms may underlie segmentation in short-germ and long-germ arthropods.

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References

Klingler M, Gergen J . Regulation of runt transcription by Drosophila segmentation genes. Mech Dev. 1993; 43(1):3-19. DOI: 10.1016/0925-4773(93)90019-t. View

Peel A, Chipman A, Akam M . Arthropod segmentation: beyond the Drosophila paradigm. Nat Rev Genet. 2005; 6(12):905-16. DOI: 10.1038/nrg1724. View

Hiromi Y, Kuroiwa A, Gehring W . Control elements of the Drosophila segmentation gene fushi tarazu. Cell. 1985; 43(3 Pt 2):603-13. DOI: 10.1016/0092-8674(85)90232-6. View

Manoukian A, Krause H . Concentration-dependent activities of the even-skipped protein in Drosophila embryos. Genes Dev. 1992; 6(9):1740-51. DOI: 10.1101/gad.6.9.1740. View

Edgar B, Odell G, Schubiger G . A genetic switch, based on negative regulation, sharpens stripes in Drosophila embryos. Dev Genet. 1989; 10(3):124-42. DOI: 10.1002/dvg.1020100303. View

Jaeger J, Blagov M, Kosman D, Kozlov K, Manu , Myasnikova E . Dynamical analysis of regulatory interactions in the gap gene system of Drosophila melanogaster. Genetics. 2004; 167(4):1721-37. PMC: 1471003. DOI: 10.1534/genetics.104.027334. View

Swantek D, Gergen J . Ftz modulates Runt-dependent activation and repression of segment-polarity gene transcription. Development. 2004; 131(10):2281-90. DOI: 10.1242/dev.01109. View

Small S, Kraut R, Hoey T, Warrior R, Levine M . Transcriptional regulation of a pair-rule stripe in Drosophila. Genes Dev. 1991; 5(5):827-39. DOI: 10.1101/gad.5.5.827. View

Fujioka M, Yusibova G, Patel N, Brown S, Jaynes J . The repressor activity of Even-skipped is highly conserved, and is sufficient to activate engrailed and to regulate both the spacing and stability of parasegment boundaries. Development. 2002; 129(19):4411-21. PMC: 2709299. DOI: 10.1242/dev.129.19.4411. View

10.

Coulter D, Wieschaus E . Gene activities and segmental patterning in Drosophila: analysis of odd-skipped and pair-rule double mutants. Genes Dev. 1988; 2(12B):1812-23. DOI: 10.1101/gad.2.12b.1812. View

11.

Clyde D, Corado M, Wu X, Pare A, Papatsenko D, Small S . A self-organizing system of repressor gradients establishes segmental complexity in Drosophila. Nature. 2003; 426(6968):849-53. DOI: 10.1038/nature02189. View

12.

Desponds J, Tran H, Ferraro T, Lucas T, Perez Romero C, Guillou A . Precision of Readout at the hunchback Gene: Analyzing Short Transcription Time Traces in Living Fly Embryos. PLoS Comput Biol. 2016; 12(12):e1005256. PMC: 5152799. DOI: 10.1371/journal.pcbi.1005256. View

13.

Davis I, Ish-Horowicz D . Apical localization of pair-rule transcripts requires 3' sequences and limits protein diffusion in the Drosophila blastoderm embryo. Cell. 1991; 67(5):927-40. DOI: 10.1016/0092-8674(91)90366-7. View

14.

Macdonald P, Struhl G . A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature. 1986; 324(6097):537-45. DOI: 10.1038/324537a0. View

15.

Edgar B, Odell G, Schubiger G . Cytoarchitecture and the patterning of fushi tarazu expression in the Drosophila blastoderm. Genes Dev. 1987; 1(10):1226-37. DOI: 10.1101/gad.1.10.1226. View

16.

Manu , Surkova S, Spirov A, Gursky V, Janssens H, Kim A . Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors. PLoS Comput Biol. 2009; 5(3):e1000303. PMC: 2646127. DOI: 10.1371/journal.pcbi.1000303. View

17.

Akam M . The molecular basis for metameric pattern in the Drosophila embryo. Development. 1987; 101(1):1-22. View

18.

Schulz C, Schroder R, Hausdorf B, Wolff C, Tautz D . A caudal homologue in the short germ band beetle Tribolium shows similarities to both, the Drosophila and the vertebrate caudal expression patterns. Dev Genes Evol. 1998; 208(5):283-9. DOI: 10.1007/s004270050183. View

19.

Janssen R, Budd G, Prpic N, Damen W . Expression of myriapod pair rule gene orthologs. Evodevo. 2011; 2(1):5. PMC: 3058060. DOI: 10.1186/2041-9139-2-5. View

20.

Gursky V, Panok L, Myasnikova E, Manu , Samsonova M, Reinitz J . Mechanisms of gap gene expression canalization in the Drosophila blastoderm. BMC Syst Biol. 2011; 5:118. PMC: 3398401. DOI: 10.1186/1752-0509-5-118. View