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Patterning potential of the terminal system in the Drosophila embryo

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Abstract

Segmentation of the Drosophila embryo is initiated by localized maternal signals. In this context, anteriorly localized Bicoid activates the gap genes in the anterior half of the embryo while posteriorly localized Nanos represses the translation of maternal hunchback mRNA to pattern the posterior half. The non-segmented termini are patterned by the localized activation of mitogen-activated protein kinase. Yet, the spatial extent of the terminal patterning system in regulating gap genes beyond poles remains unknown. We investigated the patterning potential of the terminal system using mutagenized embryos that lack both the anterior and the posterior maternal signaling systems. Using a combination of quantitative imaging and mathematical modeling, we analyzed the spatial patterns of gap genes in the early Drosophila embryo. We found that this mutant embryo develops symmetric cuticle patterns along the anteroposterior axis with two segments on each side. Notably, the terminal system can affect the expression of Krüppel in the torso region. Our mathematical model recapitulates the experimental data and reveals the potential bistability in the terminal patterning system. Collectively, our study suggests that the terminal system can act as a long-range inductive signal and establish multiple gene expression boundaries along the anteroposterior axis of the develo** embryo.

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Abbreviations

OreR:

Oregon R

AP:

Anteroposterior

Bcd:

Bicoid

Hb:

Hunchback

MAPK:

Mitogen-activated protein kinase

ERK:

Extracellular signal-regulated kinase

dpERK:

Diphosphorylated ERK

Tor:

Torso

Trk:

Trunk

Tll:

Tailless

Hkb:

Huckebein

Cic:

Capicua

Gro:

Groucho

FISH:

Fluorescent in situ hybridization

PBS:

Phosphate-buffered saline

PBST:

Phosphate buffered saline with 0.02% Triton X-100

DIG:

Digoxigenin

BIO:

Biotin

FITC:

Fluorescein

WBR:

Western blocking reagent

BSA:

Bovine serum albumin

NGS:

Normal goat serum

Kr:

Krüppel

Kni:

Knirps

Gt:

Giant

GOF:

Gain-of-function

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Acknowledgements

We thank Dr. Eric Wieschaus for providing bcd hb nos mutant flies and for the helpful discussions. K. M. O. was supported by thesis research funds by Princeton University. Y.K. was supported by the internal fund of Electronics and Telecommunications Research Institute (ETRI) [22RB1100, Exploratory and Strategic Research of ETRI-KAIST ICT Future Technology (Grant number: N05220126)].

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Author notes

  1. These authors contributed equally.

Authors and Affiliations

  1. Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon, 34141, Korea

    Keonyong Lee, Jayoung Ku & Yoosik Kim

  2. Institute for Physical Science and Technology, University of Maryland, College Park, MD, 20742, USA

    Kate Molloy O’Neill

  3. Department of Chemical and Biological Engineering, Princeton University, Princeton, NJ, 08540, USA

    Kate Molloy O’Neill

  4. Lewis Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, 08540, USA

    Stanislav Yefimovic Shvartsman

  5. Center for Computational Biology, Flatiron Institute, Simon Foundation, New York, NY, 10010, USA

    Stanislav Yefimovic Shvartsman

  6. Department of Molecular Biology, Princeton University, Princeton, NJ, 08540, USA

    Stanislav Yefimovic Shvartsman

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  1. Keonyong Lee
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  2. Kate Molloy O’Neill
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  3. Jayoung Ku
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  4. Stanislav Yefimovic Shvartsman
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Correspondence to Yoosik Kim.

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Author Contribution

K.M.O., S.Y.S., and Y.K. designed the experiments, K.M.O. and Y.K. performed the experiments. K.L., K.M.O., and J.K., performed image analysis. K.L., K.M.O., and Y.K. wrote the paper. All authors analyzed the data.

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Lee, K., O’Neill, K.M., Ku, J. et al. Patterning potential of the terminal system in the Drosophila embryo. Korean J. Chem. Eng. 40, 436–444 (2023). https://doi.org/10.1007/s11814-022-1298-6

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  • DOI: https://doi.org/10.1007/s11814-022-1298-6

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