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Asymmetric requirement of Dpp/BMP morphogen dispersal in the Drosophila wing disc

Author

Listed:
  • Shinya Matsuda

    (Biozentrum, University of Basel)

  • Jonas V. Schaefer

    (University of Zurich)

  • Yusuke Mii

    (National Institute for Basic Biology and Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences
    JST PRESTO)

  • Yutaro Hori

    (Institute for Quantitative Biosciences, The University of Tokyo)

  • Dimitri Bieli

    (Biozentrum, University of Basel)

  • Masanori Taira

    (Graduate School of Science, The University of Tokyo
    Faculty of Science and Engineering, Chuo University)

  • Andreas Plückthun

    (University of Zurich)

  • Markus Affolter

    (Biozentrum, University of Basel)

Abstract

How morphogen gradients control patterning and growth in developing tissues remains largely unknown due to lack of tools manipulating morphogen gradients. Here, we generate two membrane-tethered protein binders that manipulate different aspects of Decapentaplegic (Dpp), a morphogen required for overall patterning and growth of the Drosophila wing. One is “HA trap” based on a single-chain variable fragment (scFv) against the HA tag that traps HA-Dpp to mainly block its dispersal, the other is “Dpp trap” based on a Designed Ankyrin Repeat Protein (DARPin) against Dpp that traps Dpp to block both its dispersal and signaling. Using these tools, we found that, while posterior patterning and growth require Dpp dispersal, anterior patterning and growth largely proceed without Dpp dispersal. We show that dpp transcriptional refinement from an initially uniform to a localized expression and persistent signaling in transient dpp source cells render the anterior compartment robust against the absence of Dpp dispersal. Furthermore, despite a critical requirement of dpp for the overall wing growth, neither Dpp dispersal nor direct signaling is critical for lateral wing growth after wing pouch specification. These results challenge the long-standing dogma that Dpp dispersal is strictly required to control and coordinate overall wing patterning and growth.

Suggested Citation

  • Shinya Matsuda & Jonas V. Schaefer & Yusuke Mii & Yutaro Hori & Dimitri Bieli & Masanori Taira & Andreas Plückthun & Markus Affolter, 2021. "Asymmetric requirement of Dpp/BMP morphogen dispersal in the Drosophila wing disc," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26726-6
    DOI: 10.1038/s41467-021-26726-6
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    References listed on IDEAS

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    1. Holger Apitz & Iris Salecker, 2018. "Spatio-temporal relays control layer identity of direction-selective neuron subtypes in Drosophila," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    2. Stefan Harmansa & Fisun Hamaratoglu & Markus Affolter & Emmanuel Caussinus, 2015. "Dpp spreading is required for medial but not for lateral wing disc growth," Nature, Nature, vol. 527(7578), pages 317-322, November.
    3. Takuya Akiyama & Matthew C. Gibson, 2015. "Decapentaplegic and growth control in the developing Drosophila wing," Nature, Nature, vol. 527(7578), pages 375-378, November.
    4. Takashi Adachi-Yamada & Konomi Fujimura-Kamada & Yasuyoshi Nishida & Kunihiro Matsumoto, 1999. "Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing," Nature, Nature, vol. 400(6740), pages 166-169, July.
    5. Frank Hsiung & Felipe-Andrès Ramirez-Weber & D. David Iwaki & Thomas B. Kornberg, 2005. "Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic," Nature, Nature, vol. 437(7058), pages 560-563, September.
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    7. Fisun Hamaratoglu & Aitana Morton de Lachapelle & George Pyrowolakis & Sven Bergmann & Markus Affolter, 2011. "Dpp Signaling Activity Requires Pentagone to Scale with Tissue Size in the Growing Drosophila Wing Imaginal Disc," PLOS Biology, Public Library of Science, vol. 9(10), pages 1-17, October.
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    1. Sharif M. Ridwan & Autumn Twillie & Samaneh Poursaeid & Emma Kristine Beard & Muhammed Burak Bener & Matthew Antel & Ann E. Cowan & Shinya Matsuda & Mayu Inaba, 2024. "Diffusible fraction of niche BMP ligand safeguards stem-cell differentiation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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