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

Shinya Matsuda (), Jonas V. Schaefer, Yusuke Mii, Yutaro Hori, Dimitri Bieli, Masanori Taira, Andreas Plückthun and Markus Affolter ()
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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
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
Andreas Plückthun: University of Zurich
Markus Affolter: Biozentrum, University of Basel

Nature Communications, 2021, vol. 12, issue 1, 1-18

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-26726-6

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