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Mechanical control of morphogenesis robustness

Emmanuel Martin, Sophie Theis, Guillaume Gay, Bruno Monier, Magali Suzanne

Preprint posted on January 06, 2020 https://www.biorxiv.org/content/10.1101/2020.01.06.896266v1

Feel the force - anisotropic tissue tension, away from cell shape changes, is essential for morphogenesis robustness in Drosophila leg formation

Selected by Helen Zenner

Categories: developmental biology

Feel the force – anisotropic tissue tension away from cell shape changes is essential for morphogenesis robustness in Drosophila leg formation

Background

Patterning is essential for ensuring that morphogenetic events occur with appropriate timing and position.  The best known process is the specification of body plans by the Hox genes.  Patterning genes are ordinally transcriptional factors that control huge gene networks, including cytoskeletal regulators, which are responsible for the downstream changes in cell behaviour and shape.  More recently, research in this area has focussed on morphogenesis robustness, which refers to the idea of constraining the level of variation, in processes where variation is likely to occur.  The latest preprint from the Suzanne group highlights the importance of the actin cytoskeleton in ensuring morphogenesis robustness, in a separate process to generating force in the morphogenetic event itself. The model used by Martin et al. was the Drosophila leg.  During development the forming appendage must form four strictly parallel folds.  How this patterning occurs has been well described and is dependent on sequential Notch activation, expression of pro-apoptotic genes, subsequent force generation by apical myosin in the apoptotic cells, resulting in constriction and tissue folding.

Findings

Using an RNAi screen, the authors found that depletion of Arp2/3 caused defects in folding, but with a highly variable array of phenotypes, making it a good candidate for involvement in morphogenesis robustness.  When focussing on Arpc5 knockdown, they found no defects in Notch activation, apoptotic pattern formation, or the ability of these cells to send mechanical signals to induce the fold.  In fact, they found that the folds are initially correctly positioned but then lose their way, heading for regions enriched in Myosin II (MyoII) and under high tension.  These findings are recapitulated in silico, when a mechanical perturbation, in close vicinity to the fold, is introduced into a previously published computational model from the authors.

However, these regions of high tension are also present in the wild type tissue, but in this case, the fold formations are immune to its effects, indicating that isolation is required between fold domains and the rest of the tissue.  The authors speculated that this isolation arises from the planar polarised enrichment of MyoII and the resulting anisotropic junctional tension, directing biased force transmission. To test whether this is important for fold formation, the authors used a non-planar polarised GFP trap to redistribute Myosin Regulatory Light Chain::GFP.  The resulting leg discs recapitulated the Arpc5 phenotype with deviated folds.  Because the authors have the in silico model they are also able ask the converse question, whether introducing planar polarity into a non-polarised tissue is sufficient to rescue the fold formation, and find that it is.

Overall this preprint combines elegant experiments, both in vivo and in silico to describe a new, direct role for the actin cytoskeleton in morphogenesis robustness.

Questions arising from this work

  1. Is the role of the actin cytoskeleton a process novel to Drosophila leg development, or general feature of tissues undergoing morphogenesis?
  2. Is Arp2/3 complex itself planar polarised and how does it transduce planar polarity to MyoII?
  3. Is the planar polarity of the tissue more generally disrupted and does this have any functional consequences independent of tissue folding?

Hox info – McGinnis and Krumlauf, 1992

The science behind the folds – de Celis et al., 1998; Rauskolb and Irvine, 1999 Manjón et al., 2007

What is morphogenesis robustness – Frankel et al., 2010; Smith et al., 2018

Tags: actin, cytoskeleton, drosophila, morphogenesis robustness, patterning

Posted on: 10th February 2020

doi: https://doi.org/10.1242/prelights.16742

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