Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis

Abstract

It is unknown how growth in one tissue impacts morphogenesis in a neighboring tissue. To address this, we used the Drosophila ovarian follicle, in which a cluster of 15 nurse cells and a posteriorly located oocyte are surrounded by a layer of epithelial cells. It is known that as the nurse cells grow, the overlying epithelial cells flatten in a wave that begins in the anterior. Here, we demonstrate that an anterior to posterior gradient of decreasing cytoplasmic pressure is present across the nurse cells and that this gradient acts through TGFβ to control both the triggering and the progression of the wave of epithelial cell flattening. Our data indicate that intrinsic nurse cell growth is important to control proper nurse cell pressure. Finally, we reveal that nurse cell pressure and subsequent TGFβ activity in the stretched cells combine to increase follicle elongation in the anterior, which is crucial for allowing nurse cell growth and pressure control. More generally, our results reveal that during development, inner cytoplasmic pressure in individual cells has an important role in shaping their neighbors.

A hydro-osmotic coarsening theory of biological cavity formation

“…To test and challenge this aspect, it could be interesting to artificially merge two or more embryos before blastulation to see if several, uncoupled, cavities may form. Beyond lumenogenesis, we expect our theory to be relevant for describing the hydraulic cell coarsening phenomena underlying Drosophila and C. elegans oogenesis Alsous et al ( 2021 ); Lamiré et al ( 2020 ); Chartier et al ( 2020 ). As we showed earlier Dumortier et al ( 2019 ), gradients of cell mechanical properties can be sufficient to spatially bias lumen coarsening, and this mechanism is the main symmetry breaking process put forward to explain cell competition in oogenesis as well.…”

“…Here, we have shown that active ion pumping may be an additional source of spatial bias for coarsening. Active osmotic volume control emerges hence as a novel mode of symmetry breaking for tissue patterning, that could be relevant also to oogenesis Alsous et al ( 2021 ); Lamiré et al ( 2020 ); Chartier et al ( 2020 ), liquid phase transition of biological condensates Jalihal et al ( 2021 ) and plant tissue growth Cheddadi et al ( 2019 ); Long et al ( 2020 ). Active ion pumping can also largely affect the collective lumen dynamics, with the emergence of a novel coarsening regime dominated by coalescence.…”

“…Hydraulic and osmotic flows are indeed more and more recognized as essential determinants of embryo and tissue shaping Dasgupta et al ( 2018 ); Lamiré et al ( 2020 ); Chan et al ( 2019 ); Dumortier et al ( 2019 ); Narayanan et al ( 2020 ); Alsous et al ( 2021 ); Chartier et al ( 2020 ). However only a few physical models describe the interplay between cell mechanics, osmotic effects and fluid flow in morphogenesis Alim ( 2018 ); Cheddadi et al ( 2019 ); Dolega et al ( 2021 ); Long et al ( 2020 ) and in previous models, osmolarity is mostly considered spatially homogeneous.…”

“…Hydraulic and osmotic flows are indeed more and more recognized as essential determinants of embryo and tissue shaping [18,[35][36][37][38][39][40]. However only a few physical models describe the interplay between cell mechanics, osmotic effects and fluid flow in morphogenesis [41][42][43][44], and in all those previous models, osmolarity is considered July 15, 2021 2/21 spatially homogeneous.…”

“…Here, we propose a generic physical model to describe the hydro-osmotic coupling between pressurized compartments, explicitly accounting for osmotic gradients and ion pumping. Our model may therefore also form a relevant theoretical framework to describe the coupled dynamics between nurse cells and the future oocyte during Drosophila oogenesis [36,39], or between germ cells in the nematode C elegans [40]. Here, we do not study however the initial nucleation of small cavities.…”