RT Journal Article
SR Electronic
T1 Dynamics of altruistic fluid transport in egg development
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 2020.06.16.155606
DO 10.1101/2020.06.16.155606
A1 Alsous J Imran
A1 N Romeo
A1 J Jackson
A1 FM Mason
A1 J Dunkel
A1 AC Martin
YR 2020
UL http://biorxiv.org/content/early/2020/06/17/2020.06.16.155606.abstract
AB Interactions in which individuals benefit others at a cost to themselves are rife within the animal kingdom1, from stalk cells in slime mold fruiting bodies2 to social insect colonies where sterile workers live for the queen3. The development of an egg cell occurs within similarly self-sacrificing communes. Across species, oocytes develop within cysts alongside nurse-like germ cells; a key juncture in oogenesis occurs when these sister cells transport their cytoplasm to the oocyte prior to fertilization4,5. As a result, the oocyte grows as its sister cells regress and die6. Long observed in insects, recent work shows that development of the mammalian egg cell occurs through similar intercellular transport processes7,8. Although critical for fertility and embryonic life, the biological and physical mechanisms underlying such altruistic fluid transport remain poorly understood, owing to a lack of time-resolved quantitative data. Here, we combined ex vivo live imaging of germline cysts with mathematical modeling to investigate the dynamics and mechanisms that enable directional and complete cytoplasmic transport in Drosophila melanogaster egg chambers. We discovered that during ‘nurse cell dumping’, most cytoplasm is transported into the oocyte independently of changes in myosin-II contractility, with dynamics predicted by Young-Laplace’s law, suggesting pressure-driven transport induced by baseline cell surface tension. A minimal flow network model inspired by the famous two-balloon experiment correctly predicts transport directionality and time scale. Long thought to trigger transport through ‘squeezing’9,10, increased actomyosin contractility is required only once cell volume is reduced by ∼75%, in the form of cell peristaltic contractile waves that permit continued flow. Our work thus demonstrates how biological and physical mechanisms cooperate to enable proper cell and tissue level behaviours during a conserved act of cytoplasmic transport in early development.Competing Interest StatementThe authors have declared no competing interest.