Endoplasmic-reticulum-mediated microtubule alignment governs cytoplasmic streaming

Through imaging and theoretical modelling, Kimura et al. discover that endoplasmic reticulum flow determines microtubule alignment to promote cytoplasmic streaming of yolk granules in Caenorhabditis elegans zygotes. Cytoplasmic streaming refers to a collective movement of cytoplasm observed in many cell types 1 , 2 , 3 , 4 , 5 , 6 , 7 . The mechanism of meiotic cytoplasmic streaming (MeiCS) in Caenorhabditis elegans zygotes is puzzling as the direction of the flow is not predefined by cell polarity and occasionally reverses 6 . Here, we demonstrate that the endoplasmic reticulum (ER) network structure is required for the collective flow. Using a combination of RNAi, microscopy and image processing of C. elegans zygotes, we devise a theoretical model, which reproduces and predicts the emergence and reversal of the flow. We propose a positive-feedback mechanism, where a local flow generated along a microtubule is transmitted to neighbouring regions through the ER. This, in turn, aligns microtubules over a broader area to self-organize the collective flow. The proposed model could be applicable to various cytoplasmic streaming phenomena in the absence of predefined polarity. The increased mobility of cortical granules by MeiCS correlates with the efficient exocytosis of the granules to protect the zygotes from osmotic and mechanical stresses.