Positive feedback between golgi membranes, microtubules and ER-exit sites directs golgi de novo biogenesis

Abstract

The Golgi complex is the central organelle of the secretory pathway. It undergoes dynamic changes during the cell cycle, but how it acquires and maintains its complex structure is unclear. To address this question we have used laser nanosurgery to deplete cells of the Golgi complex and monitored its biogenesis by quantitative time-lapse microscopy and correlative electron microscopy. After Golgi depletion, ER export is inhibited and the number of ER-exit sites (ERES) is reduced and does not increase for several hours. Occasional fusion of small post-ER carriers to form the first larger structures triggers a rapid and drastic growth of Golgi precursors, due to the capacity of these structures to attract more carriers via microtubule nucleation and to stimulate ERES biogenesis. Increasing the chances of post-ER carrier fusion close to ERES by depolymerizing microtubules results in the acceleration of Golgi and ERES biogenesis. Altogether, our results propose a self-organizing principle of the early secretory pathway that integrates Golgi biogenesis, ERES biogenesis and the organization of the microtubule network by positive feedback loops.