Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER

Protein transport from the endoplasmic reticulum (ER) to the Golgi apparatus is mediated by coat complex II (COPII) vesicles. It has been believed that COPII vesicles containing cargo are released from the ER exit sites (ERES) into the cytosol and then reach and fuse with the first post-ER compartment, cis-Golgi or ER-to-Golgi intermediate compartment (ERGIC). However, it still remains elusive how cargo loading to vesicles, vesicle budding, tethering and fusion are coordinated in vivo. Here we show, using extremely high speed and high resolution confocal microscopy, that the cis-Golgi in the budding yeast Saccharomyces cerevisiae approaches and contacts the ERES. The COPII coat cage then collapses and the cis-Golgi captures cargo. The cis-Golgi, thus loaded with cargo, then leaves the ERES. We propose that this ‘hug-and-kiss’ behaviour of cis-Golgi ensures efficient and targeted cargo transport from the ERES to cis-Golgi. Protein traffic from the endoplasmic reticulum (ER) to the Golgi is mediated by COPII-coated vesicles that bud from ER exit sites and fuse with the cis-Golgi. Kurokawa et al. show that in budding yeast, the cis-Golgi reaches out to ER exit sites in a ‘hug-and-kiss’ mechanism to facilitate cargo transfer.