The vacuole controls nucleolar dynamics and micronucleophagy via the NVJ

Chromosomes have their own territories and dynamically translocate in response to internal and external cues. However, whether and how territories and the relocation of chromosomes are controlled by other intracellular organelles remains unknown. Upon nutrient starvation and target of rapamycin complex 1 (TORC1) inactivation, micronucleophagy, which preferentially degrades nucleolar proteins, occurs at the nucleus-vacuole junction (NVJ) in budding yeast. Ribosomal DNA (rDNA) is condensed and relocated against the NVJ, whereas nucleolar proteins move towards the NVJ for micronucleophagic degradation, causing dissociation of nucleolar proteins from rDNA. These findings imply that the NVJ is the critical platform in the directional movements of rDNA and nucleolar proteins. Here, we show that cells lacking the NVJ (NVJD cells) largely lost rDNA condensation and rDNA-nucleolar protein separation after TORC1 inactivation. The macronucleophagy receptor Atg39, an outer nuclear membrane protein, accumulated at the NVJ and was degraded by micronucleophagy. These suggested that macronucleophagy is also dependent on the presence of the NVJ. However, micronucleophagy, but not macronucleophagy, was abolished in NVJD cells. This study clearly demonstrated that vacuoles controls intranuclear events, nucleolar dynamics, from outside of the nucleus via the NVJ under the control of TORC1. (c) 2021 Elsevier Inc. All rights reserved.

Automated summary

The study demonstrates that in budding yeast, nutrient starvation and TORC1 inactivation trigger micronucleophagy at the nucleus-vacuole junction (NVJ), leading to condensation of rDNA and movement of nucleolar proteins towards the NVJ for degradation. These findings suggest that the NVJ plays a critical role in the directional movements of rDNA and nucleolar proteins.