Interorganelle interactions and inheritance patterns of nuclei and vacuoles in budding yeast meiosis

Abstract

Many of the mechanisms by which organelles are inherited by spores during meiosis are not well understood. Dramatic chromosome motion and bouquet formation are evolutionarily conserved characteristics of meiotic chromosomes. The budding yeast bouquet genes (NDJ1, MPS3, CSM4) mediate these movements via telomere attachment to the nuclear envelope (NE). Here, we report that during meiosis the NE is in direct contact with vacuoles via nucleus-vacuole junctions (NVJs). We show that in meiosis NVJs are assembled through the interaction of the outer NE-protein Nvj1 and the vacuolar membrane protein Vac8. Notably, NVJs function as diffusion barriers that exclude the nuclear pore complexes, the bouquet protein Mps3 and NE-tethered telomeres from the outer nuclear membrane and nuclear ER, resulting in distorted NEs during early meiosis. An increase in NVJ area resulting from Nvj1-GFP overexpression produced a moderate bouquet mutant-like phenotype in wild-type cells. NVJs, as the vacuolar contact sites of the nucleus, were found to undergo scission alongside the NE during meiotic nuclear division. The zygotic NE and NVJs were partly segregated into 4 spores. Lastly, new NVJs were also revealed to be synthesized de novo to rejoin the zygotic NE with the newly synthesized vacuoles in the mature spores. In conclusion, our results revealed that budding yeast nuclei and vacuoles exhibit dynamic interorganelle interactions and different inheritance patterns in meiosis, and also suggested that nvj1Δ mutant cells may be useful to resolve the technical challenges pertaining to the isolation of intact nuclei for the biochemical study of meiotic nuclear proteins.

Development and use of a quantum dot probe to track multiple yeast strains in mixed culture

“…1d ). These results are consistent with previous studies that have documented the transfer of cytosol, vacuole, and GSH from mother cell to daughter cell in S. cerevisiae 6 7 .…”

“…This may ultimately affect yeast growth and fermentation kinetics. Also, because only a select few organelles are transferred from mother cells to daughter cells during cell division 6 7 , stains that are not directly taken up or absorbed by the yeast cannot be transferred to newly formed cells 8 .…”

“…Yeast are able to metabolize GSH as a sole source of sulfur, or otherwise transfer a portion to storage vacuoles to be used at a later time. Therefore, fluorescent tags bound to GSH can be taken up by yeast and transferred within the cytosol and vacuoles—both of which are transferred from the mother cell to daughter cells during cell division 6 7 . Commercial kits (i.e., CellTracker™ Invitrogen™, Burlington, Ontario) successfully exploit some of these inherent properties of glutathione.…”

Developmental regulation of an organelle tether coordinates mitochondrial remodeling in meiosis

“…A key cellular differentiation program in budding yeast is gametogenesis, which includes segregation of chromosomes by meiosis and the production of specialized gamete cells called spores. Various organelles, including mitochondria, undergo extensive remodeling during this process (Stevens, 1981; Miyakawa et al, 1984; Neiman, 1998; Fuchs and Loidl, 2004; Gorsich and Shaw, 2004; Suda et al, 2007; Tsai et al, 2014). Mitochondrial distribution changes dramatically during the meiotic divisions, when mitochondria lose their plasma membrane association, instead localizing near the gamete nuclei (Stevens, 1981; Miyakawa et al, 1984; Gorsich and Shaw, 2004).…”

Developmental Regulation of an Organelle Tether Coordinates Mitochondrial Remodeling in Meiosis

“…The principal cellular differentiation program in budding yeast is gametogenesis, which includes segregation of chromosomes by meiosis and the production of specialized gamete cells called spores. Various organelles, including mitochondria, undergo extensive remodeling during this process (Fuchs and Loidl, 2004;Gorsich and Shaw, 2004;Miyakawa et al, 1984;Neiman, 1998;Stevens, 1981;Suda et al, 2007;Tsai et al, 2014). Mitochondrial distribution changes dramatically during the meiotic divisions, when mitochondria lose their plasma membrane association, instead localizing near the gamete nuclei (Gorsich and Shaw, 2004;Miyakawa et al, 1984;Stevens, 1981).…”