Developmental Regulation of an Organelle Tether Coordinates Mitochondrial Remodeling in Meiosis

Sawyer, Eric M.; Joshi, Pallavi; Berchowitz, Luke E.; Ünal, Elçin

doi:10.1101/376509

Cited by 10 publications

(14 citation statements)

References 103 publications

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“…To mark the different organelles, yeast strains endogenously expressing C-terminal GFP fusions of proteins known to localize to the organelle of interest were used in most cases. Peroxisomes were visualized via Pex3-GFP (Huh et al, 2003), vacuoles were visualized via Vph1-GFP (Lu and Drubin, 2020), mitochondria were visualized via Cit1-GFP (Sawyer et al, 2019), and nuclei were visualized via Nup59-GFP (Madrid et al, 2006). The ER was visualized via expression of a single copy of GFP-HDEL integrated into the genome at the TPI1 locus (Lu and Drubin, 2020).…”

Section: Resultsmentioning

confidence: 99%

An organelle inheritance pathway during polarized cell growth

Pedersen

et al. 2021

Preprint

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Some organelles cannot be synthesized anew, so they are segregated into daughter cells during cell division. In Saccharomyces cerevisiae, daughter cells bud from mother cells and are populated by organelles inherited from the mothers. To determine whether this organelle inheritance occurs in a stereotyped manner, we tracked organelles using fluorescence microscopy. We describe a program for organelle inheritance in budding yeast. The cortical endoplasmic reticulum (ER) and peroxisomes are inherited concomitant with bud emergence. Next, vacuoles are inherited in small buds, followed closely by mitochondria. Finally, the nucleus and perinuclear ER are inherited when buds have nearly reached their maximal size. Because organelle inheritance timing correlates with bud morphology, which is coupled to the cell cycle, we tested whether organelle inheritance order is controlled by the cell cycle. By arresting cell cycle progression but allowing continued bud growth, we determined that organelle inheritance still occurs without cell cycle progression past S-phase, and that the general inheritance order is maintained. Thus, organelle inheritance follows a preferred order during polarized cell division, but it is not controlled exclusively by cell cycle signaling.

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Section: Resultsmentioning

confidence: 99%

An organelle inheritance pathway during polarized cell growth

Pedersen

et al. 2021

Preprint

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“…Identifying the cellular pathways that must converge to completely rejuvenate gametes remains an active area of research. In particular, the cDNA libraries could be used in gain-of-function screens in mitotic cells to identify regulators of meiosis-specific gene expression, organelle remodeling, and quality control pathways (Neiman, 2005; Otto et al, 2021; Sawyer et al, 2019; Suda et al, 2007). Furthermore, gametogenesis has been shown to eliminate many types of age-associated senescence factors including excess nucleolar material, protein aggregates, and non-chromosomal ribosomal DNA (rDNA) circles (King et al, 2019; King and Ünal 2020).…”

Section: Discussionmentioning

confidence: 99%

“…In addition to dividing the genome, gamete formation also requires that gametes acquire organelles, either through inheritance prior to gamete membrane closure or through de novo synthesis (King et al, 2019; Otto et al, 2021; Sawyer et al, 2019; Suda et al, 2007). When gamete formation is complete, the lysosome-equivalent vacuole that originates from the mother precursor cell lyses and degrades all cellular content that was not inherited by the four gametes (Eastwood and Meneghini, 2015; Eastwood et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Comprehensive analysis of meiosis-derived cDNA libraries reveals gene isoforms and mitochondrial proteins important for competitive fitness

Sing

Conlon

et al. 2021

Preprint

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Gametogenesis is a highly regulated and dynamic developmental program where a diploid progenitor cell differentiates into haploid gametes, the precursors for sexual reproduction. During meiosis, several pathways converge to initiate ploidy reduction and organelle remodelling to render gametes competent for zygote formation and subsequent organismal development. Additionally, meiosis inherently rejuvenates the newly formed gametes resulting in lifespan resetting. Here, we construct five stage-specific, inducible meiotic cDNA libraries that represent over 84% of the yeast genome. We employ computational strategies to detect stage-specific meiotic transcript isoforms in each library and develop a robust screening pipeline to test the effect of each cDNA on competitive fitness. Our multi-day proof-of-principle time course reveals gene isoforms that are important for competitive fitness as well as mitochondrial proteins that cause dose-dependent disruption of respiration. Together, these novel meiotic cDNA libraries provide an important resource for systematically studying meiotic genes and gene isoforms in future studies.

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“…All experimental strains are diploid Saccharomyces cerevisiae derivatives of the SK1 strain as detailed in supplemental table 1. The following alleles were derived from previous studies: pGAL-NDT80 and GAL4.ER (Benjamin et al, 2003; Carlile and Amon, 2008), pCLB2-CDC20 (Lee and Amon, 2003), pCUP1-oSTIR (Sawyer et al, 2019), mKate-SPO20 51-91 and VPH1-mCherry (King et. al., 2019), HTB1-mCherry (Matos et al, 2008), ndt80Δ (Xu et al, 1995), GFP-ATG8 (Graef et al, 2013).…”

Section: Methodsmentioning

confidence: 99%

Programmed ER fragmentation drives selective ER inheritance and degradation in budding yeast meiosis

Gm¹,

Cheunkarndee²,

Jm³

et al. 2021

Preprint

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The endoplasmic reticulum (ER) is a membrane-bound organelle with diverse, essential functions that rely on the maintenance of membrane shape and distribution within cells. ER structure and function are remodeled in response to changes in cellular demand, such as the presence of external stressors or the onset of cell differentiation, but mechanisms controlling ER remodeling during cell differentiation are not well understood. Here, we describe a series of developmentally regulated changes in ER morphology and composition during budding yeast meiosis, a conserved differentiation program that gives rise to gametes. During meiosis, the cortical ER undergoes fragmentation before collapsing away from the plasma membrane at anaphase II. This programmed collapse depends on the meiotic transcription factor Ndt80, conserved ER membrane structuring proteins Lnp1 and reticulons, and the actin cytoskeleton. A subset of ER is retained at the mother cell plasma membrane and excluded from gamete cells via the action of ER-plasma membrane tethering proteins. ER remodeling is coupled to ER degradation by selective autophagy, which is regulated by the developmentally timed expression of the autophagy receptor Atg40. Autophagy relies on ER collapse, as artificially targeting ER proteins to the cortically retained ER pool prevents their degradation. Thus, developmentally programmed changes in ER morphology determine the selective degradation or inheritance of ER subdomains by gametes.

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Developmental Regulation of an Organelle Tether Coordinates Mitochondrial Remodeling in Meiosis

Cited by 10 publications

References 103 publications

An organelle inheritance pathway during polarized cell growth

An organelle inheritance pathway during polarized cell growth

Comprehensive analysis of meiosis-derived cDNA libraries reveals gene isoforms and mitochondrial proteins important for competitive fitness

Programmed ER fragmentation drives selective ER inheritance and degradation in budding yeast meiosis

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