Asymmetric inheritance of cytoophidia in Schizosaccharomyces pombe

Abstract

A general view is that Schizosaccharomyces pombe undergoes symmetric cell division with two daughter cells inheriting equal shares of the content from the mother cell. Here we show that CTP synthase, a metabolic enzyme responsible for the de novo synthesis of the nucleotide CTP, can form filamentous cytoophidia in the cytoplasm and nucleus of S. pombe cells. Surprisingly, we observe that both cytoplasmic and nuclear cytoophidia are asymmetrically inherited during cell division. Our time-lapse studies suggest that cytoophidia are dynamic. Once the mother cell divides, the cytoplasmic and nuclear cytoophidia independently partition into one of the two daughter cells. Although the two daughter cells differ from one another morphologically, they possess similar chances of inheriting the cytoplasmic cytoophidium from the mother cell, suggesting that the partition of cytoophidium is a stochastic process. Our findings on asymmetric inheritance of cytoophidia in S. pombe offer an exciting opportunity to study the inheritance of metabolic enzymes in a well-studied model system.

The Cytoophidium and Its Kind: Filamentation and Compartmentation of Metabolic Enzymes

“…They also demonstrated that CTPS localizes to filamentary structures in Drosophila melanogaster and in rat hippocampal neurons (Noree et al 2010). Subsequent studies have shown that CTPS can also form filaments in human cells (Carcamo et al 2011, Chen et al 2011) and fission yeast (Zhang et al 2014). Thus, the cytoophidium represents a new type of intracellular compartment that is strikingly conserved across prokaryotes and eukaryotes (Liu 2011).…”

“…A eukaryotic cell might contain both cytoplasmic cytoophidia and nuclear cytoophidia (Carcamo et al 2014, Gou et al 2014, Shen et al 2016, Zhang et al 2014). If not specified, the term cytoophidia refers to cytoplasmic cytoophidia.…”

“…Both cytoplasmic and nuclear cytoophidia can be observed in the fission yeast Schizosaccharomyces pombe (Zhang et al 2014). …”

“…Thus, the frequency of cytoophidia can be variable in different cell types. During cell division in S. pombe, only one of the two daughter cells inherits the cytoophidium from the mother cell, whereas the other daughter cell synthesizes a new cytoophidium (Zhang et al 2014). In multicellular organisms, the occurrence of cytoophidia seems complicated.…”

“…In C. crescentus, CTPS filaments translocate from the cell center to the periphery and are eventually anchored in the inner curvature (Ingerson-Mahar et al 2010). In S. pombe, cytoplasmic cytoophidia move constrainedly in certain regions, whereas nuclear cytoophidia act at the periphery of the nucleus (Zhang et al 2014). The dynamics of cytoophidia have also been studied in budding yeast and mammalian cells (Gou et al 2014, Shen et al 2016).…”