Functional interrelationships between carbohydrate and lipid storage, and mitochondrial activity during sporulation in Saccharomyces cerevisiae

Abstract

In Saccharomyces cerevisiae under conditions of nutrient stress, meiosis precedes the formation of spores. Although the molecular mechanisms that regulate meiosis, such as meiotic recombination and nuclear divisions, have been extensively studied, the metabolic factors that determine the efficiency of sporulation are less understood. Here, we have directly assessed the relationship between metabolic stores and sporulation in S. cerevisiae by genetically disrupting the synthetic pathways for the carbohydrate stores, glycogen (gsy1/2Δ cells), trehalose (tps1Δ cells), or both (gsy1/2Δ and tps1Δ cells). We show that storage carbohydrate‐deficient strains are highly inefficient in sporulation. Although glycogen and trehalose stores can partially compensate for each other, they have differential effects on sporulation rate and spore number. Interestingly, deletion of the G1 cyclin, CLN3, which resulted in an increase in cell size, mitochondria and lipid stores, partially rescued meiosis progression and spore ascus formation but not spore number in storage carbohydrate‐deficient strains. Sporulation efficiency in the carbohydrate‐deficient strain exhibited a greater dependency on mitochondrial activity and lipid stores than wild‐type yeast. Taken together, our results provide new insights into the complex crosstalk between metabolic factors that support gametogenesis.

Characterizing phenotypic diversity of trehalose biosynthesis mutants in multiple wild strains of Saccharomyces cerevisiae

“…Homozygous TPS1 deletion mutants are unable to sporulate in S288C-derived and W303 laboratory strains ( Van Aelst et al 1993 ; de Silva-Udawatta and Cannon 2001 ; Enyenihi and Saunders 2003 ; Gibney et al 2015 ; Liu et al 2020 ). However, this is not a shared phenotype to all laboratory strains as in the SK1 genetic background, we observed that 60% of tps1 Δ mutant cells are still able to sporulate, suggesting that the sporulation defect associated with this mutant may be specific to certain lab strains ( Supplementary Fig.…”

“…Another shared phenotype between tps1 Δ and tps2 Δ mutants is an inability to sporulate in the S288C background ( Sur et al 1994 ; Gibney et al 2015 ; Liu et al 2020 ). Here we similarly show that S288C tps2 Δ, Simi White tps2 Δ, and Bb32 tps2 Δ are unable to sporulate ( Fig.…”

“…Mutants of trehalose biosynthesis genes in S. cerevisiae have been characterized in many previous studies in multiple laboratory strains, including S288C derivatives, and diverse phenotypes have been observed ( Gancedo and Flores 2004 ). For example, tps1 mutants not only lack metabolic ability to synthesize T6P or trehalose but also exhibit several pleiotropic defects including inability to utilize fermentable carbon sources, thermosensitivity, alterations in glycogen levels, and sporulation deficiency ( Hottiger et al 1989 ; González et al 1992 ; Hohmann et al 1993 , 1996 ; Van Aelst et al 1993 ; Argüelles 1994 ; Neves et al 1995 ; Singer and Lindquist 1998a ; Enyenihi and Saunders 2003 ; Gancedo and Flores 2004 ; Shi et al 2010 ; Van Heerden et al 2014 ; Gibney et al 2015 ; Liu et al 2020 ). While several hypotheses and metabolic models have been proposed, the molecular mechanism underlying these unrelated phenotypes associated with this mutant remains elusive.…”