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Breaking spore dormancy in budding yeast transforms the cytoplasm and the solubility of the proteome.

ABSTRACT: The biophysical properties of the cytoplasm are major determinants of key cellular processes and adaptation. Many yeasts produce dormant spores that can withstand extreme conditions. We show that spores of Saccharomyces cerevisiae exhibit extraordinary biophysical properties, including a highly viscous and acidic cytosol. These conditions alter the solubility of more than 100 proteins such as metabolic enzymes that become more soluble as spores transit to active cell proliferation upon nutrient repletion. A key regulator of this transition is the heat shock protein, Hsp42, which shows transient solubilization and phosphorylation, and is essential for the transformation of the cytoplasm during germination. Germinating spores therefore return to growth through the dissolution of protein assemblies, orchestrated in part by Hsp42 activity. The modulation of spores' molecular properties are likely key adaptive features of their exceptional survival capacities.

SUBMITTER: Plante S

PROVIDER: S-EPMC10118125 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Breaking spore dormancy in budding yeast transforms the cytoplasm and the solubility of the proteome.

Plante Samuel S Moon Kyung-Mee KM Lemieux Pascale P Foster Leonard J LJ Landry Christian R CR

PLoS biology 20230420 4

The biophysical properties of the cytoplasm are major determinants of key cellular processes and adaptation. Many yeasts produce dormant spores that can withstand extreme conditions. We show that spores of Saccharomyces cerevisiae exhibit extraordinary biophysical properties, including a highly viscous and acidic cytosol. These conditions alter the solubility of more than 100 proteins such as metabolic enzymes that become more soluble as spores transit to active cell proliferation upon nutrient ...[more]

PMID: 37079504

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Project description:BackgroundSeed dormancy is controlled by the physiological or structural properties of a seed and the external conditions. It is induced as part of the genetic program of seed development and maturation. Seeds with deep physiological embryo dormancy can be stimulated to germinate by a variety of treatments including cold stratification. Hormonal imbalance between germination inhibitors (e.g. abscisic acid) and growth promoters (e.g. gibberellins) is the main cause of seed dormancy breaking. Differences in the status of hormones would affect expression of genes required for germination. Proteomics offers the opportunity to examine simultaneous changes and to classify temporal patterns of protein accumulation occurring during seed dormancy breaking and germination. Analysis of the functions of the identified proteins and the related metabolic pathways, in conjunction with the plant hormones implicated in seed dormancy breaking, would expand our knowledge about this process.ResultsA proteomic approach was used to analyse the mechanism of dormancy breaking in Norway maple seeds caused by cold stratification, and the participation of the abscisic (ABA) and gibberellic (GA) acids. Forty-four proteins showing significant changes were identified by mass spectrometry. Of these, eight spots were identified as water-responsive, 18 spots were ABA- and nine GA-responsive and nine spots were regulated by both hormones. The classification of proteins showed that most of the proteins associated with dormancy breaking in water were involved in protein destination. Most of the ABA- and GA-responsive proteins were involved in protein destination and energy metabolism.ConclusionIn this study, ABA was found to mostly down-regulate proteins whereas GA up-regulated proteins abundance. Most of the changes were observed at the end of stratification in the germinated seeds. This is the most active period of dormancy breaking when seeds pass from the quiescent state to germination. Seed dormancy breaking involves proteins of various processes but the proteasome proteins, S-adenosylmethionine synthetase, glycine-rich RNA binding protein, ABI3-interacting protein 1, EF-2 and adenosylhomocysteinase are of particular importance. The effect of exogenously applied hormones was not a determining factor for total inhibition (ABA) or stimulation (GA) of Norway maple seed dormancy breaking and germination but proteomic data has proven these hormones play a role.

Dataset Information

Breaking spore dormancy in budding yeast transforms the cytoplasm and the solubility of the proteome.

Publications

Breaking spore dormancy in budding yeast transforms the cytoplasm and the solubility of the proteome.

Similar Datasets

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