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Osmolyte accumulation regulates the SUMOylation and inclusion dynamics of the prionogenic Cyc8-Tup1 transcription corepressor.

ABSTRACT: Environmental stressors can severely perturb cellular homeostasis and compromise viability. To cope with environmental stressors, eukaryotes have developed distinct signaling programs that allow for adaptation during different stress conditions. These programs often require a host of post-translational modifications that alter proteins to elicit appropriate cellular responses. One crucial protein modifier during stress is the small ubiquitin-like modifier SUMO. In many cases, however, the functions of stress dependent protein SUMOylation remain unclear. Previously, we showed that the conserved Saccharomyces cerevisiae Cyc8-Tup1 transcriptional corepressor complex undergoes transient hyperosmotic stress-induced SUMOylation and inclusion formation, which are important for appropriate regulation of hyperosmotic-stress genes. Here, we show the osmostress-responsive MAP kinase Hog1 regulates Cyc8 SUMOylation and inclusion formation via its role in the transcriptional activation of glycerol biosynthesis genes. Mutations that ablate Cyc8 SUMOylation can partially rescue the osmosensitivity of hog1? cells, and this is facilitated by inappropriate derepression of glycerol-biosynthesis genes. Furthermore, cells specifically unable to synthesize the osmolyte glycerol cause transient Cyc8 SUMOylation and inclusions to persist, indicating a regulatory role for glycerol to reestablish the basal state of Cyc8 following adaptation to hyperosmotic stress. These observations unveil a novel intersection between phosphorylation and SUMOylation networks, which are critical for shifting gene expression and metabolic programs during stress adaptation.

SUBMITTER: Nadel CM

PROVIDER: S-EPMC6497323 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Osmolyte accumulation regulates the SUMOylation and inclusion dynamics of the prionogenic Cyc8-Tup1 transcription corepressor.

Nadel Cory M CM Mackie Timothy D TD Gardner Richard G RG

PLoS genetics 20190422 4

Environmental stressors can severely perturb cellular homeostasis and compromise viability. To cope with environmental stressors, eukaryotes have developed distinct signaling programs that allow for adaptation during different stress conditions. These programs often require a host of post-translational modifications that alter proteins to elicit appropriate cellular responses. One crucial protein modifier during stress is the small ubiquitin-like modifier SUMO. In many cases, however, the functi ...[more]

PMID: 31009461

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Project description:Saccharomyces cerevisiae normally cannot assimilate mannitol, a promising brown macroalgal carbon source for bioethanol production. To date, the molecular mechanisms underlying this inability remain unknown. Here, we found that cells acquiring mannitol-assimilating ability appeared from wild-type S. cerevisiae strain during prolonged culture in mannitol medium. Our microarray analysis revealed that genes for putative mannitol dehydrogenase and hexose transporters were up-regulated in cells acquiring mannitol-assimilating ability. Take account of our other results including complementation analysis and cell growth data, we demonstrated that this acquisition of mannitol-assimilating ability was due to the spontaneous mutation in the gene encoding Tup1 or Cyc8. Tup1-Cyc8 is the general corepressor complex involved in the repression of many kinds of genes. Thus, it is suggested that the inability of wild-type S. cerevisiae to assimilate mannitol can be attributed to the transcriptional repression of a set of genes involved in mannitol utilization by Tup1-Cyc8 corepressor. In other words, Tup1-Cyc8 is a key regulator of mannitol metabolism in S. cerevisiae. We also showed that S. cerevisiae strain which carries mutant allele of TUP1 or CYC8 produced ethanol from mannitol efficiently. Especially, strain carrying mutant allele of CYC8 showed high tolerance to salt, which is superior to other ethanologenic microorganisms. This characteristic is highly beneficial to produce bioethanol from marine biomass. Taken together, Tup1-Cyc8 can be an ideal target to develop a yeast-algal bioethanol production system. To figure out how Mtl+ strains (cells acquiring ability to grow in mannitol medium) had acquired the ability to assimilate mannitol, we performed genome-wide analysis by using Nimblegen microarrays. Yeast Saccharomyces cerevisiae cells (wild-type BY4742 strain and two Mtl+ strains, MK3619 and MK3683) were grown at 30Â°C to the logarithmic phase in SC or SM media. Total RNA was purified and the 4 RNA samples (BY4742 cells in SC as control, MK3619 cells in SM, MK3683 cells in both SC and SM) were analyzed with Nimblegen microarrays.

Dataset Information

Osmolyte accumulation regulates the SUMOylation and inclusion dynamics of the prionogenic Cyc8-Tup1 transcription corepressor.

Publications

Osmolyte accumulation regulates the SUMOylation and inclusion dynamics of the prionogenic Cyc8-Tup1 transcription corepressor.

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