Cyc8p and Tup1p transcription regulators antagonistically regulate Flo11p expression and complexity of yeast colony biofilms

Nguyen, Peter H.; Hlaváček, Otakar; Maršíková, Jana; Váchová, Libuše; Palková, Zdena

doi:10.1371/journal.pgen.1007495

Cited by 22 publications

(28 citation statements)

References 79 publications

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“…The Cyc8p (Ssn6)‐Tup1p co‐repressor complex negatively regulates the expression of all the FLO genes but the regulation of FLO11 gene expression by this complex is different. Cyc8p acts as the repressor of FLO11 gene expression whereas Tup1p antagonize the repressive activity of Cyc8p (Nguyen et al , ). Furthermore, we also found constitutive recruitment of Pol II and TBP, and reduced occupancy of Tup1 at the promoters of FLO genes in flocculating (Fig.…”

Section: Discussionmentioning

confidence: 99%

Flocculation of Saccharomyces cerevisiae is dependent on activation of Slt2 and Rlm1 regulated by the cell wall integrity pathway

Sariki

Kumawat

Singh

et al. 2019

Molecular Microbiology

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Summary Flocculation is an essential characteristic of yeast cells required for survival under adverse conditions. The multicellular structure (flocs) of yeast provides a suitable microenvironment to enhance the chances of survival during stress conditions. Although the signaling events triggering flocculation have been studied earlier, molecular mechanisms remain elusive. In the present study, we used flocculating sen1 mutants to identify the mechanism of flocculation. Based on the abnormal cell surface morphology and constitutive phosphorylation of Slt2p in flocculating sen1 mutant cells, we hypothesized if flocculation was regulated by the cell wall integrity (CWI) pathway. Up‐regulation of FLO genes in wild‐type cells was observed upon the activation of CWI pathway either by chemical treatment or by deleting Slt2 phosphatase (Msg5). Our study with Slt2 mutants reveals that the active state of Slt2 is indispensable for flocculation. Deletion of either SLT2 or RLM1 leads to reduced flocculation. Furthermore, we observed overlapping binding sites for Rlm1 and Tup1 at the promoters of almost all the FLO genes. Finally, we show higher Rlm1 and lower Tup1 occupancy at the promoters of FLO1 and FLO5 in flocculating cells. Altogether we demonstrate that CWI MAPK (Slt2) pathway uses a non‐catalytic mechanism to activate the transcription of FLO genes.

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Section: Discussionmentioning

confidence: 99%

Flocculation of Saccharomyces cerevisiae is dependent on activation of Slt2 and Rlm1 regulated by the cell wall integrity pathway

Sariki

Kumawat

Singh

et al. 2019

Molecular Microbiology

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“…Cyc8p represses the FLO11 gene, preventing the formation of colony biofilms, whereas Tup1p antagonizes Cyc8pmediated FLO11 repression and, in addition, stabilizes the Flo11p protein by preventing its degradation. 22 Here we show that Cyc8p negatively and Tup1p positively control adhesion of S. cerevisiae strains to plastic surfaces and subsequent formation of structured solid-liquid interface biofilm. The regulators influence adhesion of both shaken planktonic and static (sedimented) cells at any growth phase.…”

Section: Introductionmentioning

confidence: 64%

“…In glucose absence, Cyc8p level is decreased and its function is inhibited via Tup1p "3" as described. 22 Subsequently Flo11p is produced and contributes to cell adhesion. Arrow, induction; blunt line, repression.…”

Section: Discussionmentioning

confidence: 99%

“…Cyc8p and Tup1p conversely regulate cell adhesion Next, we asked whether Cyc8p and Tup1p, which regulate formation of structured colony biofilms 22 are also involved in BRF cell adhesion to plastic. We therefore assayed the adhesion capability of BRF-derived strains with modified levels of Cyc8p and Tup1p (Table 1).…”

Section: Adhesion To Plastic Varies In Different S Cerevisiae Strainsmentioning

confidence: 99%

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Glucose, Cyc8p and Tup1p regulate biofilm formation and dispersal in wild Saccharomyces cerevisiae

Nguyen

Plocek

Váchová

et al. 2020

npj Biofilms Microbiomes

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Saccharomyces cerevisiae is a mainly beneficial yeast, widely used in the food industry. However, there is growing evidence of its potential pathogenicity, leading to fungemia and invasive infections. The medical impact of yeast pathogens depends on formation of biofilms: multicellular structures, protected from the environment. Cell adhesion is a prerequisite of biofilm formation. We investigated the adherence of wild and genetically modified S. cerevisiae strains, formation of solid-liquid interface biofilms and associated regulation. Planktonic and static cells of wild strain BRF adhered and formed biofilms in glucose-free medium. Tup1p and Cyc8p were key positive and negative regulators, respectively. Glucose caused increased Cyc8p levels and blocked cell adhesion. Even low glucose levels, comparable with levels in the blood, allowed biofilm dispersal and release of planktonic cells. Cyc8p could thus modulate cell adhesion in different niches, dependently on environmental glucose level, e.g., high-glucose blood versus low-glucose tissues in host organisms.

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“…Notably, the similar profiles of DAPs shared between mutants cyc8 Ϫ/Ϫ and tup1 Ϫ/Ϫ , for instance, showing upregulated glycolysis and gluconeogenesis proteins and downregulated amino acid biosynthesis proteins, suggest opposite and collaborative roles according to the environmental conditions. Indeed, it has been reported previously that the Cyc8-Tup1 complex showed antagonistic and activator effects (26)(27)(28), but it is necessary to elucidate this behavior and its effect on carotenogenesis.…”

Section: Discussionmentioning

confidence: 99%

Convergence between Regulation of Carbon Utilization and Catabolic Repression in Xanthophyllomyces dendrorhous

Martínez-Moya

Campusano

Córdova

et al. 2020

mSphere

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Xanthophyllomyces dendrorhous is a carotenogenic yeast with a singular metabolic capacity to produce astaxanthin, a valuable antioxidant pigment. This yeast can assimilate several carbon sources and sustain fermentation even under aerobic conditions. Since astaxanthin biosynthesis is affected by the carbon source, the study of carotenogenesis regulatory mechanisms is key for improving astaxanthin yield in X. dendrorhous. This study aimed to elucidate the regulation of the metabolism of different carbon sources and the phenomenon of catabolic repression in this yeast. To this end, protein and transcript levels were quantified by iTRAQ (isobaric tags for relative and absolute quantification) and transcriptomic sequencing (RNA-seq) in the wild-type strain under conditions of glucose, maltose, or succinate treatment and in the mutant strains for genes MIG1, CYC8, and TUP1 under conditions of glucose treatment. Alternative carbon sources such as maltose and succinate affected the relative abundances of 14% of the wild-type proteins, which were mainly grouped into the carbohydrate metabolism category, with the glycolysis/gluconeogenesis and citrate cycle pathways being the most highly represented pathways. Each mutant strain showed significant proteomic profile changes, affecting approximately 2% of the total proteins identified, compared to the wild-type strain under glucose treatment conditions. Similarly to the results seen with the alternative carbon sources, the changes in the mutant strains mainly affected carbohydrate metabolism, with glycolysis/gluconeogenesis and the pentose phosphate and citrate cycle pathways being the most highly represented pathways. Our results showed convergence between carbon assimilation and catabolic repression in the strains studied. Interestingly, indications of cooperative, opposing, and overlapping processes during catabolic regulation were found. We also identified target proteins of the regulatory processes, reinforcing the likelihood of catabolic repression at the posttranscriptional level. IMPORTANCE The conditions affecting catabolic regulation in X. dendrorhous are complex and suggest the presence of an alternative mechanism of regulation. The repressors Mig1, Cyc8, and Tup1 are essential elements for the regulation of the use of glucose and other carbon sources. All play different roles but, depending on the growth conditions, can work in convergent, synergistic, and complementary ways to use carbon sources and to regulate other targets for yeast metabolism. Our results reinforced the belief that further studies in X. dendrorhous are needed to clarify a specific regulatory mechanism at the domain level of the repressors as well as its relationship with those of other metabolic repressors, i.e., the stress response, to elucidate carotenogenic regulation at the transcriptomic and proteomic levels in this yeast.

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Cyc8p and Tup1p transcription regulators antagonistically regulate Flo11p expression and complexity of yeast colony biofilms

Cited by 22 publications

References 79 publications

Flocculation of Saccharomyces cerevisiae is dependent on activation of Slt2 and Rlm1 regulated by the cell wall integrity pathway

Flocculation of Saccharomyces cerevisiae is dependent on activation of Slt2 and Rlm1 regulated by the cell wall integrity pathway

Glucose, Cyc8p and Tup1p regulate biofilm formation and dispersal in wild Saccharomyces cerevisiae

Convergence between Regulation of Carbon Utilization and Catabolic Repression in Xanthophyllomyces dendrorhous

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