Divergent Roles for cAMP–PKA Signaling in the Regulation of Filamentous Growth in <i>Saccharomyces cerevisiae</i> and <i>Saccharomyces bayanus</i>

Kayıkçı, Ömür; Magwene, Paul M.

doi:10.1534/g3.118.200413

Cited by 18 publications

(6 citation statements)

References 74 publications

(77 reference statements)

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“…The catalytic subunits of PKA in S. cerevisiae are encoded by TPK1 , TPK2 and TPK3 , but there are two isoforms TPK1 and TPK2 encoded by TPK1 and TPK2 as the catalytic subunits of PKA in C . albicans [44, 45]. In T. cutaneum B3, c9021_g1 , c9875_g1 and c10736_g1 are homologous to GPR1 , RAS2 and TPK3 , which were overexpressed in the yeast-form cells at 1.14-, 1.58- and 1.63-folds to regulate the cAMP-PKA signaling pathway and consequently to repress the development of hyphae.…”

Section: Resultsmentioning

confidence: 99%

Dimorphism of Trichosporon cutaneum and impact on its lipid production

Ren

Tang

et al. 2019

Biotechnol Biofuels

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Background Compared to the oleaginous yeast Yarrowia lipolytica , Trichosporon cutaneum can metabolize pentose sugars more efficiently, and in the meantime is more tolerant to inhibitors, which is suitable for lipid production from lignocellulosic biomass. However, this species experiences dimorphic transition between yeast-form cells and hyphae during submerged fermentation, which consequently affects the rheology and mass transfer performance of the fermentation broth and its lipid production. Results The strain T. cutaneum B3 was cultured with medium composed of yeast extract, glucose and basic minerals. The experimental results indicated that yeast-form morphology was developed when yeast extract was supplemented at 1 g/L, but hyphae were observed when yeast extract supplementation was increased to 3 g/L and 5 g/L, respectively. We speculated that difference in nitrogen supply to the medium might be a major reason for the dimorphic transition, which was confirmed by the culture with media supplemented with yeast extract at 1 g/L and urea at 0.5 g/L and 1.0 g/L to maintain total nitrogen at same levels as that detected in the media with yeast extract supplemented at 3 g/L and 5 g/L. The morphological change of T. cutaneum B3 affected not only the content of intracellular lipids but also their composition, due to its impact on the rheology and oxygen mass transfer performance of the fermentation broth, and more lipids with less polyunsaturated fatty acids such as linoleic acid (C18:2) were produced by the yeast-form cells. When T. cutaneum B3 was cultured at an aeration rate of 1.5 vvm for 72 h with the medium composed of 60 g/L glucose, 3 g/L yeast extract and basic minerals, 27.1 g (dry cell weight)/L biomass was accumulated with the lipid content of 46.2%, and lipid productivity and yield were calculated to be 0.174 g/L/h and 0.21 g/g, respectively. Comparative transcriptomics analysis identified differently expressed genes for sugar metabolism and lipid synthesis as well as signal transduction for the dimorphic transition of T. cutaneum B3. Conclusions Assimilable nitrogen was validated as one of the major reasons for the dimorphic transition between yeast-form morphology and hyphae with T. cutaneum , and the yeast-form morphology was more suitable for lipid production at high content with less polyunsaturated fatty acids as feedstock for biodiesel production. Electronic supplementary material The online version of this article (10.1186/s13068-019-1543-3) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Dimorphism of Trichosporon cutaneum and impact on its lipid production

Ren

Tang

et al. 2019

Biotechnol Biofuels

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“…The model yeast, S. cerevisiae , exhibits multiple social phenotypes in the lab, including filamentous growth and quorum sensing. The filamentous growth phenotype appears to be conserved among other Saccharomyces spp (Kayikci and Magwene 2018) and among medically relevant yeasts, including Candida albicans (Cutler 1991), other Candida spp (Silva et al 2011), Asperigillus fumigatus (Mowat et al 2009) and Trichosporon asahii (Di Bonaventura et al 2006), with filamentation ranging from pseudohyphae to true hyphae. Thus, filamentous growth is likely an important fungal response to environmental cues.…”

Section: Discussionmentioning

confidence: 99%

Variation in Filamentous Growth and Response to Quorum-Sensing Compounds in Environmental Isolates ofSaccharomyces cerevisiae

Lenhart

Meeks

Murphy³

2019

G3 Genes|Genomes|Genetics

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In fungi, filamentous growth is a major developmental transition that occurs in response to environmental cues. In diploid Saccharomyces cerevisiae , it is known as pseudohyphal growth and presumed to be a foraging mechanism. Rather than unicellular growth, multicellular filaments composed of elongated, attached cells spread over and into surfaces. This morphogenetic switch can be induced through quorum sensing with the aromatic alcohols phenylethanol and tryptophol. Most research investigating pseudohyphal growth has been conducted in a single lab background, Σ1278b. To investigate the natural variation in this phenotype and its induction, we assayed the diverse 100-genomes collection of environmental isolates. Using computational image analysis, we quantified the production of pseudohyphae and observed a large amount of variation. Population origin was significantly associated with pseudohyphal growth, with the West African population having the most. Surprisingly, most strains showed little or no response to exogenous phenylethanol or tryptophol. We also investigated the amount of natural genetic variation in pseudohyphal growth using a mapping population derived from a highly-heterozygous clinical isolate that contained as much phenotypic variation as the environmental panel. A bulk-segregant analysis uncovered five major peaks with candidate loci that have been implicated in the Σ1278b background. Our results indicate that the filamentous growth response is a generalized, highly variable phenotype in natural populations, while response to quorum sensing molecules is surprisingly rare. These findings highlight the importance of coupling studies in tractable lab strains with natural isolates in order to understand the relevance and distribution of well-studied traits.

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“…Mechanistically, the Tpk2-dependent regulation of filamentous growth is thought to involve the phosphorylation and targeting of two transcription factors, Sfl1 and Flo8. These factors act antagonistically in the transcriptional regulation of a key cell wall, flocculin Flo11, and FLO11 transcription represents a critical determinant of filamentous growth [ 46 , 62 , 63 ]. More specifically, Tpk2 inhibits the Sfl1 repressor, while acting as a positive regulator of Flo8 [ 61 ].…”

Section: Unravelling Tpk Isoform Specificitymentioning

confidence: 99%

Yeast Protein Kinase A Isoforms: A Means of Encoding Specificity in the Response to Diverse Stress Conditions?

et al. 2022

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Eukaryotic cells have developed a complex circuitry of signalling molecules which monitor changes in their intra- and extracellular environments. One of the most widely studied signalling pathways is the highly conserved cyclic AMP (cAMP)/protein kinase A (PKA) pathway, which is a major glucose sensing circuit in the yeast Saccharomyces cerevisiae. PKA activity regulates diverse targets in yeast, positively activating the processes that are associated with rapid cell growth (e.g., fermentative metabolism, ribosome biogenesis and cell division) and negatively regulating the processes that are associated with slow growth, such as respiratory growth, carbohydrate storage and entry into stationary phase. As in higher eukaryotes, yeast has evolved complexity at the level of the PKA catalytic subunit, and Saccharomyces cerevisiae expresses three isoforms, denoted Tpk1-3. Despite evidence for isoform differences in multiple biological processes, the molecular basis of PKA signalling specificity remains poorly defined, and many studies continue to assume redundancy with regards to PKA-mediated regulation. PKA has canonically been shown to play a key role in fine-tuning the cellular response to diverse stressors; however, recent studies have now begun to interrogate the requirement for individual PKA catalytic isoforms in coordinating distinct steps in stress response pathways. In this review, we discuss the known non-redundant functions of the Tpk catalytic subunits and the evolving picture of how these isoforms establish specificity in the response to different stress conditions.

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Divergent Roles for cAMP–PKA Signaling in the Regulation of Filamentous Growth in Saccharomyces cerevisiae and Saccharomyces bayanus

Cited by 18 publications

References 74 publications

Dimorphism of Trichosporon cutaneum and impact on its lipid production

Dimorphism of Trichosporon cutaneum and impact on its lipid production

Variation in Filamentous Growth and Response to Quorum-Sensing Compounds in Environmental Isolates ofSaccharomyces cerevisiae

Yeast Protein Kinase A Isoforms: A Means of Encoding Specificity in the Response to Diverse Stress Conditions?

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