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Control of yeast filamentous-form growth by modules in an integrated molecular network.

ABSTRACT: On solid growth media with limiting nitrogen source, diploid budding-yeast cells differentiate from the yeast form to a filamentous, adhesive, and invasive form. Genomic profiles of mRNA levels in Saccharomyces cerevisiae yeast-form and filamentous-form cells were compared. Disparate data types, including genes implicated by expression change, filamentation genes known previously through a phenotype, protein-protein interaction data, and protein-metabolite interaction data were integrated as the nodes and edges of a filamentation-network graph. Application of a network-clustering method revealed 47 clusters in the data. The correspondence of the clusters to modules is supported by significant coordinated expression change among cluster co-member genes, and the quantitative identification of collective functions controlling cell properties. The modular abstraction of the filamentation network enables the association of filamentous-form cell properties with the activation or repression of specific biological processes, and suggests hypotheses. A module-derived hypothesis was tested. It was found that the 26S proteasome regulates filamentous-form growth.

SUBMITTER: Prinz S

PROVIDER: S-EPMC353223 | biostudies-literature | 2004 Mar

REPOSITORIES: biostudies-literature

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Control of yeast filamentous-form growth by modules in an integrated molecular network.

Prinz Susanne S Avila-Campillo Iliana I Aldridge Christine C Srinivasan Ajitha A Dimitrov Krassen K Siegel Andrew F AF Galitski Timothy T

Genome research 20040301 3

On solid growth media with limiting nitrogen source, diploid budding-yeast cells differentiate from the yeast form to a filamentous, adhesive, and invasive form. Genomic profiles of mRNA levels in Saccharomyces cerevisiae yeast-form and filamentous-form cells were compared. Disparate data types, including genes implicated by expression change, filamentation genes known previously through a phenotype, protein-protein interaction data, and protein-metabolite interaction data were integrated as the ...[more]

PMID: 14993204

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Project description:Many fungal species, including pathogens, undergo a morphogenetic response called filamentous growth, where cells differentiate into a specialized cell type to promote nutrient foraging and surface colonization. Despite the fact that filamentous growth is required for virulence in some plant and animal pathogens, certain aspects of this behavior remain poorly understood. By examining filamentous growth in the budding yeast Saccharomyces cerevisiae and the opportunistic pathogen Candida albicans, we identify responses where cells undergo filamentous growth in groups of cells or aggregates. In S. cerevisiae, aggregate invasive growth was regulated by signaling pathways that control normal filamentous growth. These pathways promoted aggregation in part by fostering aspects of microbial cooperation. For example, aggregate invasive growth required cellular contacts mediated by the flocculin Flo11p, which was produced at higher levels in aggregates than cells undergoing regular invasive growth. Aggregate invasive growth was also stimulated by secreted enzymes, like invertase, which produce metabolites that are shared among cells. Aggregate invasive growth was also induced by alcohols that promote density-dependent filamentous growth in yeast. Aggregate invasive growth also required highly polarized cell morphologies, which may affect the packing or organization of cells. A directed selection experiment for aggregating phenotypes uncovered roles for the fMAPK and RAS pathways, which indicates that these pathways play a general role in regulating aggregate-based responses in yeast. Our study extends the range of responses controlled by filamentation regulatory pathways and has implications in understanding aspects of fungal biology that may be relevant to fungal pathogenesis.IMPORTANCE Filamentous growth is a fungal morphogenetic response that is critical for virulence in some fungal species. Many aspects of filamentous growth remain poorly understood. We have identified an aspect of filamentous growth in the budding yeast Saccharomyces cerevisiae and the human pathogen Candida albicans where cells behave collectively to invade surfaces in aggregates. These responses may reflect an extension of normal filamentous growth, as they share the same signaling pathways and effector processes. Aggregate responses may involve cooperation among individual cells, because aggregation was stimulated by cell adhesion molecules, secreted enzymes, and diffusible molecules that promote quorum sensing. Our study may provide insights into the genetic basis of collective cellular responses in fungi. The study may have ramifications in fungal pathogenesis, in situations where collective responses occur to promote virulence.

Project description:Tardigrades are able to tolerate almost complete dehydration by entering a reversible ametabolic state called anhydrobiosis and resume their animation upon rehydration. Dehydrated tardigrades are exceptionally stable and withstand various physical extremes. Although trehalose and late embryogenesis abundant (LEA) proteins have been extensively studied as potent protectants against dehydration in other anhydrobiotic organisms, tardigrades produce high amounts of tardigrade-unique protective proteins. Cytoplasmic-abundant heat-soluble (CAHS) proteins are uniquely invented in the lineage of eutardigrades, a major class of the phylum Tardigrada and are essential for their anhydrobiotic survival. However, the precise mechanisms of their action in this protective role are not fully understood. In the present study, we first postulated the presence of tolerance proteins that form protective condensates via phase separation in a stress-dependent manner and searched for tardigrade proteins that reversibly form condensates upon dehydration-like stress. Through a comprehensive search using a desolvating agent, trifluoroethanol (TFE), we identified 336 proteins, collectively dubbed "TFE-Dependent ReversiblY condensing Proteins (T-DRYPs)." Unexpectedly, we rediscovered CAHS proteins as highly enriched in T-DRYPs, 3 of which were major components of T-DRYPs. We revealed that these CAHS proteins reversibly polymerize into many cytoskeleton-like filaments depending on hyperosmotic stress in cultured cells and undergo reversible gel-transition in vitro. Furthermore, CAHS proteins increased cell stiffness in a hyperosmotic stress-dependent manner and counteract the cell shrinkage caused by osmotic pressure, and even improved the survival against hyperosmotic stress. The conserved putative helical C-terminal region is necessary and sufficient for filament formation by CAHS proteins, and mutations disrupting the secondary structure of this region impaired both the filament formation and the gel transition. On the basis of these results, we propose that CAHS proteins are novel cytoskeleton-like proteins that form filamentous networks and undergo gel-transition in a stress-dependent manner to provide on-demand physical stabilization of cell integrity against deformative forces during dehydration and could contribute to the exceptional physical stability in a dehydrated state.

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Control of yeast filamentous-form growth by modules in an integrated molecular network.

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Control of yeast filamentous-form growth by modules in an integrated molecular network.

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