Spatiotemporal control of pathway sensors and cross-pathway feedback regulate a differentiation MAPK pathway in yeast

Abstract

Mitogen-Activated Protein Kinase (MAPK) pathways control cell differentiation and the response to stress. In Saccharomyces cerevisiae, the MAPK pathway that controls filamentous growth (fMAPK) shares components with the pathway that regulates the response to osmotic stress (HOG). Here, we show that the two pathways exhibit different patterns of activity throughout the cell cycle. The different patterns resulted from different expression profiles of genes encoding mucin sensors that regulate the pathways. Cross-pathway regulation from the fMAPK pathway stimulated the HOG pathway, presumably to modulate fMAPK pathway activity. We also show that the shared tetraspan protein, Sho1p, which has a dynamic localization pattern, induced the fMAPK pathway at the mother-bud neck. A Sho1p-interacting protein, Hof1p, which also localizes to the mother-bud neck and regulates cytokinesis, also regulated the fMAPK pathway. Therefore, spatial and temporal regulation of pathway sensors, and cross-pathway regulation, control a MAPK pathway that regulates cell differentiation in yeast.

MAPK CcSakA of the HOG Pathway Is Involved in Stipe Elongation during Fruiting Body Development in Coprinopsis cinerea

“…However, how Basidiomycetes sense different environmental stresses during fruiting body development is still unclear [ 49 ]. In yeasts and filamentous fungi, MAPK cascades are important signaling pathways to respond to environmental stresses and regulate processes, such as the cell cycle, reproduction, cell differentiation, morphogenesis, and stress response [ 25 , 28 , 30 , 51 , 52 , 53 , 54 ]. The signal induced by environmental stresses is transmitted by the sequential phosphorylation of a basic array of three proteins, often termed MAPKKK, MAPKK, and MAPK, [ 54 , 55 ].…”

“…In fungi, the HOG pathway is involved not only in the response to osmotic pressure but also in the response to UV, light, heavy metal, heat, citric acid, and oxidative stresses [ 25 , 28 , 58 , 62 , 63 , 64 ]. Since the stipe would not continue to elongate normally after being dissected from the fruiting body of C. cinerea and because of the presence of a hydrophobic material layer outside the stipe, it was not possible to treat the stipe with solutions containing different stresses [ 7 , 59 ].…”

“…Some studies show that photoreceptors for blue light, such as Dst1, Dst2, and WC-2, may sense light signals in the environment and are involved in fruiting body photomorphogenesis of C. cinerea , but their downstream regulatory genes are not yet known [ 4 , 9 , 24 ]. MAPK pathways are evolutionarily conserved signaling modules in eukaryotic organisms [ 25 ]. In fungi such as Saccharomyces cerevisiae and Aspergillus fumigatus , the MAPK pathways respond to a variety of environmental signals, such as cell wall stress, light, nitrogen, and carbon deprivation and high osmolarity, and regulate the expression of genes associated with cell differentiation and development [ 25 , 26 , 27 , 28 , 29 , 30 ].…”

“…MAPK pathways are evolutionarily conserved signaling modules in eukaryotic organisms [ 25 ]. In fungi such as Saccharomyces cerevisiae and Aspergillus fumigatus , the MAPK pathways respond to a variety of environmental signals, such as cell wall stress, light, nitrogen, and carbon deprivation and high osmolarity, and regulate the expression of genes associated with cell differentiation and development [ 25 , 26 , 27 , 28 , 29 , 30 ].…”

Exploring the Regulation of Cdc42 Stability and Turnover in Yeast

“…Three Cdc42p-dependent MAPK pathways regulate different cellular responses, including filamentous growth (fMAPK) (Cullen and Sprague, 2012), mating (Good et al, 2009; Sprague et al, 1983), and the response to osmotic stress (HOG) (Saito and Posas, 2012). Understanding how Cdc42 and other common proteins function in a pathway-specific response has been intensively explored (Bao et al, 2004; Basu et al, 2020; Boulter et al, 2010; Patterson et al, 2021; Prabhakar et al, 2021; Saito, 2010; Van Drogen et al, 2020; Vázquez-Ibarra et al, 2020). Cdc42p also regulates exocytosis (Adamo et al, 2001), endocytosis (Aguilar et al, 2006), vacuolar functions (Jones et al, 2010), and nuclear membrane disassembly and migration (Lu and Drubin, 2020).…”