Academic journal article Genetics

Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast

Academic journal article Genetics

Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast

Article excerpt

FUNGAL microorganisms exhibit a range of nutrient-related responses. Under certain conditions, fungal cells can differentiate into filamentous or hyphal cells that can expand across, and/or penetrate into, new environments (Soll and Daniels 2016). Many fungal species can also grow in communities of biofilms or mats, which are composed of interconnected cells that attach to each other and to surfaces. One property of mats is the formation of highly organized patterns that result from adhesive contacts between cells. In pathogens, filamentous growth (Lo et al. 1997) and biofilm formation (Desai et al. 2014) are critical determinants of virulence. For example, cells can adhere to medical devices and grow in dense mats that are resistant to antifungal medicines (Chandra et al. 2001; Sudbery et al. 2004; Kumamoto 2005; Ramage et al. 2005; Nett and Andes 2015).

The budding yeast Saccharomyces cerevisiae is a unicellular fungal microbe, and a convenient model for studying nutrientregulated foraging responses like filamentous growth and mat formation. These responses are best studied in "wild" strain backgrounds (such as S1278b) as the responses have been lost in certain laboratory strains due to genetic manipulation (Liu et al. 1996; Dowell et al. 2010; Chin et al. 2012). During filamentous growth, yeast cells differentiate into elongated and polarized filaments that remain connected in pseudohyphae (Gimeno et al. 1992; Cullen and Sprague 2012).

At least 600 genes have been identified by genetic screens (Lorenz and Heitman 1998; Palecek etal. 2000) and genome-wide studies (Jin et al. 2008; Xu et al. 2010; Ryan et al. 2012) that play some role in filamentous growth. A subset of these genes encode signaling pathway components that include at least four major nutrient-sensing pathways [filamentous growth MAPK (fMAPK), RAS, TOR (target of rapamycin), and SNF1], as well as pathways that regulate the response to pH (RIM101), phosphate utilization (PHO85), and mitochondrial stress [the retrograde mitochondriato-nucleus (RTG) pathway]. In addition, proteins that control the epigenetic modification of histones to alter gene expression have also been implicated in the regulation of filamentous growth (Rpd3p).

Many of the pathways that regulate filamentous growth are functionally connected through their ability to coregulate common target genes (Figure 1A). In some cases, this occurs at the level of transcription. In a pioneering study, it was shown that many of the transcription factors that control filamentous growth control each other's expression (Borneman et al. 2006). Transcription factors can also converge at common promoter elements. One example is the gene encoding the major cell adhesion molecule in yeast, Flo11p (Kraushaar et al. 2015; Chan et al 2016). The FLO11 gene contains one of the largest and most highly regulated promoters in the yeast genome, and functions as a hub where multiple transcription factors and chromatin remodeling enzymes bind (Robertson and Fink 1998; Rupp et al. 1999; Palecek et al. 2000; Pan and Heitman 2000; Kuchin et al. 2002; van Dyk et al. 2005; Barrales et al. 2008). Signaling pathways that control filamentous growth can also regulate each other's activity. The classic example comes from the discovery that the RAS pathway can regulate the activity of the fMAPK pathway (Mösch et al. 1996). It is now clear that many pathways regulate the activity of the fMAPK pathway (Chavel etal. 2010, 2014). One way this may occur is through the protein kinases of the major regulatory pathways, which can regulate each other's localization and activity (Bharucha et al. 2008).

Yeast can also undergo mat formation (Reynolds and Fink 2001; Bojsen et al. 2012), where colonies expand radially across surfaces and form ruffled patterns (Granek and Magwene 2010; Granek et al. 2011; Tam et al. 2018). Mats form wheel-spoke patterns in low-percentage agar media [0.3% agar (Reynolds and Fink 2001)], and wrinkled or ruffled colonies on high-percentage agar media [1-4% (Granek and Magwene 2010; Karunanithi et al. …

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