Pleiotropic signaling pathways orchestrate yeast development
Highlights
► Nutrient stress induces developmental switches in Saccharomyces cerevisiae (baker’s yeast) and related fungi. ► The signaling pathways that control development are highly pleoiotropic. ► Because of signaling pathway pleiotropy, developmental phenotypes can be strongly correlated. ► Pleiotropy can be exploited in functional studies to discover or understand interactions within and between signaling pathways. ► Understanding the causes and consequences of pleiotropy is important in ecological, clinical, and agricultural contexts.
Introduction
In response to stress, the baker’s yeast Saccharomyces cerevisiae and related fungi undergo a variety of developmental switches. These developmental switches include transitions to filamentous growth [1], changes in interactions between cells that lead to biofilms [2••], and architecturally complex colonies 3, 4, or the induction of meiosis and sporulation [5]. These responses are induced by signals that act through a variety of signaling pathways, all of which regulate multiple developmental phenotypes. In this review, we emphasize the pleiotropic nature of developmental pathways in yeast. We consider the implications of pleiotropy for understanding functional relationships among developmental responses and discuss the ecological, industrial, and clinical implications of developmental pleiotropy.
Section snippets
Filamentous growth
Filamentous growth refers to both diploid pseudohyphal growth and haploid invasive growth, both of which are induced by nutrient limitation. Pseudohyphal growth is primarily induced by nitrogen starvation [6], although several reports demonstrate a secondary role for carbon type and quality in its regulation (Figure 1b) 7, 8, 9. The pseudohyphal response is characterized by a switch from bipolar to unipolar budding, incomplete mother-daughter cell separation, and cell elongation. These
Developmental pathways
Genetic and biochemical studies have identified five major signaling pathways [21] that are involved in nutrient-induced developmental responses in yeast: (1) the cAMP-PKA pathway; (2) the TOR pathway; (3) the SNF1/AMPK pathway; (4) the Rim101 pathway; and (5) the Kss1-MAPK pathway. As we discuss below, all these pathways have known or predicted pleiotropic effects on at least two (and in some cases all three) developmental phenotypes.
Combinatorial patterns of pathway activity regulate yeast development
If almost every one of the key signaling pathways regulates multiple developmental phenotypes, often in the same direction, how then do yeast mount appropriate responses in the face of particular nutrient challenges? The answer almost surely lies in combinatorial pathway interactions. The joint effects of multiple signaling pathways and their relative activities are key features of the cellular decision making that leads to different developmental fates in yeast [58]. Recent studies have used
Summary
Yeast, like most microbes, make developmental decisions in response to nutrient cues. Most investigations aimed at understanding the mechanisms that regulate developmental switches in S. cerevisiae have focused on single developmental outcomes, without considering the potential for parallel responses in other phenotypes. As we have outlined above, the gene networks that regulate development in yeast are highly pleiotropic, and thus correlated changes in developmental responses are likely to be
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We thank Jennifer Reininga and Debra Murray for helpful comments on this manuscript. This work was supported in part by the NIH (P50GM081883-01) and NSF (MCB-0614959).
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