Although cells respond specifically to environments, how environmental identity is encoded intracellularly is not understood. Here, we study this organization of information in budding yeast by estimating the mutual information between environmental transitions and the dynamics of nuclear translocation for 10 transcription factors. Our method of estimation is general, scalable, and based on decoding from single cells. The dynamics of the transcription factors are necessary to encode the highest amounts of extracellular information, and we show that information is transduced through two channels: Generalists (Msn2/4, Tod6 and Dot6, Maf1, and Sfp1) can encode the nature of multiple stresses, but only if stress is high; specialists (Hog1, Yap1, and Mig1/2) encode one particular stress, but do so more quickly and for a wider range of magnitudes. In particular, Dot6 encodes almost as much information as Msn2, the master regulator of the environmental stress response. Each transcription factor reports differently, and it is only their collective behavior that distinguishes between multiple environmental states. Changes in the dynamics of the localization of transcription factors thus constitute a precise, distributed internal representation of extracellular change. We predict that such multidimensional representations are common in cellular decision-making.
This work was supported by the Biotechnology and Biological Sciences Research Council (J.M.J.P., I.F., and P.S.S.), the Engineering and Physical Sciences Research Council (EPSRC) (A.A.G.), and Austrian Science Fund Grant FWF P28844 (to G.T.).
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Granados A, Pietsch J, Cepeda Humerez SA, Farquhar I, Tkačik G, Swain P. Distributed and dynamic intracellular organization of extracellular information. PNAS. 2018;115(23):6088-6093. doi:10.1073/pnas.1716659115
Granados, A., Pietsch, J., Cepeda Humerez, S. A., Farquhar, I., Tkačik, G., & Swain, P. (2018). Distributed and dynamic intracellular organization of extracellular information. PNAS. National Academy of Sciences. https://doi.org/10.1073/pnas.1716659115
Granados, Alejandro, Julian Pietsch, Sarah A Cepeda Humerez, Isebail Farquhar, Gašper Tkačik, and Peter Swain. “Distributed and Dynamic Intracellular Organization of Extracellular Information.” PNAS. National Academy of Sciences, 2018. https://doi.org/10.1073/pnas.1716659115.
A. Granados, J. Pietsch, S. A. Cepeda Humerez, I. Farquhar, G. Tkačik, and P. Swain, “Distributed and dynamic intracellular organization of extracellular information,” PNAS, vol. 115, no. 23. National Academy of Sciences, pp. 6088–6093, 2018.
Granados A, Pietsch J, Cepeda Humerez SA, Farquhar I, Tkačik G, Swain P. 2018. Distributed and dynamic intracellular organization of extracellular information. PNAS. 115(23), 6088–6093.
Granados, Alejandro, et al. “Distributed and Dynamic Intracellular Organization of Extracellular Information.” PNAS, vol. 115, no. 23, National Academy of Sciences, 2018, pp. 6088–93, doi:10.1073/pnas.1716659115.
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