Epigenetics Decouples Mutational from Environmental Robustness. Did It Also Facilitate Multicellularity?

Saurabh Gombar, Thomas MacCarthy, Aviv Bergman

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

The evolution of ever increasing complex life forms has required innovations at the molecular level in order to overcome existing barriers. For example, evolving processes for cell differentiation, such as epigenetic mechanisms, facilitated the transition to multicellularity. At the same time, studies using gene regulatory network models, and corroborated in single-celled model organisms, have shown that mutational robustness and environmental robustness are correlated. Such correlation may constitute a barrier to the evolution of multicellularity since cell differentiation requires sensitivity to cues in the internal environment during development. To investigate how this barrier might be overcome, we used a gene regulatory network model which includes epigenetic control based on the mechanism of histone modification via Polycomb Group Proteins, which evolved in tandem with the transition to multicellularity. Incorporating the Polycomb mechanism allowed decoupling of mutational and environmental robustness, thus allowing the system to be simultaneously robust to mutations while increasing sensitivity to the environment. In turn, this decoupling facilitated cell differentiation which we tested by evaluating the capacity of the system for producing novel output states in response to altered initial conditions. In the absence of the Polycomb mechanism, the system was frequently incapable of adding new states, whereas with the Polycomb mechanism successful addition of new states was nearly certain. The Polycomb mechanism, which dynamically reshapes the network structure during development as a function of expression dynamics, decouples mutational and environmental robustness, thus providing a necessary step in the evolution of multicellularity.

Original languageEnglish (US)
Article numbere1003450
JournalPLoS Computational Biology
Volume10
Issue number3
DOIs
StatePublished - 2014

Fingerprint

Epigenomics
epigenetics
cell differentiation
Cell Differentiation
Genes
Gene Regulatory Networks
Robustness
Time and motion study
Histone Code
Polycomb-Group Proteins
Time and Motion Studies
gene
Innovation
Gene Regulatory Network
Proteins
Decoupling
histones
Network Model
Cues
mutation

ASJC Scopus subject areas

  • Computational Theory and Mathematics
  • Modeling and Simulation
  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Molecular Biology
  • Ecology
  • Cellular and Molecular Neuroscience

Cite this

Epigenetics Decouples Mutational from Environmental Robustness. Did It Also Facilitate Multicellularity? / Gombar, Saurabh; MacCarthy, Thomas; Bergman, Aviv.

In: PLoS Computational Biology, Vol. 10, No. 3, e1003450, 2014.

Research output: Contribution to journalArticle

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