Evolutionary principles of modular gene regulation in yeasts
Dawn A Thompson,
Sushmita Roy,
Michelle Chan,
Mark P Styczynsky,
Jenna Pfiffner,
Courtney French,
Amanda Socha,
Anne Thielke,
Sara Napolitano,
Paul Muller,
Manolis Kellis,
Jay H Konieczka,
Ilan Wapinski,
Aviv Regev
Affiliations
Dawn A Thompson
Broad Institute of MIT and Harvard, Cambridge, United States
Sushmita Roy
Broad Institute of MIT and Harvard, Cambridge, United States; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, United States
Michelle Chan
Broad Institute of MIT and Harvard, Cambridge, United States; Computational and Systems Biology Program, Massachusetts Institute of Technology, Cambridge, United States
Mark P Styczynsky
Broad Institute of MIT and Harvard, Cambridge, United States
Jenna Pfiffner
Broad Institute of MIT and Harvard, Cambridge, United States
Courtney French
Broad Institute of MIT and Harvard, Cambridge, United States
Amanda Socha
Broad Institute of MIT and Harvard, Cambridge, United States
Anne Thielke
Broad Institute of MIT and Harvard, Cambridge, United States
Sara Napolitano
Broad Institute of MIT and Harvard, Cambridge, United States
Paul Muller
Broad Institute of MIT and Harvard, Cambridge, United States
Manolis Kellis
Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, United States
Jay H Konieczka
Broad Institute of MIT and Harvard, Cambridge, United States
Ilan Wapinski
Broad Institute of MIT and Harvard, Cambridge, United States
Aviv Regev
Broad Institute of MIT and Harvard, Cambridge, United States; Department of Biology, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, United States
Divergence in gene regulation can play a major role in evolution. Here, we used a phylogenetic framework to measure mRNA profiles in 15 yeast species from the phylum Ascomycota and reconstruct the evolution of their modular regulatory programs along a time course of growth on glucose over 300 million years. We found that modules have diverged proportionally to phylogenetic distance, with prominent changes in gene regulation accompanying changes in lifestyle and ploidy, especially in carbon metabolism. Paralogs have significantly contributed to regulatory divergence, typically within a very short window from their duplication. Paralogs from a whole genome duplication (WGD) event have a uniquely substantial contribution that extends over a longer span. Similar patterns occur when considering the evolution of the heat shock regulatory program measured in eight of the species, suggesting that these are general evolutionary principles.
