Yangyun Zou1, Wei Huang1, Zhenglong Gu2, Xun Gu1,3,*
1MOE Key Laboratory of Contemporary Anthropology and Center for Evolutionary Biology, School of Life Sciencesand Institutes of Biomedical Sciences, Fudan University, Shanghai, 200433, China; 2Division of Nutritional Sciences, Cornell University, Ithaca, New York, 14850,USA. 3Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IA 50011, USA; *Correspondence to: xgu.@iastate.edu
Mol Biol Evol (2011) 28: 2893-2904
Abstract
TATA box, the core promoter element, exists in a broad range of eukaryotes, and the expression of TATA-containing genes usually responds to various environmental stresses. Hence, the evolution of TATA-box in duplicate genes may provide some clues for the interrelationship among environmental stress, expression differentiation, and duplicate gene preservation. In the present study, we observed that the TATA box is significantly overrepresented in duplicate genes compared with singletons in human, worm, Arabidopsis, and yeast genomes. We then conducted an extensive functional genomic analysis to investigate the evolution of TATA box along over 700 yeast gene family phylogenies. After reconstructing the ancestral TATA-box states (presence or absence), we found that significantly higher numbers of TATA box gain events than loss events had occurred after yeast gene duplications—the overall gain–loss ratio is about 3–4 to 1. Interestingly, these TATA-gain duplicate genes on average have experienced greater expression divergence from the ancestral expression states than their most closely related TATA-less duplicate partners, but only under environmental stress conditions (asymmetric evolution); indeed, under normal physiological conditions, they have similar expression divergence (symmetric evolution). Moreover, we showed that TATA-gain duplicates are enriched in stress-associated functional categories but that is not the case for TATA-ancestral duplicates (those inherited from their ancestors prior to duplication). Together, we conclude that after the gene duplication, gain of the TATA box in duplicate promoters may have played an important role in yeast duplicate preservation by accelerating expression divergence that may facilitate the adaptive evolution of the organism in response to environmental changes.