From elements to modules: regulatory evolution in Ascomycota fungi

Abstract

SummaryRegulatory divergence is likely a major driving force in evolution. Comparative transcriptomics provides a new glimpse into the evolution of gene regulation. Ascomycota fungi are uniquely suited among eukaryotes for studies of regulatory evolution, due to broad phylogenetic scope, many sequenced genomes, and facility of genomic analysis. Here we review the substantial divergence in gene expression in Ascomycota and how this is reconciled with the modular organization of transcriptional networks. We show that flexibility and redundancy in both cis-and trans-regulation can lead to changes from altered expression of single genes to wholesale re-wiring of regulatory modules. Redundancy thus emerges as a major driving force facilitating expression divergence while preserving the coherent functional organization of a transcriptional response.

Gene duplication and the evolution of ribosomal protein gene regulation in yeast

“…Our comparative computational and experimental approach shows how gene duplication can constrain and drive regulatory evolution and provides a general strategy for reconstructing the evolutionary trajectory of gene regulation across species. T he coordinated expression of modules of functionally related genes, such as ribosomal proteins or oxidative phosphorylation enzymes, is often conserved at great evolutionary distances (1). This is consistent with a selective pressure to conserve coordinated transcript levels to maintain functional cellular modules.…”

“…As previously shown, the outgroup species C. albicans has a different cis-regulatory organization, dominated by binding sites for Tbf1 and Cbf1 and lacking directly discernible IFHL sites (5). Because the Ifh1/Fhl1 complex is physically associated with RP gene promoters in C. albicans (6), there are two possibilities for this discrepancy: (1) Fhl1 and Ifh1 bind indirectly through the Tbf1 protein (6), or (2) the Fhl1 protein recognizes a variant site, similar to the Tbf1 consensus (1,4). Both cases are consistent with Ifh1's role as a regulator of RP gene expression in C. albicans.…”

“…This is consistent with a selective pressure to conserve coordinated transcript levels to maintain functional cellular modules. Recent studies have shown that the regulatory mechanisms controlling conserved modules can diverge, most notably by switching from one regulatory system to another while preserving coregulation (1,2). However, because previous studies have typically relied on functional expression data from only one or two species, it is unknown whether these changes in regulatory mechanisms affect the expression levels of a module's genes at all or whether both coexpression and expression levels are conserved.…”

Arboretum: Reconstruction and analysis of the evolutionary history of condition-specific transcriptional modules

“…Comparative functional genomics approaches are increasingly used to study regulatory evolution in unicellular ( Jensen et al 2006;Gasch 2007; Thompson and Regev 2009;Wohlbach et al 2009;Romero et al 2012) and multicellular organisms (Brawand et al 2011;Schmidt et al 2012;Xiao et al 2012). Such studies measure and compare genomic profiles, including mRNA levels (Bergmann et al 2003b;Tirosh et al 2006;Wapinski et al 2010;Brawand et al 2011;Fowlkes et al 2011;Rhind et al 2011;Tirosh et al 2011), chromatin organization (Segal et al 2006;Tsankov et al 2010;Xiao et al 2012), or protein-DNA interactions (Borneman et al 2007;Schmidt et al 2010Schmidt et al , 2012Kutter et al 2011) across two or more species.…”

The Transcription Factors Tec1 and Ste12 Interact with Coregulators Msa1 and Msa2 To Activate Adhesion and Multicellular Development

“…In Drosophila and mammals, for example, the TEA regulators Scalloped and TEAD1 to -4 are known to control development by interacting with the coactivators Yki and YAP, which are not found in fungi (67)(68)(69). Thus, not only adaptation of DNA-binding domains and cis-regulatory sequences but also the development of novel coregulators might be important to drive the evolution of fungal transcriptional regulatory networks (70)(71)(72).…”