Intrinsic cooperativity potentiates parallel cis -regulatory evolution

• Published in: eLife Vol. 7
• Main Authors: Sorrells, Trevor R, Johnson, Amanda N, Howard, Conor J, Britton, Candace S, Fowler, Kyle R, Feigerle, Jordan T, Weil, P Anthony, Johnson, Alexander D
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 10.09.2018; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Base sequence; BASIC BIOLOGICAL SCIENCES; Binding sites; Biophysics; Butterflies; Chromosomes and Gene Expression; Convergent evolution; Cooperativity; DNA; DNA binding; DNA sequencing; DNA-Binding Proteins - genetics; Drug resistance; ENVIRONMENTAL SCIENCES; Evolution; Evolution (Biology); Evolutionary Biology; Experiments; Fungal Proteins - genetics; Fungi; Gene expression; Gene Expression Regulation, Fungal; Genes; Genetic regulation; Genetic research; Genomes; Genomics; Kluyveromyces lactis; Life Sciences & Biomedicine - Other Topics; Minichromosome Maintenance 1 Protein - genetics; Mutation; Pathogenic microorganisms; Protein binding; Proteins; Rap1 protein; Regulatory Elements, Transcriptional - genetics; Regulatory proteins; Regulatory sequences; Ribosomal proteins; Ribosomal Proteins - genetics; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae Proteins - genetics; Stock prices; Telomere-Binding Proteins - genetics; TFIID protein; Transcription (Genetics); Transcription activation; transcription factors; Transcription Factors - genetics; United States > US; San Francisco California; California; evolutionary biology; transcription factors; chromosomes; Kluyveromyces lactis; evolution; gene expression; S. cerevisiae
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.37563

Convergent evolutionary events in independent lineages provide an opportunity to understand why evolution favors certain outcomes over others. We studied such a case where a large set of genes-those coding for the ribosomal proteins-gained -regulatory sequences for a particular transcription regulator (Mcm1) in independent fungal lineages. We present evidence that these gains occurred because Mcm1 shares a mechanism of transcriptional activation with an ancestral regulator of the ribosomal protein genes, Rap1. Specifically, we show that Mcm1 and Rap1 have the inherent ability to cooperatively activate transcription through contacts with the general transcription factor TFIID. Because the two regulatory proteins share a common interaction partner, the presence of one ancestral -regulatory sequence can 'channel' random mutations into functional sites for the second regulator. At a genomic scale, this type of intrinsic cooperativity can account for a pattern of parallel evolution involving the fixation of hundreds of substitutions.