Intrinsic cooperativity potentiates parallel cis-regulatory evolution

Elife. 2018 Sep 10:7:e37563. doi: 10.7554/eLife.37563.

Abstract

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 cis-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 cis-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.

Keywords: Kluyveromyces lactis; S. cerevisiae; chromosomes; evolution; evolutionary biology; gene expression; transcription factors.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • DNA-Binding Proteins / genetics
  • Fungal Proteins / genetics
  • Gene Expression Regulation, Fungal
  • Minichromosome Maintenance 1 Protein / genetics*
  • Regulatory Elements, Transcriptional / genetics
  • Ribosomal Proteins / genetics*
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae Proteins / genetics*
  • Shelterin Complex
  • Telomere-Binding Proteins / genetics*
  • Transcription Factors / genetics*

Substances

  • DNA-Binding Proteins
  • Fungal Proteins
  • MCM1 protein, S cerevisiae
  • Minichromosome Maintenance 1 Protein
  • RAP1 protein, S cerevisiae
  • Ribosomal Proteins
  • Saccharomyces cerevisiae Proteins
  • Shelterin Complex
  • Telomere-Binding Proteins
  • Transcription Factors