Duplication of a promiscuous transcription factor drives the emergence of a new regulatory network.

Ksenia Pougach,Vladimir Benes,Jan Aerts,Joaquin F Christiaens,Fyodor A Kondrashov,Karin Voordeckers,Patrick Van Dijck,Arnout Voet,Bo Zhu,Kevin J Verstrepen,Bianka Baying,Ryo Sakai

doi:10.1038/ncomms5868

Abstract

The emergence of new genes throughout evolution requires rewiring and extension of regulatory networks. However, the molecular details of how the transcriptional regulation of new gene copies evolves remain largely unexplored. Here we show how duplication of a transcription factor gene allowed the emergence of two independent regulatory circuits. Interestingly, the ancestral transcription factor was promiscuous and could bind different motifs in its target promoters. After duplication, one paralogue evolved increased binding specificity so that it only binds one type of motif, whereas the other copy evolved a decreased activity so that it only activates promoters that contain multiple binding sites. Interestingly, only a few mutations in both the DNA-binding domains and in the promoter binding sites were required to gradually disentangle the two networks. These results reveal how duplication of a promiscuous transcription factor followed by concerted cis and trans mutations allows expansion of a regulatory network.

Highlights

The emergence of new genes throughout evolution requires rewiring and extension of regulatory networks
We have previously shown that the MALS genes in S. cerevisiae underwent several duplication events, with some of the paralogues gaining a novel hydrolyzing activity towards a 1–6 glycosidic bonds, while other MalS paralogues retained the ancestral preference for a 1–4 glycosidic bonds[7,36]
The genome of S. bayanus contains only one MALR of the promiscuous MALX3 type (Arg in the position 12) and lacks the palatinose-specific Yfl052w-like regulator, which is present in S. cerevisiae, S. paradoxus, S. mikatae and S. kudriavzevii

Summary

Introduction

The emergence of new genes throughout evolution requires rewiring and extension of regulatory networks. To confirm the binding sites of the different MalR regulators (Malx[3] and Yfl052w), we first deleted the binding sites in a strain carrying a fluorescent reporter fusion of a maltose-specific target gene (MAL32) and in a strain carrying a reporter for a palatinosespecific gene (IMA5).

Results

Conclusion