Plastic Rewiring of Sef1 Transcriptional Networks and the Potential of Nonfunctional Transcription Factor Binding in Facilitating Adaptive Evolution

Abstract Prior and extensive plastic rewiring of a transcriptional network, followed by a functional switch of the conserved transcriptional regulator, can shape the evolution of a new network with diverged functions. The presence of three distinct iron regulatory systems in fungi that use orthologo...

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Veröffentlicht in:Molecular biology and evolution 2021-11, Vol.38 (11), p.4732-4747
Hauptverfasser: Hsu, Po-Chen, Lu, Tzu-Chiao, Hung, Po-Hsiang, Jhou, Yu-Ting, Amine, Ahmed A A, Liao, Chia-Wei, Leu, Jun-Yi
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container_end_page 4747
container_issue 11
container_start_page 4732
container_title Molecular biology and evolution
container_volume 38
creator Hsu, Po-Chen
Lu, Tzu-Chiao
Hung, Po-Hsiang
Jhou, Yu-Ting
Amine, Ahmed A A
Liao, Chia-Wei
Leu, Jun-Yi
description Abstract Prior and extensive plastic rewiring of a transcriptional network, followed by a functional switch of the conserved transcriptional regulator, can shape the evolution of a new network with diverged functions. The presence of three distinct iron regulatory systems in fungi that use orthologous transcriptional regulators suggests that these systems evolved in that manner. Orthologs of the transcriptional activator Sef1 are believed to be central to how iron regulatory systems developed in fungi, involving gene gain, plastic network rewiring, and switches in regulatory function. We show that, in the protoploid yeast Lachancea kluyveri, plastic rewiring of the L. kluyveri Sef1 (Lk-Sef1) network, together with a functional switch, enabled Lk-Sef1 to regulate TCA cycle genes, unlike Candida albicans Sef1 that mainly regulates iron-uptake genes. Moreover, we observed pervasive nonfunctional binding of Sef1 to its target genes. Enhancing Lk-Sef1 activity resuscitated the corresponding transcriptional network, providing immediate adaptive benefits in changing environments. Our study not only sheds light on the evolution of Sef1-centered transcriptional networks but also shows the adaptive potential of nonfunctional transcription factor binding for evolving phenotypic novelty and diversity.
doi_str_mv 10.1093/molbev/msab192
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subjects Candida albicans - genetics
Discoveries
Gene Regulatory Networks
Plastics - metabolism
Transcription Factors - genetics
Transcription Factors - metabolism
Yeasts - genetics
title Plastic Rewiring of Sef1 Transcriptional Networks and the Potential of Nonfunctional Transcription Factor Binding in Facilitating Adaptive Evolution
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