The rewiring of transcription circuits in evolution

Abstract

The binding of transcription regulators to cis-regulatory sequences is a key step through which all cells regulate expression of their genes. Due to gains and losses of cis-regulatory sequences and changes in the transcription regulators themselves, the binding connections between regulators and their target genes rapidly change over evolutionary time and constitute a major source of biological novelty. This review covers recent work, carried out in a wide range of species, that addresses the overall extent of these evolutionary changes, their consequences, and some of the molecular mechanisms that lie behind them.

The antitoxin MqsA homologue in Pseudomonas fluorescens 2P24 has a rewired regulatory circuit through evolution

“…Since agtR is regulated by PfMqsA, it is very likely that PfMqsA could also influence diverse aspects of the physiology of P. fluorescens 2P24 through the rewired AgtR-mediated regulatory circuit. As previously proposed, the overall output of the regulatory circuit may remain more or less constant despite extensive evolutionary rewiring (Johnson, 2017). However, with respect to the mqsA regulatory circuit, it is still unknown to what extent the output of the circuit is preserved over evolutionary time.…”

“…In this work, we identified the consensus DNA motif [5′‐TACCCT(N) 3 AGGGTA‐3′] recognized by PfMqsA in the upstream region of the PfmqsRA operon and this motif is different from the shorter consensus motif [5′‐ACCT(N) 2‐4 AGGT‐3′] recognized by EcMqsA and PpMqsA. Another type of genetic change that can lead to evolutionary rewiring is a gain or loss of cis ‐regulatory sequences (Johnson, ). In both P. fluorescens 2P24 and P. putida , no MqsA binding motifs were found in promoter regions of rpoS , csgD and cspD , which are regulated by EcMqsA and involved in persister cell formation in E coli (Kim and Wood, ; Wang et al, ; Soo and Wood, ).…”

Identification of genes regulated by a jasmonate- and salt-inducible transcription factor JRE3 in tomato

“…In the sense of metabolic evolution, it is indicative that GO terms, catalytic activity and transferase, are enriched among the JRE3-regulated genes. To reveal possibly frequent rewiring of gene networks (Johnson 2017), which is considered prerequisite for rise of the metabolic regulons (Shoji 2018), it is worth to address whether and if so how much genes regulated by are shared among the non-alkaloidal ERFs from same and different species.…”

The mechanisms of gene regulatory networks constrain evolution: A lesson from synthetic circuits

“…Comparisons of GRNs in related species indicate that they indeed solve the problem of producing a specific adaptive phenotype in many different ways, and that these solutions diverge substantially on evolutionary time scales, even when the ultimate phenotype stays qualitatively the same (Dalal and Johnson, 2017; Johnson, 2017; Savageau, 1983; True and Haag, 2001; Weiss and Fullerton, 2000). Examples include the GRN that regulates mating in yeast: Even though both Saccharomyces cerevisiae and Candida albicans produce two mating types (a-cells and α-cells), the circuit responsible for determining these mating type has changed substantially during evolution (Sorrells et al, 2015; Tsong et al, 2006).…”