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Coeevolution of a transcriptional network by compensatory trans and cis mutations

ABSTRACT: Transcriptional networks have been shown to evolve very rapidly, prompting questions as to how such changes arise and are tolerated. Recent comparisons of transcriptional networks across species have implicated variations in the cis-acting DNA sequences near genes as the main cause of divergence. What is less clear is how these changes interact with trans-acting changes occurring elsewhere in the genetic circuit. Here, we report the discovery of a system of compensatory trans and cis mutations in the yeast AP-1 transcriptional network that allows for conserved transcriptional regulation despite continued genetic change. We pinpoint a single species, the fungal pathogen Candida glabrata, in which a trans mutation has occurred very recently in a single AP-1 family member distinguishing it from its Saccharomyces ortholog. Comparison of chromatin immunoprecipitation profiles between Candida and Saccharomyces shows that, despite their different DNA binding domains, the AP-1 orthologs regulate a conserved block of genes. This conservation is enabled by concomitant changes in the cis-regulatory motifs upstream of each gene. Thus, both trans and cis mutations have perturbed the yeast AP-1 regulatory system in such a way as to compensate for one another. This demonstrates an example of “co-evolution” between a DNA-binding transcription factor and its cis-regulatory site, reminiscent of the co-evolution of protein binding partners.

ORGANISM(S): Nakaseomyces glabratus Saccharomyces cerevisiae

PROVIDER: GSE15818 | GEO | 2010/09/17

SECONDARY ACCESSION(S): PRJNA116737

REPOSITORIES: GEO

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Project description:Changes in gene regulation rapidly accumulate between species and may contribute to reproductive isolation through misexpression of genes in interspecific hybrids. Hybrid misexpression, defined by expression levels outside the range of both parental species, is thought to be a result of cis- and trans-acting regulatory changes that interact in the hybrid, or arise from changes in the relative abundance of various tissues or cell types due to defects in developmental. Here, we show that misexpressed genes in a sterile interspecific Saccharomyces yeast hybrid result from a heterochronic shift in the timing of the normal meiotic gene expression program. By tracking nuclear divisions, we find that S. cerevisiae initiates meiosis earlier than its closest known relative, S. paradoxus, yet both species complete meiosis at the same time. Although the hybrid up- and down-regulates genes in a similar manner to both parents, the hybrid meiotic program occurs earlier than both parents. The timing shift results in a heterochronic pattern of misexpression throughout meiosis I and the beginning of meiosis II. Coincident with the timing of misexpression, we find an increase in the relative abundance of opposing cis and trans-acting changes and compensatory changes, as well as a transition from predominantly trans-acting to cis-acting expression divergence over the course of meiosis. However, misexpression does not appear to be a direct consequence of cis- and trans-acting regulatory divergence. Our results demonstrate that hybrid misexpression in yeast results from a heterochronic shift in the meiotic gene expression program. We analyzed three biological replicates of the parental yeast strains, S. cerevisiae and S. paradoxus, and four replicates of their hybrid over four developmental time points. Two hybrid replicates contain MATa from S. cerevisiae and MATalpha from S. paradoxus. The other two hybrid replicates are reciprocal crosses. The developmental time points are T0, which serves as a control, and is the moment cells enter sporulation media. M1 is the beginning of meiosis I. M1/M2 is the overlap of the end of meiosis I and the beginning of meiosis II. M2 is the end of meiosis II.

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Coeevolution of a transcriptional network by compensatory trans and cis mutations

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