Abstract
The study of allele-specific expression (ASE) in interspecific hybrids has played a central role in our understanding of a wide range of phenomena, including genomic imprinting, X-chromosome inactivation, and cis-regulatory evolution. However across the hundreds of studies of hybrid ASE, all have been restricted to sexually reproducing eukaryotes, leaving a major gap in our understanding of the genomic patterns of cis-regulatory evolution in prokaryotes. Here we introduce a method to generate stable hybrids between two species of halophilic archaea, and measure genome-wide ASE in these hybrids with RNA-seq. We found that over half of all genes have significant ASE, and that genes encoding kinases show evidence of lineage-specific selection on their cis-regulation. This pattern of polygenic selection suggested species-specific adaptation to low phosphate conditions, which we confirmed with growth experiments. Altogether, our work extends the study of ASE to archaea, and suggests that cis-regulation can evolve under polygenic lineage-specific selection in prokaryotes.
Highlights
For the past 50 years, interspecific hybrids have been an invaluable resource for studying the regulation of gene expression
We have previously shown that H. volcanii and H. mediterranei are able to efficiently mate and generate interspecies recombinants[14]
In order to generate a stable H. volcanii × H. mediterranei hybrid, we needed to prevent the possibility of recombination between chromosomes, forcing the hybrid to retain both parental chromosomes
Summary
For the past 50 years, interspecific hybrids have been an invaluable resource for studying the regulation of gene expression. Despite the multitude of studies employing ASE (over 750 publications when searching “allele-specific expression” or “allele-specific gene expression” in PubMed abstracts), a limitation shared by all of them is that they have been restricted to eukaryotes The reason for this is that prokaryotes do not undergo sexual reproduction, so generating hybrids has not been possible. Some halophilic archaea can undergo a fusion process that can generate hybrid cells[11, 12] This process is efficient even between different species, but the heterozygous hybrid state is unstable due to gene conversion events[13], as well as large-scale recombination events that result in homozygous recombinants[14]. This obstacle by maintaining two different selection markers at the same genetic locus in the two parental species. In such a condition any homologous recombination event will result in swapping one selection marker for the other, and as long as one selects for both markers, only heterozygous cells will survive, assuming no ectopic recombination occurs
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