Dataset Information

Cis-regulatory evolution in prokaryotes revealed by interspecific archaeal hybrids.

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.

SUBMITTER: Artieri CG

PROVIDER: S-EPMC5479820 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Cis-regulatory evolution in prokaryotes revealed by interspecific archaeal hybrids.

Artieri Carlo G CG Naor Adit A Turgeman-Grott Israela I Zhou Yiqi Y York Ryan R Gophna Uri U Fraser Hunter B HB

Scientific reports 20170621 1

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 st ...[more]

PMID: 28638059

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Project description:Hybrid progeny can enjoy increased fitness and stress tolerance relative to their ancestral species, a phenomenon known as hybrid vigor. Though this phenomenon has been documented throughout the Eukarya, evolution of hybrid populations has yet to be explored experimentally in the lab. To fill this knowledge gap we created a pool of Saccharomyces cerevisiae and S. bayanus homoploid and aneuploid hybrids, and then investigated how selection in the form of incrementally increased temperature or ethanol impacted hybrid genome structure and adaptation. During 500 generations of continuous ammonia-limited, glucose-sufficient culture, temperature was raised from 25C to 46??C. This selection invariably resulted in nearly-complete loss of the S. bayanus genome, although the dynamics of genome loss differed among independent replicates. Temperature-evolved isolates were significantly more thermal tolerant and exhibited greater phenotypic plasticity than parental species and founding hybrids. By contrast, when the same hybrid pool was subjected to increases in exogenous ethanol from 0% to 14%, selection favored euploid S. cerevisiae x S. bayanus hybrids. Ethanol-evolved isolates exhibited significantly greater ethanol tolerance relative only to S. bayanus and one of the founding hybrids tested. Adaptation to thermal and ethanol stress manifested as heritable changes in cell wall structure demonstrated by resistance to zymolyase or micafungin treatment. This is the first study to show experimentally that the fate of interspecific hybrids critically depends on the type of selection they encounter during the course of evolution. Array-CGH was performed on the S. cerevisiae parent strain CEN.PK (GSY2160), the S. bayanus parent strain CBS7001 (GSY2161) and on the F1 interspecific hybrid resulting from mating the 2 parents (GSY2168). Additionally, three rare viable spores obtained after sporulation of the F1 were assayed by array-CGH (F2a, F2b, F2c). A large pool of F2 spores (and probably some number of F1 hybrid cells) were subjected to gradually increasing temperatures, in three independent vessels, with populations sampled at various generation times. Likewise, the same pool was used to found populations in an additional three independent vessels, which were then subjected to gradually increasing ethanol concentrations (at constant temperature). Array-CGH was performed on three different clones from each of the three temperature vessels at the final 500 generation time point (T500 clones). Biological replicates of the T500 clones were performed (T500-new). Two self-self array-CGH hybridization controls were also performed (self-control). Array-CGH was performed on one clone from each of the three ethanol vessels taken at the 400 generation timepoint (EtOH400gen clones).

Dataset Information

Cis-regulatory evolution in prokaryotes revealed by interspecific archaeal hybrids.

Publications

Cis-regulatory evolution in prokaryotes revealed by interspecific archaeal hybrids.

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