2017Genome Biology and EvolutionOpen access

Genome Expression Balance in a Triploid Trihybrid Vertebrate

Kyle E. McElroy, Robert D. Denton, Joel Sharbrough, Laura Bankers, Maurine Neiman, H. Lisle Gibbs

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Abstract

Polyploidy is increasingly recognized as a driver of biological diversity. How and why polyploidization affects gene expression is critical to understanding the link between ploidy elevation and diversification. In polyploid plants, multiple studies have demonstrated that ploidy elevation can confer major but variable consequences for gene expression, ranging from gene-by-gene alterations to entirely silenced genomes. By contrast, animal polyploids remain largely uncharacterized. Accordingly, how animals respond to and manage polyploidy events is not understood. Here, we address this important knowledge gap by analyzing transcriptomes from a triploid hybrid animal, a unisexual Ambystoma salamander, and three sexual Ambystoma species that represent all three parental genomes in the unisexual. We used a novel bioinformatics pipeline that includes competitively mapping triploid sequences to a reference set of orthologous genes in the sexual species to evaluate subgenome expression. Our comparisons of gene expression levels across the three parental genomes revealed that the unisexual triploid displays a pattern of genome balance, where 72% of the genes analyzed were expressed equally among the subgenomes. This result is strikingly different from the genome imbalance typically observed in hybrid polyploid plants. Our analyses represent the first to address gene expression in a triploid hybrid animal and introduce a novel bioinformatic framework for analyzing transcriptomic data.

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Polyploidy is increasingly recognized as a driver of biological diversity. How and why polyploidization affects gene expression is critical to understanding the link between ploidy elevation and diversification. In polyploid plants, multiple studies have demonstrated that ploidy elevation can confer major but variable consequences for gene expression, ranging from gene-by-gene alterations to entirely silenced genomes. By contrast, animal polyploids remain largely uncharacterized. Accordingly, how animals respond to and manage polyploidy events is not understood. Here, we address this important knowledge gap by analyzing transcriptomes from a triploid hybrid animal, a unisexual Ambystoma salamander, and three sexual Ambystoma species that represent all three parental genomes in the unisexual. We used a novel bioinformatics pipeline that includes competitively mapping triploid sequences to a reference set of orthologous genes in the sexual species to evaluate subgenome expression. Our comparisons of gene expression levels across the three parental genomes revealed that the unisexual triploid displays a pattern of genome balance, where 72% of the genes analyzed were expressed equally among the subgenomes. This result is strikingly different from the genome imbalance typically observed in hybrid polyploid plants. Our analyses represent the first to address gene expression in a triploid hybrid animal and introduce a novel bioinformatic framework for analyzing transcriptomic data.

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Available abstract

Polyploidy is increasingly recognized as a driver of biological diversity. How and why polyploidization affects gene expression is critical to understanding the link between ploidy elevation and diversification. In polyploid plants, multiple studies have demonstrated that ploidy elevation can confer major but variable consequences for gene expression, ranging from gene-by-gene alterations to entirely silenced genomes. By contrast, animal polyploids remain largely uncharacterized. Accordingly, how animals respond to and manage polyploidy events is not understood. Here, we address this important knowledge gap by analyzing transcriptomes from a triploid hybrid animal, a unisexual Ambystoma salamander, and three sexual Ambystoma species that represent all three parental genomes in the unisexual. We used a novel bioinformatics pipeline that includes competitively mapping triploid sequences to a reference set of orthologous genes in the sexual species to evaluate subgenome expression. Our comparisons of gene expression levels across the three parental genomes revealed that the unisexual triploid displays a pattern of genome balance, where 72% of the genes analyzed were expressed equally among the subgenomes. This result is strikingly different from the genome imbalance typically observed in hybrid polyploid plants. Our analyses represent the first to address gene expression in a triploid hybrid animal and introduce a novel bioinformatic framework for analyzing transcriptomic data.

Key concepts: Biology, Polyploid, Genome, Gene, Ploidy, Genetics, Transcriptome, Evolutionary biology

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