Widespread loss of Y expression in the absence of transcriptional dosage compensation in Rumex hastatulus

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Abstract

There is growing interest in the potential role of gene regulatory evolution in the expansion and degeneration of Y chromosomes. Evolutionarily young sex chromosomes, such as those found in the flowering plant Rumex hastatulus, can provide insights into the early stages of this process. Using a new high-quality genome assembly with a well-assembled Y chromosome and a highly replicated transcriptome dataset, we found widespread underexpression of Y genes compared to their homologous counterparts on the X chromosome. We also found evidence for increased expression differences for more distantly diverged gametologs, suggestive of progressive loss of expression of Y linked genes over time. Genes with greater expression loss on the Y chromosome also showed elevated rates of protein evolution, as expected if silencing alleles mask the effects of deleterious mutations on the Y and/or if selective interference drives early degeneration in regulatory sequences. However, in contrast with the predictions of recent models of sex chromosome expansion and degeneration by regulatory evolution, there was no evidence of early dosage compensation. Overall, we conclude that in Rumex Hill-Robertson interference alone may be the main driver of Y chromosome degeneration, although further understanding of the temporal order of regulatory changes could help further untangle cause and effect.

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