Abstract

Author SummaryThe mammalian sex chromosomes originated from an ancestral pair of autosomes about 150 million years ago and the Y chromosome subsequently degenerated, losing most of its genes. During this process, a phenomenon called dosage compensation evolved to compensate for the gene loss on the Y chromosome and to equalize expression of X-linked genes in the two sexes. In humans, this is achieved by inactivating one of the two X chromosomes in females. Dosage compensation has also been reported in other animal XY systems such as fruit flies and worms, each 100 million years old or more. Here we studied dosage compensation in plants. We used high-throughput RNA sequencing in male and female Silene latifolia (white campion)—a dioecious plant whose XY chromosomes originated only about 10 million years ago—to identify hundreds of sex-linked genes. Analysis of their expression patterns in males and females revealed equal doses of sex-linked transcripts in both sexes, regardless of the degree of reduction of Y expression due to degeneration. Our results thus show that dosage compensation occurs in plants and is thus not an animal-specific phenomenon. They also reveal that proportionate dosage compensation can evolve rapidly de novo after the origin of sex chromosomes.

Highlights

  • In humans, where the evolution of sex chromosomes is probably best known, the XY chromosome pair was originally a recombining pair of autosomes that progressively stopped recombining, most likely because of a series of inversions on the Y chromosome [1,2,3,4]

  • To estimate how many sex-linked contigs we missed with our method, we checked how many of the previously identified sex-linked genes were among our sex-linked contigs (Table S3). 42% of these were not found, which means that our rate of false negatives is quite high, and we identified a subset of the sex-linked genes in S. latifolia

  • As Chibalina and Filatov (2011) analyzed crosses, they were able to identify X-linked genes without detectable homologous Y-linked copies. They compared the expression levels of these hemizygous genes between sexes, found a significantly reduced expression in males compared to females, and concluded that this was evidence for the absence of dosage compensation in S. latifolia [42]

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Summary

Introduction

In humans, where the evolution of sex chromosomes is probably best known, the XY chromosome pair was originally a recombining pair of autosomes that progressively stopped recombining, most likely because of a series of inversions on the Y chromosome [1,2,3,4]. Previous work suggests that S. latifolia XY chromosomes have stopped recombining gradually [21,22,25] and that the Y is undergoing degeneration (gene loss, reduced polymorphism, accumulation of repeats, maladapted proteins, reduced gene expression) as in animal sex chromosomes [26,27,28,29,30,31,32,33,34] Despite these highly interesting results, work on sex chromosome evolution in S. latifolia has been limited by the slow pace of sex-linked gene identification

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