The Ceratodon purpureus genome uncovers structurally complex, gene rich sex chromosomes

Abstract

<jats:title>Abstract</jats:title><jats:p>Sex chromosomes occur in diverse organisms, but their structural complexity has often prevented evolutionary analyses. Here we use two chromosome-scale reference genomes of the moss <jats:italic>Ceratodon purpureus</jats:italic> to trace the evolution of the sex chromosomes in bryophytes. Comparative analyses show the moss genome comprises seven remarkably stable ancestral chromosomal elements. An exception is the sex chromosomes, which share thousands of broadly-expressed genes but lack any synteny. We show the sex chromosomes evolved over 300 million years ago and expanded via at least two distinct chromosomal fusions. These results link suppressed recombination between the sex chromosomes with rapid structural change and the evolution of distinct transposable element compositions, and suggest haploid gene expression promotes the evolution of independent female and male gene-regulatory networks.</jats:p><jats:sec><jats:title>One Sentence Summary</jats:title><jats:p>Moss sex chromosomes retain thousands of broadly-expressed genes despite millions of years of suppressed recombination.</jats:p></jats:sec>

Living apart if you can – how genetically and developmentally controlled sex has shaped the evolution of liverworts

“…Empirical data derived from Marchantia polymorpha (Bowman et al, 2017) and Ceratodon purpureus (Carey et al, 2020) agrees largely with the theories in suppressed recombination on both U and V chromosomes with concomitant repetitive element acquisition. The presence of homologs between the U and V, known as gametologs, also supports the prediction that in a haploid organism the essential genes on sex chromosomes are more likely to persist.…”

“…Compared with M. polymorpha, the sex chromosomes of C. purpureus show structural variation between the U and V to a similar extent, and highly differentiated transposable elements accumulation, but with the non-recombining regions younger (McDaniel et al, 2013a;Carey et al, 2020). Carey et al (2020) demonstrated that the sex chromosomes of C. purpureus expanded via at least two distinct chromosomal fusions to form neo-sex chromosomes and most of the numerous sex-linked genes to the non-recombining U and V are of recent recruitment. The authors suggest that the evolution of sexual dimorphism in bryophytes is largely driven by sexual antagonistic selection through sex chromosome rearrangement, including gene translocations and also sex chromosome translocations in some species (Carey et al, 2020).…”

“…Carey et al (2020) demonstrated that the sex chromosomes of C. purpureus expanded via at least two distinct chromosomal fusions to form neo-sex chromosomes and most of the numerous sex-linked genes to the non-recombining U and V are of recent recruitment. The authors suggest that the evolution of sexual dimorphism in bryophytes is largely driven by sexual antagonistic selection through sex chromosome rearrangement, including gene translocations and also sex chromosome translocations in some species (Carey et al, 2020). They further showed that in C. purpureus, genes involved in sexual development and functions evolved faster than other genes, indicating there is distinct set of evolutionary forces acting on sex chromosomes relative to autosomes.…”

“…They further showed that in C. purpureus, genes involved in sexual development and functions evolved faster than other genes, indicating there is distinct set of evolutionary forces acting on sex chromosomes relative to autosomes. Therefore, sex chromosomes should have profound impact on genome evolution, such as lack of ancient polyploidy in liverworts (Bowman et al, 2017), and likely also on speciation process (Carey et al, 2020). This unique feature of sex chromosomes has remained largely unexplored in bryophytes.…”

“…These are the most convincing data on the sex-determining role of specific chromosomes in liverworts. Following these insights, a stasis of several decades ensued until recently, after the sequences of sex chromosomes of a liverwort Marchantia polymorpha (Yamato et al 2007;Bowman et al, 2017) and a moss Ceratodon purpureus (McDaniel et al, 2013a;Carey et al, 2020) were characterized.…”