Characterization of UV sex chromosomes and synteny-guided phylogenomic resolution of subgenomes in Bryopsida mosses

Abstract

The UV chromosomal sex-determination system primarily found in bryophytes, together with the XY and ZW chromosomal sex-determination systems, constitute the three principal types of chromosomal sex determination systems in nature. In this report, the genome of the moss Bryum argenteum was sequenced and assembled into 11 chromosomes containing 17,721 protein coding genes. A giant female U sex chromosome demonstrated conspicuously lower gene density, higher repeat coverage, and higher GC content compared to the ten autosomes. By further characterizing the sex-chromosomes and sex-linked genes in seven chromosomal-scale Bryopsida genomes, lower gene densities and distinct GC contents were revealed to be common in all moss sex chromosomes, likely resulting from degeneration. Weaker purifying selection, as evidenced by lower codon usage preference in sex-linked genes, was shared in most but not all Bryopsida mosses. Retained genomic syntenies between U/V sex chromosomes and ancestral Bryopsida chromosome 4 provided new evidence to support an autosomal origin for sex chromosomes. The seven ancestral Bryopsida chromosomes were reconstructed to decipher and depict chromosomal evolution; Dicranidae and Bryidae mosses demonstrated one and three chromosomal fusions and evolved 13 and 11 ancestral chromosomes, respectively. Ancient whole genome duplications characterized many plant lineages including the psi polyploidy event that occurred in the early diversification of Bryopsida. By aligning the modern chromosomes to the seven reconstructed ancestral chromosomes, genomic synteny-guided phylogenomic analyses provided strong evidence for the ancestral psi event shared by Dicranidae, Bryidae and P. patens. Furthermore, ancestral chromosomal projections and a phylogenomic resolution of Bryopsida subgenomes revealed distinct and lineage-specific chromosomal loss patterns in Dicranidae and Bryidae following the psi event. Our reconstructions reinforced the evolutionary significance and phylogenetic timing of the psi event and provided systemic insights into the sex and chromosomal evolution in mosses.