Evidence for evolution of a new sex chromosome within the Marchantiales haploid plant lineage

Sex chromosome have evolved independently in numerous lineages across the tree of life, in both diploid-dominant species, including many animals and plants, and the less studied haploid-dominant plants and algae. Strict genetic sex determination ensures that individuals reproduce by outcrossing. However, species with separate sexes (termed dioecy in diploid plants, and dioicy in haploid plants) may sometimes evolve different sex systems, and become monoicous, with the ability to self-fertilize. Here, we study dioicy-monoicy transitions in the ancient liverwort haploid plant lineage, using three telomere-to-telomere gapless chromosome-scale reference genome assemblies from the Ricciaceae group of Marchantiales. Ancestral liverworts are believed to have been dioicous, with U and V chromosomes determining femaleness and maleness, respectively. We confirm the finding that monoicy inRicciocarpos natansevolved from a dioicous ancestor, and most ancestrally U chromosomal genes have become autosomal in this species. We also describe evidence suggesting the re-evolution of dioicy in the genusRiccia, with probablede novoestablishment of a sex chromosome from an autosome, and further translocations of genes from the new sex chromosome to autosomes. Our results also indicated that m-chromosomes are consistent genomic features, and may have evolved independently from sex chromosomes inRicciocarposandRiccialineages.