Distinct patterns of genome size evolution in each bryophyte lineage are not correlated with whole genome duplication.

Abstract

Background and aims: Genome size varies by orders of magnitude across land plants, and the factors driving evolutionary increases and decreases in genome size vary across lineages. Bryophytes have the smallest genomes relative to other land plants and there is growing evidence for frequent whole genome duplication (WGD) across the lineage. However, the broad patterns of genome size, chromosome number, and WGD have yet to be characterized across bryophytes in a phylogenetic context.

Methods: In the present study, we use a phylogenetic comparative approach and leverage previously published data on genome size, chromosome number, and WGD to reconstruct the evolutionary history of these traits across the three major bryophyte lineages: hornworts, liverworts, and mosses. We infer ancestral haploid chromosome numbers for each lineage and introduce a novel metric for assessing polyploidy using chromosome counts.

Key results: Each lineage of bryophytes exhibits a distinct pattern of genome size evolution and prevalence of WGD, with mosses having the most dynamic genome sizes and highest propensity for WGD. We found that 21.3% of mosses and 13% of liverworts species have naturally occurring polyploids. In addition, haploid genome size (1C) is most dynamic in the mosses which includes 15 transitions to larger genomes and nine reversals, largely in the orders Dicranales and Hypnales.

Conclusions: There is no correlation between genome size and WGD or genome size and chromosome number, potentially suggesting rapid genome downsizing following WGD. As bryophytes are poikilohydric (desiccation tolerant) plants, having large genomes may be physiologically prohibitive given the cost to growth and metabolism associated with them. These findings emphasize the unique evolution of the bryophytes broadly and of the hornworts, liverworts, and mosses individually, and should therefore serve as impetus for more in-depth experimental studies of genome size evolution and WGD in bryophytes.