Divergent evolutionary trajectories of bryophytes and tracheophytes from a complex common ancestor of land plants

Abstract

The origin of plants and their colonization of land fundamentally transformed the terrestrial environment. Here we elucidate the basis of this formative episode in Earth history through patterns of lineage, gene and genome evolution. We use new fossil calibrations, a relative clade age calibration (informed by horizontal gene transfer) and new phylogenomic methods for mapping gene family origins. Distinct rooting strategies resolve tracheophytes (vascular plants) and bryophytes (non-vascular plants) as monophyletic sister groups that diverged during the Cambrian, 515–494 million years ago. The embryophyte stem is characterized by a burst of gene innovation, while bryophytes subsequently experienced an equally dramatic episode of reductive genome evolution in which they lost genes associated with the elaboration of vasculature and the stomatal complex. Overall, our analyses reveal that extant tracheophytes and bryophytes are both highly derived from a more complex ancestral land plant. Understanding the origin of land plants requires tracing character evolution across a diversity of modern lineages.

The ancestral chromatin landscape of land plants

“…To address the conservation of the association of PTMs of chromatin and DNA methylation among bryophytes, we used the model hornwort Anthoceros agrestis that diverged from bryophyte ancestors earlier than liverworts and mosses (Puttick et al, 2018; Harris et al, 2021). We used Enzymatic Methyl-seq (Vaisvila et al, 2021) to obtain a genome wide profile of 5-methylated cytosine from four week old vegetative tissue of A. agrestis .…”

“…500-480 MYA from the vascular plants. Bryophytes comprise three monophyletic groups – hornworts, liverworts and mosses (Harris et al, 2021). Five histone PTMs and DNA methylation have been profiled in the genomes of two model bryophytes, the moss Physcomitrium patens (Yaari et al, 2019; Widiez et al, 2014) and the model liverwort Marchantia polymorpha (Ikeda et al, 2018; Montgomery et al, 2020).…”

­Evolution of the most species-rich family of simple thalloid liverworts (Aneuraceae): a time-calibrated perspective into its evolutionary history and diversification

“…5 Mya, using six combinations of fossil calibration(Cardinal-McTeague et al 2016). Even in the fossil-rich genus of Previous estimates of early land plant divergences from chronograms have been a subject of much debate, as they tend to extend into the time before the known date for the earliest land plant (475 Mya;Bowles et al, 2022;Graur & Martin, 2004;Harris et al, 2022;Morris et al, 2018). Our estimate of the origin of Metzgeriidae also experienced a similar issue of a wide HPD interval, likely due to the small number of fossils.…”

Diverse branching forms regulated by a core auxin transport mechanism in plants

“…As some of the earliest land plant macrofossils comprise bifurcating axes with terminal sporangia but no specialised water conducting cells (e.g. Edwards et al, 2021, 2022), and there is growing evidence of evolutionary loss in the bryophytes (Harris et al, 2020, 2021), we speculate that the single-stemmed state of bryophyte sporophytes was derived from a last common ancestor of land plants manifesting PIN-regulated bifurcation (Fig. 7A).…”