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 resulted in the transformation of the terrestrial environment. Here we investigate the evolution of the land plants (embryophytes) and their two main lineages, the tracheophytes (vascular plants) and bryophytes (non-vascular plants). We used new fossil calibrations, relative lineage dating implied by horizontal gene transfer, and new phylogenomic methods for mapping gene family origins. Distinct rooting strategies resolve tracheophytes and bryophytes as monophyletic sister groups that diverged during the Cambrian, 515-494 Ma. The embryophyte stem is characterised by a burst of gene innovation, while bryophytes subsequently experienced a no less dramatic episode of reductive genome evolution in which they lost genes associated with the elaboration of vasculature and the stomatal complex. Overall, our analyses confirm that extant tracheophytes and bryophytes are both highly derived; as a result, understanding the origin of land plants requires tracing character evolution across the diversity of modern lineages.

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

“…In bryophytes, that diverged from vascular plants ca. 500-460 MYA and comprise hornworts, liverworts and mosses 20 , a large fraction of TEs are covered by H3K27me3 in the liverwort Marchantia polymorpha 9 while TEs in the model moss Physcomitrium patens are covered mostly by H3K9me2 21 . To address the conservation of the association of H3K27me3 with TEs among bryophytes, we used the model hornwort Anthoceros agrestis that diverged from bryophyte ancestors before the divergence of liverworts from mosses 22 .…”

Loss of Plastid Developmental Genes Coincides With a Reversion to Monoplastidy in Hornworts

“…We found that the gene content of hornworts is significantly lower than tracheophytes and other bryophytes (ANOVA; F = 129.5; d.f. = 2,30; p < 0.001), thereby suggesting that hornwort diversification and speciation were accompanied by significant instances of gene loss ( Supplementary Figure 2 ), even more than what is observed for bryophytes in general ( Harris et al, 2021 ).…”

“…It is evident that hornwort—and bryophyte—emergence and diversification were accompanied by major instances of gene loss ( Harris et al, 2021 ). Our results reinforce this hypothesis, specifically highlighting that the combined loss of certain genes may be responsible for the unique plastid phenotype observed in this group.…”

Loss of plastid developmental genes coincides with a reversion to monoplastidy in hornworts

“…It is evident that hornwort – and bryophyte – emergence and diversification was accompanied by major instances of gene loss (Harris et al 2021). We suggest that a consequence of some of plastid-related gene losses, namely the combined loss of FtsZ2 and ARC3, resulted in hornworts reverting back to a monoplastidic phenotype, which the embryophyte ancestor was able to escape.…”