Phylogenomics unveil a recent origin of morphological complexity in Coleochaetophyceae

Abstract

Land plants (embryophytes) are the morphologically most elaborate photosynthetic eukaryotes. The evolutionary origin of many of their key morphogenetic processes can be traced back to ancestors with those close streptophyte algal relatives that belong—together with embryophytes—to the Phragmoplastophyta. The Zygnematophyceae is the closest algal sister lineage to land plants,1 but it has the least complex body plans among phragmoplastophytic streptophyte algae. One explanation could be that the zygnematophyte body complexity is ancestrally reduced.2,3 By stark contrast, within the streptophyte algal class Coleochaetophyceae, thalli are composed of branching filaments with apical cell division, and some Coleochaete species have elaborate discoid thalli, in some cases including marginal meristems. In our new phylogenomic framework for Coleochaetophyceae, we find that all Coleochaete species with complex bodies formed by perpendicular cell division are merely a 66.5 ± 17.8-Ma-old group. Such complex thalli are formed by both periclinal and anticlinal cell divisions, which also underpin the morphological complexity of land plants. Our data underscore the versatility that leads to complex streptophyte bodies and bolster the concept that an ancient morphogenetic toolkit was actualized multiple times independently throughout streptophyte evolution.