A phylogenomically informed five-order system for the closest relatives of land plants

The evolution of streptophytes had a profound impact on life on Earth. They brought forth those photosyn-thetic eukaryotes that today dominate the macroscopic flora: the land plants (Embryophyta).1 There is convincing evidence that the unicellular/filamentous Zygnematophyceae-and not the morphologically more elaborate Coleochaetophyceae or Charophyceae-are the closest algal relatives of land plants.2-6 Despite the species richness (>4,000), wide distribution, and key evolutionary position of the zygnemato-phytes, their internal phylogeny remains largely unresolved.7,8 There are also putative zygnematophytes with interesting body plan modifications (e.g., filamentous growth) whose phylogenetic affiliations remain un-known. Here, we studied a filamentous green alga (strain MZCH580) from an Austrian peat bog with central or parietal chloroplasts that lack discernible pyrenoids. It represents Mougeotiopsis calospora PALLA, an enig-matic alga that was described more than 120 years ago9 but never subjected to molecular analyses. We generated transcriptomic data of M. calospora strain MZCH580 and conducted comprehensive phyloge-nomic analyses (326 nuclear loci) for 46 taxonomically diverse zygnematophytes. Strain MZCH580 falls in a deep-branching zygnematophycean clade together with some unicellular species and thus represents a formerly unknown zygnematophycean lineage with filamentous growth. Our well-supported phylogenomic tree lets us propose a new five-order system for the Zygnematophyceae and provides evidence for at least five independent origins of true filamentous growth in the closest algal relatives of land plants. This phylogeny provides a robust and comprehensive framework for performing comparative analyses and inferring the evo-lution of cellular traits and body plans in the closest relatives of land plants.

Automated summary

The evolution of streptophytes has had a significant impact on life on Earth, particularly in the emergence of land plants. Recent research on a filamentous green alga from an Austrian peat bog reveals a previously unknown lineage of zygnematophytes with filamentous growth, shedding light on the evolutionary relationships and origins of this group. The findings provide a solid framework for further comparative analyses and understanding the evolution of cellular traits and body plans in the closest relatives of land plants.