A deep genetic structure phylogenomically frames the closest algal relatives of land plants

Abstract

To discern the nature of the closest streptophyte algal relatives of land plants (embryophytes) is a major question in the field of plant evolutionary biology; discerning that nature is essential for our ability to infer the last common ancestor of embryophytes and algae, allowing to retrace the adaptations that ushered in the conquest of land by plants. Albeit initially coming as a surprise, all major phylogenomic efforts have concluded that the Zygnematophyceae are the algal sisters to land plants1-6. The Zygnematophyceae are the streptophyte algal class with the greatest species richness7 and while we now have ample genome information on a few select members of zygnematophytes8-13, our understanding of the genetic and genomic divergence as well as potential is limited by a lack of phylodiverse data that accounts for this diversity and integrates it into a phylogenomic framework. We here sequenced 43 new transcriptome datasets for the Zygnematophyceae and built a phylogenomic tree based on a total of 104 zygnematophyceaen transcriptomes and 2243 loci. We recover a deep genetic structure for the Zygnematophyceae, revealing that this algal class is ancient. Despite the deep split between Spirogyrales and their unicellular sister group Desmidiales, most Spirogyrales emerged after pronounced genetic divergence, accommodating the attainment of multicellularity and divergent traits such as unique cell and plastid division13. Overall, our data capture signatures of massive ancient radiations. Zygnematophyceae are characterized by deep genetic divergences that necessitated a phylodiverse sampling to be revealed, together with their vast evolutionary history, and to illuminate the nature of the algal progenitors of land plants.