Land Plant Terrestrialization and What We Can Learn from Chara

All land plants share one algal ancestor. Phylogenomics tell us that Zygnematophyceae represent the closest algal relatives to land plants and their genomes carry key information on why plants succeeded on land. Two issues complicate the matter: (i) Zygnematophyceae have experienced reductive evolution and (ii) mosaic evolution has scattered the exaptations that are thought to have favoured streptophyte terrestrialization across higher streptophyte algae (namely the Zygnematophyceae, Coleochaetophyceae and Charophyceae). A comparative and complementing approach is hence pivotal to understanding the genetic suite that favoured streptophyte terrestrialization. To provide insight into the morphologically complex Charophyceae, we sequenced the genome of Chara braunii. We obtained 1.75 Gb of scaffolded sequence data, corresponding to ~90% of the genome. 36,877 protein-coding genes were predicted, among which we found numerous land plant signature genes. These genes include key plant transcription factors such as all four HD-ZIP classes and a battery of phytohormone signalling components. Intriguingly, in some aspects Chara braunii’s suite of land plant signature genes equalled that of the basal land plant Physcomitrella (e.g., in the case of plastid-nucleus retrograde signalling proteins) or even surpassed it (e.g., ARP-type MYB transcription factors). Our data redefine the list of embryophyte-specific genes and highlight their origin within the trajectory of streptophyte algal evolution. The more comprehensive our picture of streptophyte algal genomes becomes, the closer we are to reassembling the scattered catalogue of genes that allowed one to settle on land and evolve the embryophyte diversity that we witness today.