New Zygnematophycean chloroplast genomes provide further support for the sister relationship of land plants and conjugating algae

Colonization of the land by plants was one of the crucial steps in the ecological history of the biosphere. It is well established that all land plants (LP; embryophytes) are of monophyletic origin, hence reconstructing the genetic complement and structure of the ancestral LP chloroplast is great importance for the study of the genetic and physiological changes that accompanied the transition from an aquatic to terrestrial environment. However, the identification of an extant LP sister group among charophytic algae has not been unequivocal, despite extensive efforts. The intuitive choice of Charales, which was supported as the LP sister group by morphological and early biomolecular data, now appears incorrect as growing phylogenetic evidence places LP closer to conjugating algae (Zygnematales).Here we present three newly reconstucted Zygnematophycean cp genomes – Mesotaenium endlicherianum, Roya anglica and Gonatozygon brebissonii, and we demonstrate that our understanding of the Zygnematophycean cp structure has been partially misled by coincidental features of the previously sequenced Zygnema and Staurastrum. Among the three new cp genomes, we identify a quadripartite architecture, as well as genes, ORFs, and intron-sets that are exclusively found in the LP. Phylogenetic analyses indicate that the Zynematales are monophyletic and the sister group to LP, and also that both bryophytes and tracheophytes are monophyletic groups. The expanded set of Zygnematophycean cp genomes demonstrates that the ancestor of this morphologically diverse and taxonomically rich group of streptophytic algae possessed a cp genome both structurally and genetically similar to the chloroplasts of early land plants.