The Origin of Land Plants Is Rooted in Two Bursts of Genomic Novelty

Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move from water to land and the origins of vascular tissues, seeds, and flowers [1]. These have resulted in the evolution of terrestrial flora that has shaped modern ecosystems and the diversification of the Plant Kingdom, Viridiplantae, into over 374,000 described species [2]. Each of these transitions was accompanied by the gain and loss of genes in plant genomes. For example, whole-genome duplications are known to be fundamental to the origins of both seed and flowering plants [3, 4]. With the ever-increasing quality and quantity of whole-genome data, evolutionary insight into origins of distinct plant groups using comparative genomic techniques is now feasible. Here, using an evolutionary genomics pipeline to compare 208 complete genomes, we analyze the gene content of the ancestral genomes of the last common ancestor of land plants and all other major groups of plant. This approach reveals an unprecedented level of fundamental genomic novelties in two nodes related to the origin of land plants: the first in the origin of streptophytes during the Ediacaran and another in the ancestor of land plants in the Ordovician. Our findings highlight the biological processes that evolved with the origin of land plants and emphasize the importance of conserved gene novelties in plant diversification. Comparisons to other eukaryotic studies suggest a separation of the genomic origins of multicellularity and terrestrialization in plants. [Display omitted] •Comparing 208 genomes gives insight into the role of gene novelty in plant evolution•Two bursts of genomic novelty played a major role in the evolution of land plants•Functions linked to these novelties are multicellularity and terrestrialization•The backbone of hormone signaling either predates or accompanies this transition Bowles et al. show that two consecutive bursts of genomic novelty predate the origin of land plants. Identifying these events provides insights into the evolution of flora that has defined modern ecosystems.