Adaptive evolutionary shifts in de novo birth and fixation strategy of lineage‐specific genes during plant terrestrialization

As a type of new genes, lineage-specific genes (LSGs) play crucial roles in many aspects of organism development. Although the origin mechanisms of LSGs have been sporadically reported, previous studies have focused on limited lineages, and the global landscape of Archaeplastida-specific genes origin remains unclear. In this study, we systematically analyzed the number, functional profiles, origin mechanisms, and evolutionary trajectories of LSGs originated from ancestral nodes in Archaeplastida. Our study revealed 14 episodes of LSGs originated from ancestral nodes at the order level. The episodes of LSGs from the ancestor of Zygnematophyceae and Embryophyta (land plants) and the ancestor of land plants promoted plant terrestrialization, particularly through cell wall remodeling. Regarding origin mechanisms, we found that de novo-originated LSGs in algae (i.e., rhodophytes, glaucophytes, chlorophytes, streptophyte algae) were derived from preadapted non-coding sequences. In contrast, de novo birth in land plants adopts the continuum model. Following their emergence, LSGs fixation in algae was mainly facilitated by elevated expression level, whereas gene duplication served as the key driver for LSGs fixation in land plants. Our findings demonstrate a comprehensive landscape of LSGs evolution in Archaeplastida and reveal adaptive shifts of de novo birth during plant terrestrialization.