Phylogenomic Reconstruction and Functional Divergence of the PARP Gene Family Illuminate Its Role in Plant Terrestrialization

The evolution of robust DNA repair mechanisms was a prerequisite for the conquest of land by plants, a transition that exposed them to harsh new environmental stressors. The poly (ADP-ribose) polymerase (PARP) family is central to this adaptation, as it orchestrates DNA repair and stress signaling pathways essential for coping with the elevated UV radiation and desiccation of terrestrial environments. Yet its early evolutionary origins are unknown. Here, we present a comprehensive reconstruction of the PARP family's history across the plant kingdom. Our phylogenomic analysis reveals that <i>PARP</i> evolution ignited during the bryophyte radiation, expanding from a single ancestral algal gene into three distinct subfamilies (<i>PARP1</i>, <i>PARP2</i>, and <i>PARP3</i>). This diversification was driven by structural innovations in DNA-binding domains and a rewiring of transcriptional networks to respond to terrestrial challenges. We provide direct experimental support for this hypothesis through functional analysis of PARPs from the extremotolerant moss <i>Syntrichia caninervis</i>. We show that its PARP proteins provide multifaceted protection against UV radiation, heat, and genotoxic agents, and that recently duplicated <i>PARP2</i> genes are already diverging in function. Our work pinpoints the molecular adaptations in a key DNA repair family that enabled the greening of Earth and uncovers novel genetic targets for enhancing crop resilience.