Pre-meiotic H1.1 degradation is essential for Arabidopsis gametogenesis

Despite being evolutionary distant, plants and animals share a common phenomenon at the somatic-to-reproductive cell fate transition with extensive structural and compositional changes in chromatin. Such chromatin reprogramming occurs in the plant SMCs (Spore Mother Cells) and animal PGCs (primordial germ cells) and is initiated by the loss of linker histones (H1). H1 loss is essential to establish pluripotency in animal PGCs but its role is not known in plants. Here, we identified two regulatory pathways involving a citrullinase and an E3-ubiquitin ligase that contribute H1.1 loss in female SMC in Arabidopsis. We also identified roles for two specific residues: an arginine, whose positive charge contributes to H1.1 destabilization from chromatin, and a lysine in the globular domain that is essential for H1.1 degradation. Ovules with impaired H1.1 loss in the SMC proceed through sporogenesis but fail to complete gametogenesis. We propose a citrullination-ubiquitination pathway governing pre-meiotic H1 depletion as a critical mechanism for establishing post-meiotic competence in the Arabidopsis germline.