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

## TL;DR

This study shows that removing a specific histone, H1.1, before meiosis is crucial for plant reproduction in Arabidopsis.

## Contribution

The study identifies two pathways and key residues involved in H1.1 degradation during plant germline development.

## Key findings

- Two pathways involving AIH citrullinase and CULLIN4 E3 ubiquitin ligase regulate H1.1 depletion in female SMCs.
- Residues R57 and K89 in H1.1 affect its chromatin stability and degradation.
- Pre-meiotic H1.1 depletion is necessary for female gametogenesis but not for meiosis itself.

## Abstract

Despite being evolutionary distant, plants and animals exhibit a shared phenomenon during the transition from somatic-to-reproductive cell fate marked by extensive structural and compositional changes in chromatin. This 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 SMCs 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 that a citrullination–ubiquitination pathway governs pre-meiotic H1 depletion as a critical mechanism for establishing post-meiotic competence in the Arabidopsis germline.

Linker histones (H1) loss is essential to establish pluripotency in animal primordial germ cells, but its role is unknown in plants. This study uncovers the roles and mechanisms of linker histone depletion at the onset of germline development in Arabidopsis. A citrullination–ubiquitination pathway emerges as a key mechanism establishing reproductive competence in the female plant germline.

Two regulatory pathways involving the AIH citrulinase and CULLIN4 E3 Ubiquitin ligase control H1.1 depletion in female Spore Mother Cells (SMCs).The conserved residues R57 and K89 in H1.1 modulate its chromatin stability and degradation likely via charge neutralization and ubiquitination, respectively.Loss of H1.1 depletion alters heterochromatin organization and SMC growth but does not impair meiosis.Pre-meiotic depletion of H1.1 is necessary for female gametogenesis.

Two regulatory pathways involving the AIH citrulinase and CULLIN4 E3 Ubiquitin ligase control H1.1 depletion in female Spore Mother Cells (SMCs).

The conserved residues R57 and K89 in H1.1 modulate its chromatin stability and degradation likely via charge neutralization and ubiquitination, respectively.

Loss of H1.1 depletion alters heterochromatin organization and SMC growth but does not impair meiosis.

Pre-meiotic depletion of H1.1 is necessary for female gametogenesis.

H1.1 removal in Arabidopsis female Spore Mother Cells is regulated by two pathways involving a citrullinase and an E3-ubiquitin ligase.