SWI3 regulates male sex determination in Marchantia polymorpha

Abstract

Land plants alternate between multicellular haploid and diploid phases, a life cycle requiring tight coordination between vegetative growth and sexual reproduction. Chromatin regulators such as SWI3, a core subunit of the SWI/SNF complex, are ancestral and highly diversified in angiosperms. As their functions outside of angiosperms remain unclear, we investigated SWI3 of the liverwort Marchantia polymorpha, a non-vascular dioecious land plant. A mutation in the promoter of MpSWI3 affected gametangiophore development and spermiogenesis in males, revealing its male-specific role in reproductive development. The MpSWI3 mutant line amplifies vegetative propagation in males under conditions that would normally induce reproductive growth. The phenotype was underpinned by transcriptomic changes, showing that MpSWI3 modulates key regulators of gametangiophore initiation (e.g. BONOBO, GLID), sperm development and motility (e.g. DUO1, PKAR), and asexual reproduction (e.g. KAI2). Together, this positions MpSWI3 as a chromatin-level regulator balancing vegetative and reproductive phases, highlighting an ancient epigenetic function that coordinates developmental phase transitions in land plants.