AbstractThe female germline of flowering plants develops within a niche of somatic ovule cells, also referred to as the nucellus. How niche cells maintain their own somatic developmental program, yet support the development of adjoining germline cells, remains largely unknown. Here we report that MADS31, a conserved MADS-box transcription factor from the B-sister subclass, is a potent regulator of niche cell identity in barley. MADS31 is preferentially expressed in nucellar cells directly adjoining the germline, and loss-of-functionmads31mutants exhibit deformed and disorganized nucellar cells, leading to impaired germline development and partial female sterility. Molecular assays indicate that MADS31 encodes a potent transcriptional repressor, repressing genes in the ovule that are normally active in the seed. One prominent target of MADS31 isNRPD4b, a seed-expressed component of RNA polymerase IV/V that is involved in gene silencing via RNA directed DNA methylation.NRPD4bis directly repressed by MADS31in vivoand is de-repressed inmads31ovules, while overexpression ofNRPD4brecapitulates themads31ovule phenotype. This coincides with specific changes in histone methylation and is consistent withNRPD4bbeing directly repressed by MADS31 to maintain ovule niche functionality. Our findings reveal a new mechanism by which somatic ovule tissues maintain their own identity before transitioning to the post-fertilization program.