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Summary: Development in higher organisms requires proper gene silencing, partially achieved through trimethylation of lysine 27 on histone H3 (H3K27me3). However, how the normal distribution of this modification is established and maintained and how it affects gene expression remains unclear, especially in fungi. Polycomb repressive complex 2 (PRC2) catalyses H3K27me3 to assemble transcriptionally repressed facultative heterochromatin and is crucial in animals, plants, and fungi.Here, we report on the critical role of an additional PRC2 subunit in the normal distribution of H3K27me3 occupancy and the stable maintenance of gene repression in the rice fungal pathogen Magnaporthe oryzae. P55, identified as an additional PRC2 subunit, is physically associated with core subunits of PRC2 and is required for a complete level of H3K27me3 modification.Loss of P55 caused severe global defects in the normal distribution of H3K27me3 and transcriptional reprogramming on the H3K27me3‐occupied genes. Furthermore, we found that the Sin3 histone deacetylase complex was required to sustain H3K27me3 occupancy and stably maintain gene repression by directly interacting with P55.Our results revealed a novel mechanism by which P55 and Sin3 participate in the normal distribution of facultative heterochromatic modifications and the stable maintenance of gene repression in eukaryotes. [ABSTRACT FROM AUTHOR]