PRC1-mediated H2A.Zub promotes gene expression by preventing H3.1K27me1 incorporation in Arabidopsis

PcG complexes are pivotal in orchestrating the transition from embryonic to vegetative development in plants. However, the mechanisms underlying the gene expression reprogramming that takes place during this developmental transition are still not fully understood. Several studies suggest that incorporating PcG modifications into distinct histone variants may play a key role in this process. However, while PRC2-mediated H3K27me3 is essential for gene repression, the timing of PRC2 action on canonical H3.1 or variant H3.3 remains unclear. Furthermore, the exact role of PRC1 in transcriptional regulation is still unresolved, partly owing to limited knowledge of the conditions under which this complex monoubiquitinates canonical H2A or H2A.Z variant.

Here, we demonstrate that H2A.Z undergoes monoubiquitination during the seed-to-seedling transition. H2A.Zub facilitates the recruitment of PRC2 to mediate H3.3 trimethylation, repressing seed-specific genes; however, H2A.Zub also promotes the activation of vegetative-specific genes by preventing H3K27me1 incorporation into H3.1. Notably, the histone demethylase REF6 initiates this process by removing two methyl groups from stably repressed H3.1K27me3-marked genes, enabling the subsequent H2A.Zub incorporation. This result suggests that REF6 activity is a critical early step in PRC1-mediated transcriptional activation.

Our findings reveal the long-sought mechanism by which PRC1 participates in transcriptional activation. We demonstrate that PRC1-mediated H2A.Zub, acting as a "switcher", plays a pivotal role in reprogramming active and repressed genes during the transition from embryonic to vegetative development. Moreover, our results provide new insights into the intricate relationship between histone modifications and histone variants in reprogramming and maintaining gene expression patterns.