AGAMOUS regulates various target genes via cell cycle-coupled H3K27me3 dilution in floral meristems and stamens

Cell cycle-coupled H3K27me3 dilution at various target loci regulates floral development. The MADS domain transcription factor AGAMOUS (AG) regulates floral meristem termination by preventing maintenance of the histone modification lysine 27 of histone H3 (H3K27me3) along the KNUCKLES (KNU) coding sequence. At 2 d after AG binding, cell division has diluted the repressive mark H3K27me3, allowing activation of KNU transcription prior to floral meristem termination. However, how many other downstream genes are temporally regulated by this intrinsic epigenetic timer and what their functions are remain unknown. Here, we identify direct AG targets regulated through cell cycle-coupled H3K27me3 dilution in Arabidopsis thaliana. Expression of the targets KNU, AT HOOK MOTIF NUCLEAR LOCALIZED PROTEIN18 (AHL18), and PLATZ10 occurred later in plants with longer H3K27me3-marked regions. We established a mathematical model to predict timing of gene expression and manipulated temporal gene expression using the H3K27me3-marked del region from the KNU coding sequence. Increasing the number of del copies delayed and reduced KNU expression in a polycomb repressive complex 2- and cell cycle-dependent manner. Furthermore, AHL18 was specifically expressed in stamens and caused developmental defects when misexpressed. Finally, AHL18 bound to genes important for stamen growth. Our results suggest that AG controls the timing of expression of various target genes via cell cycle-coupled dilution of H3K27me3 for proper floral meristem termination and stamen development.

Automated summary

Cell cycle-coupled H3K27me3 dilution regulates floral development by controlling the expression timing of various target genes. The transcription factor AG prevents maintenance of H3K27me3 along the KNU coding sequence, allowing activation of KNU transcription prior to floral meristem termination. AHL18, a downstream target of AG, is specifically expressed in stamens and involved in stamen growth. Our findings highlight the importance of cell cycle-coupled H3K27me3 dilution in floral development and provide insights into the regulatory mechanisms.