Seminars

In an indeterminate shoot apical meristem, stem cells persist for the life of the plant. In contrast, in a determinate floral meristem, a fixed number of organs are produced before the meristem is terminated. In Arabidopsis, the floral stem cell identity is sustained by expression of the homeo-domain transcription factor WUSCHEL (WUS). Expression of WUS is terminated by multiple genetic pathways, including the zinc finger protein KNUCKLES (KNU), with the result that stem cell identity is inactivated. KNU expression is induced by the floral homeotic protein AGAMOUS (AG). The induction process requires approximately two days and entails the dynamic changes of the repressive histone modification H3K27me3 at the KNU locus. The precise temporal induction of KNU is essential for the coordinated growth and differentiation of floral stem cells, but the mechanism that control this timing has remained unclear. Here we present an epigenetic mechanism in which the floral homeotic protein AG induces KNU at approximately two days of delay. AG binding sites colocalize with a Polycomb Response Element in the KNU upstream region. AG binding to the KNU promoter causes the eviction of the Polycomb group proteins (PcG) from the locus, leading to cell division-dependent loss of the repressive status. We reconstituted an epigenetic-based synthetic circuit in cell lines that shows similar delayed-induction. These analyses demonstrate that floral stem cells measure developmental timing by a division-dependent epigenetic timer triggered by PcG eviction. We also discuss how KNU represses WUS expression through epigenetic regulation and our current approach to reveal molecular details of recruitment and modification of PcG activity in floral meristems.