An epigenetic timer regulates the transition from cell division to cell expansion during Arabidopsis petal organogenesis

A number of studies have demonstrated that epigenetic factors regulate plant developmental timing in response to environmental changes. However, we still have an incomplete view of how epigenetic factors can regulate developmental events such as organogenesis, and the transition from cell division to cell expansion, in plants. The small number of cell types and the relatively simple developmental progression required to form the Arabidopsis petal makes it a good model to investigate the molecular mechanisms driving plant organogenesis. In this study, we investigated how the RABBIT EARS (RBE) transcriptional repressor maintains the downregulation of its downstream direct target, TCP5, long after RBE expression dissipates. We showed that RBE recruits the Groucho/Tup1-like corepressor TOPLESS (TPL) to repress TCP5 transcription in petal primordia. This process involves multiple layers of changes such as remodeling of chromatin accessibility, alteration of RNA polymerase activity, and histone modifications, resulting in an epigenetic memory that is maintained through multiple cell divisions. This memory functions to maintain cell divisions during the early phase of petal development, and its attenuation in a cell division-dependent fashion later in development enables the transition from cell division to cell expansion. Overall, this study unveils a novel mechanism by which the memory of an epigenetic state, and its cell-cycle regulated decay, acts as a timer to precisely control organogenesis. Epigenetic changes, such as histone modifications or DNA methylation, can modify gene expression without affecting the genetic code. Such alterations can persist for many cell generations, and often are induced by various environmental inputs in both plants and animals. By contrast, little is known of how intrinsic epigenetic changes can act to regulate the temporal progression of development. Here we showed that the expression of RABBIT EARS (RBE) represses the transcription of its target, TCP5, through inducing a variety of epigenetic changes at the TCP5 locus. These changes dissipated over a period of days, allowing for eventual activation of TCP5 expression and a concomitant shift from cell division to cell expansion during Arabidopsis petal development. The gradual loss of repressive epigenetic marks at the TCP5 locus represents an internal timing mechanism to temporally control the development of the Arabidopsis petal.