A Molecular Switch for Initiating Cell Differentiation in Arabidopsis

Abstract

The onset of differentiation entails modifying the gene expression state of cells, to allow activation of developmental programs that are maintained repressed in the undifferentiated precursor cells [1, 2]. This requires a mechanism to change gene expression on a genome-scale. Recent evidence suggests that in mammalian stem cells, derepression of developmental regulators during differentiation involves a shift from stalled to productive elongation of their transcripts [3-5], but factors mediating this shift have not been identified and the evidence remains correlative. We report the identification of the MINIYO (IYO) gene, a positive regulator of transcriptional elongation that is essential for cells to initiate differentiation in Arabidopsis. IYO interacts with RNA polymerase II and the Elongator complex and is required to sustain global levels of transcriptional elongation activity, specifically in differentiating tissues. Accordingly, IYO is expressed in embryos, meristems, and organ primordia and not in mature tissues. Moreover, differential subcellular protein distribution further refines the domain of IYO function by directing nuclear accumulation, and thus its transcriptional activity, to cells initiating differentiation. Importantly, IYO overexpression induces premature cell differentiation and leads to meristem termination phenotypes. These findings identify IYO as a necessary and sufficient factor for initiating differentiation in Arabidopsis and suggest that the targeted nuclear accumulation of IYO functions as a transcriptional switch for this fate transition.