The ASHR3 SET-domain Protein Controls Cell Division Competence of the Meristem and Quiescent Centre of the Arabidopsis thaliana Primary Root

The stem cell niche (SCN) of the Arabidopsis thaliana primary root apical meristem is composed of the quiescent (or organising) centre (QC) surrounded by stem (initial) cells for the different tissues. Initial cells generate a population of transit amplifying cells that undergo a limited number of cell divisions before elongating and differentiating. It is unclear whether these divisions occur stochastically or in an orderly manner. Using the thymidine analogue EdU to monitor DNA replication of cells of Arabidopsis root meristems we identified a pattern of two, four and eight neighbouring cells with synchronized replication along the cortical, epidermal and endodermal cell files, suggested to be daughters, granddaughters and great-granddaughters of the direct progeny of each stem cell. Markers of mitosis and cytokinesis were not present in the region closest to the transition zone where the cells start to elongate, suggesting that great-granddaughter cells switch synchronously from the mitotic cell cycle to endoreduplication. Mutations in the SCN-expressed ASH1 RELATED3 (ASHR3) gene, encoding a SET-domain protein conferring histone H3 lysine 36 methylation, disrupted this pattern of co-ordinated DNA replication and cell division, and increased the cell division rate in the QC. E2Fa/E2Fb transcription factors controlling the G1-to-S phase transition regulate ASHR3 expression and bind to the ASHR3 promoter, substantiating a role for ASHR3 in cell division control. Reduced length of the root apical meristem and primary root of the mutant ashr3-1 indicate that synchronization of replication and cell divisions is required for normal root growth and development.