As the shoot apex produces most of the cells that comprise the aerial part of the plant, a perfect orchestration between the cell division rates and fate specification is thought to be essential for normal organ formation and plant development. However, the interdependence between the cell cycle machinery and meristem-organizing genes is still poorly understood. To investigate this mechanism, we specifically inhibited the cell cycle machinery in the shoot apex by the expression of a dominant negative allele of the A-type cyclin-dependent kinase (CDK) CDKA;1 in meristematic cells. A decrease in the cell division rate within the SHOOTMERISTEMLESS domain of the shoot apex affected dramatically plant growth and development. Within the meristem, a subset of cells was pushed into the differentiation pathway, as visualized by premature cell expansion and endoreduplication onset. Although in most plants the meristem structure and expression patterns of the meristem identity genes were maintained, in a certain number of plants, the reduced CDK activity caused splitting of the meristem. This phenotype correlated with the dominant negative CDKA;1 expression level. Therefore, we propose a threshold model in which the impact of the cell cycle machinery on the meristem organization is determined by the level of CDK activity.