Active Control of Cell Size Generates Spatial Detail during Plant Organogenesis

Abstract

SummaryHow cells regulate their dimensions is a long-standing question [1, 2]. In fission and budding yeast, cell-cycle progression depends on cell size, although it is still unclear how size is assessed [3, 4, 5]. In animals, it has been suggested that cell size is modulated primarily by the balance of external signals controlling growth and the cell cycle [1], although there is evidence of cell-autonomous control in cell cultures [6, 7, 8, 9]. Regardless of whether regulation is external or cell autonomous, the role of cell-size control in the development of multicellular organisms remains unclear. Plants are a convenient system to study this question: the shoot meristem, which continuously provides new cells to form new organs, maintains a population of actively dividing and characteristically small cells for extended periods [10]. Here, we used live imaging and quantitative, 4D image analysis to measure the sources of cell-size variability in the meristem and then used these measurements in computer simulations to show that the uniform cell sizes seen in the meristem likely require coordinated control of cell growth and cell cycle in individual cells. A genetically induced transient increase in cell size was quickly corrected by more frequent cell division, showing that the cell cycle was adjusted to maintain cell-size homeostasis. Genetically altered cell sizes had little effect on tissue growth but perturbed the establishment of organ boundaries and the emergence of organ primordia. We conclude that meristem cells actively control their sizes to achieve the resolution required to pattern small-scale structures.