Variable Cell Growth Yields Reproducible Organ Development through Spatiotemporal Averaging

Organ sizes and shapes are strikingly reproducible, despite the variable growth and division of individual cells within them. To reveal which mechanisms enable this precision, we designed a screen for disrupted sepal size and shape uniformity in Arabidopsis and identified mutations in the mitochondrial i-AAA protease FtsH4. Counterintuitively, through live imaging we observed that variability of neighboring cell growth was reduced in ftsh4 sepals. We found that regular organ shape results from spatiotemporal averaging of the cellular variability in wild-type sepals, which is disrupted in the less-variable cells of ftsh4 mutants. We also found that abnormal, increased accumulation of reactive oxygen species (ROS) in ftsh4 mutants disrupts organ size consistency. In wild-type sepals, ROS accumulate in maturing cells and limit organ growth, suggesting that ROS are endogenous signals promoting termination of growth. Our results demonstrate that spatiotemporal averaging of cellular variability is required for precision in organ size. [Display omitted] •Reduced cellular variability can lead to the formation of irregular organs•Spatiotemporal averaging of noisy cellular growth produces uniform organs•Reactive oxygen species (ROS) promote maturation of sepals•Abnormal ROS accumulation hinders the averaging of noisy cellular growth During development, organs form with reproducible sizes and shapes despite the variable and unpredictable growth of their cells. Through live imaging and computational modeling of Arabidopsis sepals, Hong et al. show that spatiotemporal averaging of cellular variability resolves this apparent contradiction. Reactive oxygen species inhibit spatiotemporal averaging and promote organ maturation.