With the increased availability of high-resolution sequence information, genome-wide association (GWA) studies have become feasible in a number of species. The vast majority of these studies are conducted in human populations, where it is difficult to provide strong evidence for the functional involvement of unknown genes that are identified using GWA. Here we used the model organism Arabidopsis thaliana to combine high-throughput confocal microscopy imaging of traits at the cellular level, GWA and expression analyses to identify genomic regions that are associated with developmental cell-type traits. We identify and characterize a new F-box gene, KUK, that regulates meristem and cell length. We further show that polymorphisms in the coding sequence are the major causes of KUK allele-dependent natural variation in root development. This work demonstrates the feasibility of GWA using cellular traits to identify causal genes for basic biological processes such as development.