Different plant species within the grasses were parallel targets of domestication, giving rise to crops with distinct evolutionary histories and traits. Key traits that distinguish these species are mediated by specialized cell types within organs. Here, we compare the transcriptomes of all cells within roots in three grasses—Zea mays (maize), Sorghum bicolor (sorghum), and outgroup Setaria viridis (Setaria). We first show that single-cell and single-nucleus RNA-seq provide complementary readouts of cell identity, warranting a combined analysis. Comparative cellular analysis shows that the transcriptomes of some cell types diverged more rapidly than others, in part by recruiting gene modules from other cell types. Furthermore, examining the whole genome duplication in maize, we detect extensive dosage compensation in surviving co-expressed homeologs, reinforcing genomic balance1. Homeolog pairs that underwent subfunctionalization2, partitioning their expression among cell types, represented a minor pattern but showed the highest rate of acquiring a novel (non-ancestral) domain. These results fit a conjecture in which mechanisms that maintain stoichiometric balance at the molecular level aid in homeolog retention for extended periods to allow new functions to arise. An unexpected synergy between spatial sub- and neo-functionalization then contributes to changes in transcriptional cell identity.