Single-cell resolution of lineage trajectories in the Arabidopsis stomatal lineage and developing leaf

Dynamic cell identities underlie flexible developmental programs. The stomatal lineage in the Arabidopsis leaf epidermis features asynchronous and indeterminate divisions that can be modulated by environmental cues. The products of the lineage, stomatal guard cells and pavement cells, regulate plant-atmosphere exchanges, and the epidermis as a whole influences overall leaf growth. How flexibility is encoded in development of the stomatal lineage and how cell fates are coordinated in the leaf are open questions. Here, by leveraging single-cell transcriptomics and molecular genetics, we uncovered models of cell differentiation within Arabidopsis leaf tissue. Profiles across leaf tissues identified points of regulatory congruence. In the stomatal lineage, single-cell resolution resolved underlying cell heterogeneity within early stages and provided a fine-grained profile of guard cell differentiation. Through integration of genome-scale datasets and spatiotemporally precise functional manipulations, we also identified an extended role for the transcriptional regulator SPEECHLESS in reinforcing cell fate commitment. [Display omitted] •Distinct models of cell differentiation and lineage trajectories define leaf tissue•Cell-cycle regulators exhibit distinct, yet overlapping, expression profiles•Flexible stomatal lineage cell states exist along a continuum•Single-cell resolution refines cell fate commitment decisions that yield stomata How do cells build developmentally flexible organs? Lopez-Anido et al. employed single-cell transcriptomics to uncover distinct models of cell differentiation within Arabidopsis leaf tissue. Along with revealing dynamics of cellular programs, they identified underlying cell heterogeneity within the epidermal lineage and interrogated new roles for a core transcriptional regulator.