Drought and salinity stress remodel Asian rice (Oryza sativa) leaf development through cell-type-specific regulatory programs.
Osmotic stressors impair tissue expansion and slow crop development, which can ultimately reduce yield. The mechanisms through which dividing and differentiating cells perceive, integrate, and respond to stress are not well understood. To explore this knowledge gap, we assessed Asian rice (Oryza sativa) seedling responses to drought and salinity stress by performing single-nucleus transcriptome analyses on developing leaves and by assaying ion distribution using ICP-MS and CoroNa Green staining. With a dataset of > 125 000 high-quality nuclei, we identified transcriptome signatures of developmental trajectories for each of the major tissue systems, from their origin as dividing cells in the shoot apical meristem to mature cells in epidermal, mesophyll, and vascular tissues. We explored the extensive heterogeneity between cell types with respect to their responses to stress by developing an ensemble-based Perturbation Index and a tool for visualizing pseudobulk expression data and characterizing regulatory modules for different stress responses. Transcriptionally, moderate stress perturbs cells early in development and induces regulatory networks that inhibit cell division, whereas mild stressors primarily disrupt gene expression in differentiated tissues. Overall, these results indicate that leaf development occurring in salt and drought stress conditions is the product of a complex interplay of developmental, environmental, and cell-type contexts.