Time Series Single-Cell Transcriptional Atlases Reveal Cell Fate Differentiation Driven by Light in Arabidopsis Seedlings

Abstract

Abstract Light serves as the energy source as well as a signal for plant growth and development during their whole life cycle. Seedling de-etiolation is the most dramatic manifestation of light-regulated plant development processes, as massive reprogramming of the plant transcriptome occurs. Although there were organ-specific development and genome expression studies reported, there still lack a systematic analysis of cell type specific differentiation and the associated genome transcriptional regulation. Here, we obtained single-cell transcriptional atlases for etiolated, de-etiolating and light-grown Arabidopsis (Arabidopsis thaliana) whole seedlings. These atlases comprised 31,796 and 61,065 informative cells from shoot and root tissues, respectively, that were clustered and annotated as 48 different cell types. Although key transcription factors underlying photomorphogenesis such as HY5/HYH and PIF1,5 were found to be universally induced by light in all the evaluated cell types, one-third (12,447) of all the genes showed preferential spatiotemporal expression during de-etiolation. Different development occurred in respective cell types in pifq mutants, leading to photomorphogensis-like epidermal cells and skotomorphogenesis-like mesophyll cells. With the determination of comprehensive developmental trajectories, light modulation of cell fate differentiation during hook opening, guard cell specialization, and vasculature development have been demonstrated. A series of cell type-specific developmental factors modulated by light were identified, revealing strikingly different light-induced switches in their respective cell types. Our results provide information concerning the light signaling networks at the cell-type resolution, improving our understanding of how light regulates plant development at the cell-type and genome-wide levels. The learned information could serve as a valuable resource for comprehensively investigating molecular mechanism of cell development and differentiation in response to light.