Stomatal setpoints and environmental responsiveness are sculpted by developmental trajectories

Abstract

Efficient gas and water exchange between plants and their environment largely depends on the number and distribution of stomata, cellular valves in leaf epidermis. Core genetic regulators of stomatal cell identity and pattern along with asymmetric stem-cell like divisions in stomatal precursors are hypothesized to customize stomatal production for optimal leaf performance. How these regulators work in concert and how division dynamics are modified and adjusted in different environments, however, are poorly understood. Here, we leveraged the variation in stomatal patterning in Arabidopsis thaliana accessions from diverse environments to define developmental rules and constraints in the stomatal lineage. The accessions subtle and quantitative variation enables us to identify which cellular parameters are flexible, revealing how developmental plasticity generates phenotypic plasticity. By developing live-cell imaging tools to track cellular behaviors during leaf growth under varying environmental conditions in these accessions, we could decompose stomatal density variation into its developmental origins. Variation in final stomatal numbers is driven by differences in the relative contributions of stomatal initiation, cell size-based fate thresholds, general proliferative capacity, and coordination between sister and neighbor cell behaviors. Overall, diverse accessions converge toward two lineage regimes: one dominated by autonomous decisions with loose cell-cell coordination, the other by extensive cell-cell coordination. Challenging accessions with environmental fluctuations revealed regime-specific flexibility, with plasticity primarily mediated by a single division-related parameter. Our results show how cellular parameters integrate into alternative developmental strategies that shape environmental responsiveness.

Plant phenotyping relevance

葉の成長中の細胞挙動を追跡するライブセルイメージングツールを開発し、気孔密度の発生的起源を定量化しており、植物フェノタイピング手法が研究の中心である。

Code and data availability

The supplied blocks describe live-cell imaging phenotyping of Arabidopsis stomatal lineages and computational analyses (regression, PCA, PLS), but contain no public phenotype dataset, image deposit, analysis code, or model availability statement with an authors' public URL. Supplemental tables are referenced but no de­

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