Non-destructive quantification of shoot apical meristem homeostasis for plant architecture and biomass prediction based on robot-based 3D imaging and photosynthetic measurements

Shoot apical meristem (SAM) homeostasis integrates environmental and genetic cues to regulate growth dynamics that drive biomass accumulation and crop yield; however, no robust, non-destructive, quantitative proxy has been established to model or monitor SAM homeostasis-associated dynamics. Here, we developed a novel robot-based three-dimensional (3D) imaging system as well as a custom pot-chamber gas exchange system to non-destructively measure plant occupation volume (POV) and plant-level photosynthetic rate in Arabidopsis wild-type plants and nine mutants with disrupted SAM homeostasis. We demonstrate that POV robustly captures 3D plant architecture, whereas plant photosynthetic rate serves as a superior proxy for optimal growth dynamics and final biomass associated with SAM homeostasis, outperforming conventional traits such as leaf number, leaf size, total leaf area, and rosette diameter. The strong positive correlations among POV, plant photosynthesis, and biomass accumulation establish a powerful new framework for quantitative studies of SAM homeostasis and data-driven evaluation of plant architecture.