Non-destructive quantification of shoot apical meristem homeostasis for prediction of plant architecture and biomass using robot-based 3D imaging and photosynthesis 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 for modeling or monitoring SAM-homeostasis-associated dynamics. Here, we developed a novel robot-based 3D imaging system and a custom pot-chamber gas exchange system to non-destructively measure plant occupation volume (POV) and whole-plant photosynthetic rate in wild-type Arabidopsis plants and nine mutants with disrupted SAM homeostasis. We demonstrate that POV robustly captures 3D plant architecture, whereas whole-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, whole plant photosynthesis, and biomass accumulation establish a powerful new framework for quantitative studies of SAM homeostasis and data-driven evaluation of plant architecture.