Root growth and branching are enabled by brassinosteroid-regulated growth anisotropy and carbon allocation

Abstract

Plants function as an integrated system of interconnected organs, with shoots and roots mutually influencing each other. Brassinosteroid (BR) signaling is essential for whole-plant growth, yet the relative importance of shoot versus root BR function in shaping root system architecture (RSA) remains unclear. Here, we directly tackle this question using micro-grafts between wild-type and BR-null mutants in both Arabidopsis and tomato, assisted by phenotyping, transcriptomics, metabolic profiling, transmission electron microscopy, and modeling approaches. These analyses demonstrate that shoot BR, by determining root carbon availability, allows for a full rescue of mutant root biomass, while loss of shoot BR attenuates root growth. In parallel, root BR dictates the spatial distribution of carbon along the root, through local regulation of growth anisotropy and cell wall thickness, shaping root morphology. A newly developed “grow and branch” simulation model demonstrates that these shoot- and root-derived BR effects are sufficient to explain and predict root growth dynamics and branching phenotype in wild-type, BR-deficient mutants, and micro-graft combinations. Our interdisciplinary approach, applied to two plant species and integrating shoot and root hormonal functions, provides a new understanding of how RSA is modulated at various scales.