Shoot loss reveals the latent capacity of Arabidopsis roots to reconstruct the plant body

Abstract

Plant body organization depends on the coordinated development and function of shoots and roots, yet their functional specialization and interdependence remain incompletely understood. Whereas shoot senescence and death, as well as root regeneration from shoot tissues, are well studied, what capacities roots retain in the absence of the shoot remain unclear. To address this question, we tracked Arabidopsis roots after complete shoot excision. Initially, the remaining roots entered a growth-arrested but viable state. Despite broad repression of growth-associated programs, auxin and cytokinin signaling persisted, and the roots retained developmental responsiveness. This arrested state, however, was not developmentally terminal. By approximately 20 days after excision, green structures emerged from lateral root-associated domains. They accumulated chlorophyll and starch, assimilated carbon in response to light, and developed persistent cuticle-covered surfaces. Based on their origin and shoot-like characteristics, we termed them lateral root-derived shoots (LRSs). LRSs arose preferentially in the most shoot-proximal region, where cytokinin signaling progressively accumulated. Excision of this region repositioned LRS formation to the newly established proximal boundary, indicating spatial redefinition of shoot-forming competence. Auxin and cytokinin antagonistically governed the choice between continued lateral root growth and LRS identity, with cytokinin further promoting leaf-like differentiation. LRSs subsequently formed roots and developed into fertile plants under appropriate conditions. These findings reveal that roots retain developmental competence after shoot loss and can reorganize positional and hormonal programs to acquire shoot identity and reconstruct a complete plant body.