TOP1 alpha fine-tunes TOR-PLT2 to maintain root tip homeostasis in response to sugars

Photosynthesis promotes the expression of TOPOISOMERASE1 alpha, which in turn represses TARGET OF RAPAMYCIN (TOR) expression at the root tip. Glucose-TOR regulates cell division at the quiescent centre, and phosphorylates and stabilizes PLETHORA2 in columella cells to maintain root tip homeostasis. Plant development is highly dependent on energy levels. TARGET OF RAPAMYCIN (TOR) activates the proximal root meristem to promote root development in response to photosynthesis-derived sugars during photomorphogenesis in Arabidopsis thaliana. However, the mechanisms of how root tip homeostasis is maintained to ensure proper root cap structure and gravitropism are unknown. PLETHORA (PLT) transcription factors are pivotal for the root apical meristem (RAM) identity by forming gradients, but how PLT gradients are established and maintained, and their roles in COL development are not well known. We demonstrate that endogenous sucrose induces TOPOISOMERASE1 alpha (TOP1 alpha) expression during the skotomorphogenesis-to-photomorphogenesis transition. TOP1 alpha fine-tunes TOR expression in the root tip columella. TOR maintains columella stem cell identity correlating with reduced quiescent centre cell division in a WUSCHEL RELATED HOMEOBOX5-independent manner. Meanwhile, TOR promotes PLT2 expression and phosphorylates and stabilizes PLT2 to maintain its gradient consistent with TOR expression pattern. PLT2 controls cell division and amyloplast formation to regulate columella development and gravitropism. This elaborate mechanism helps maintain root tip homeostasis and gravitropism in response to energy changes during root development.