How plants coordinate local organ formation with systemic information about environmental conditions remains largely unclear. Here we show that availability of the phytohormone auxin across the Arabidopsis root provides a shared hormonal state that integrates environmental cues and gates whether locally specified branching sites develop. Long-term luminescence imaging, time-resolved transcriptomics and metabolite profiling reveal approximately 24-hour rhythms in auxin abundance and signalling at 21°C, with shoot-perceived light setting the amplitude of the systemic signalling. At 29°C, this organisation is reprogrammed into a root-wide decline followed by a light-dependent systemic recovery of auxin signalling. Recovery under sufficient light supports root branching-site progression without requiring restored circadian rhythmicity. In contrast, weaker recovery under reduced light leads to arrest of early primordia. Genetic analyses implicate phytochrome B as well as cryptochromes photoreceptors and the morning loop of the circadian clock in this conditional response. The auxin oxidase DIOXYGENASE FOR AUXIN OXIDATION 1 (DAO1) reprograms systemic auxin dynamics at elevated temperature. Reducing auxin oxidation sustains signalling in branching sites and lateral root development during warming, whereas increased oxidation weakens recovery and enhances developmental inhibition. Our findings reveal how systemic metabolic control allows plants to interpret global environmental information in context and therewith align local de novo organ formation.
