Two distinct oscillatory auxin signals define the plasticity of lateral rooting in Arabidopsis thaliana

The phytohormone auxin defines lateral root pre-branch sites (PBS) in the growing primary root tip. How PBS contribute to the plasticity of the root system architecture remains incompletely understood1,2,3,4. Here, we reveal in the model plant Arabidopsis thaliana that two distinct oscillatory systems for the phytohormone auxin coordinate the spatial and temporal identity of PBS, jointly defining the lateral root density. We followed auxin signalling dynamics for days and thereby detected a systemic auxin signal oscillating along the mature primary root, where PBS potentially form functional root branches. While a previously proposed local oscillatory auxin zone spatially primes the PBS in the growing root tip, we reveal that the systemic oscillatory auxin signal temporally controls the auxin-dependent identity of these PBS. Light perception in the shoot defines the strength of the systemic auxin signal and thereby controls the auxin-reliant ability of PBS to develop into lateral roots. Moreover, PHYB and CRY1 mediate the light-dependent integration of other environmental signals, such as ambient temperature, into the control systemic auxin signalling and lateral root density. Our work reveals how two spatially distinct oscillatory auxin signals define the plasticity of plant root development in response to fluctuating conditions.