The architecture of the branched root system of plants is a major
determinant of vigor. Water availability is known to impact root
physiology and growth; however, the spatial scale at which this
stimulus influences root architecture is poorly understood. Here we
reveal that differences in the availability of water across the
circumferential axis of the root create spatial cues that determine
the position of lateral root branches. We show that roots of several
plant species can distinguish between a wet surface and air environments
and that this also impacts the patterning of root hairs,
anthocyanins, and aerenchyma in a phenomenon we describe as
hydropatterning. This environmental response is distinct froma touch
response and requires available water to induce lateral roots along
a contacted surface. X-ray microscale computed tomography and 3D
reconstruction of soil-grown root systems demonstrate that such
responses also occur under physiologically relevant conditions. Using
early-stage lateral root markers, we show that hydropatterning acts
before the initiation stage and likely determines the circumferential
position at which lateral root founder cells are specified. Hydropatterning
is independent of endogenous abscisic acid signaling,
distinguishing it from a classic water-stress response. Higher water
availability induces the biosynthesis and transport of the lateral
root-inductive signal auxin through local regulation of TRYPTOPHAN
AMINOTRANSFERASE OF ARABIDOPSIS 1 and PIN-FORMED
3, both of which are necessary for normal hydropatterning. Our
work suggests that water availability is sensed and interpreted at
the suborgan level and locally patterns a wide variety of developmental
processes in the root.