The point of disconnection: early-drought fine root shrinkage is driven by plant water use in Pinus radiata

Understanding the root-soil interface is essential for determining when plants become hydraulically isolated from their soil environment during drought. Emerging evidence suggests roots shrink substantially during dehydration, but the drivers and water-flow implications remain elusive, with few data linking shrinkage across soil and plant water status. Using Pinus radiata, a widespread isohydric conifer, we use synchrotron-based Micro-CT to scan intact roots < 2.5 mm in soil during mild plant drying (prior to embolism) to isolate relationships between shrinkage, soil (Ψsoil) and xylem (Ψplant) water potential. Fine roots in situ began shrinking during the earliest stages of Ψplant drying (-0.2 MPa to -0.88 MPa), losing 14.8 ± 10.3% initial transverse-sectional area (62% of observed shrinkage) prior to incipient soil drying (0-72 kPa Ψsoil). Ψplant was a significantly better predictor of shrinkage than Ψsoil, showing a linear shrinkage-Ψplant relationship across this early drying gradient when normalised to shrinkage at -1 MPa, accounting for variable initial Ψplant. Ψplant decline was linearly coordinated with cortical lacunae formation. This Ψplant-driven pattern identifies root shrinkage as an essential component of plant hydraulic function during commonly experienced water potential gradients, occurring long prior to stomatal closure and xylem embolism. This reveals water use from cortical tissues as a key physiological process defining plant-soil disconnection during water deficit.