Spatiotemporal coupling of vessel cavitation and discharge of stored xylem water in a tree sapling.

Water discharge from stem internal storage compartments is thought to minimize the risk of vessel cavitation. Based on this concept, one would expect that water storage compartments involved in the buffering of xylem tensions empty prior to the onset of vessel cavitation under drought stress, and potentially refill following soil saturation. However, scant in-vivo data exist that elucidate this localized spatiotemporal coupling. In this study on intact saplings of Castanea dentata, X-ray computed microtomography showed that the xylem matrix surrounding vessels releases stored water and becomes air-filled either concurrent to or following vessel cavitation under progressive drought stress. Among annual growth rings, the xylem matrix of the current-year remained largely water-filled even under severe drought stress. In line with observations on intact saplings, microCT images collected on excised stems showed that applied pressures of >>0 MPa were required to induce water release from the xylem matrix. Viability staining highlighted that water release from the xylem matrix was associated primarily with emptying of dead fibers. Refilling of xylem matrix and vessels was detected in intact saplings when the canopy was bagged and stem water potential was close to 0 MPa, and in leafless saplings over the winter period. In conclusion, this study indicates that the bulk of water stored in the xylem matrix is released after the onset of vessel cavitation, and suggests that capillary water contributes to overall stem water storage under drought but is not utilized primarily for the prevention of drought-induced vessel cavitation in this species.