Spatiotemporal Coupling of Vessel Cavitation and Discharge of Stored Xylem Water in a Tree Sapling

Abstract

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 before the onset of vessel cavitation under drought stress, and potentially refill after soil saturation. However, scant in vivo data exist that elucidate this localized spatiotemporal coupling. In this study on intact saplings of American chestnut (Castanea dentata), x-ray computed microtomography (microCT) showed that the xylem matrix surrounding vessels releases stored water and becomes air-filled either concurrent to or after 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 comparison, microtomography images collected on excised stems showed that applied pressures of much greater than 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 the 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 used primarily for the prevention of drought-induced vessel cavitation in this species. The water transport system of woody plants can experience excessive xylem tensions in response to changing environmental conditions. It is generally assumed that water stored in capacitive tissue is sourced into the transpiration stream to buffer liquid tensions that develop inside the vessel lumen, and in turn protect vessel functionality by reducing the risk of gas emboli formation (Holbrook, 1995). Experimental data collected on intact trees using sap flow sensors suggest that the process of stem water storage-release is dynamic, where water is stored during the nighttime and is released during the daytime when transpiration and xylem tension become significant (e.g. Waring et al., 1979; Goldstein et al., 1998; Cermák et al., 2007). More recently, magnetic resonance imaging (MRI) data have provided direct evidence that water storage dynamics are tightly linked to changes in stem dimensions associated with bark shrinkage and swelling (De Schepper et al., 2012). Recent studies using frequency domain reflectometry highlighted that water storage also plays an important role in long-term maintenance of plant water balance, and that the utilization of stored water can differ between xylem regions (Hao et al., 2013; Matheny et al., 2015). Expanding on these findings, we recently used x-ray computed microtomography (microCT) to characterize the time course of tissuespecific ...

Wood capacitance is related to water content, wood density, and anatomy across 30 temperate tree species

“…suggesting that water may be released from fibres in these species (as well as vessels, see 556 above). This is in agreement with microCT evidence of emptying fibres (and vessels) as 557 water potential decreases (Knipfer et al 2017(Knipfer et al , 2019). An interesting path forward would be to 558 measure the size of fibre lumina and taper, because these characteristics could have an 559 additional effect on capillary water release as capillary tension and lumen diameter are 560 negatively correlated (Tyree & Yang 1990;Hölttä et al 2009).…”

“…Given these knowledge gaps, it is surprising that parenchyma, the main living tissue 83 in wood commonly believed to have elastic cell walls, is often assumed the primary source of (fibres, vessels) via highly lignified middle lamella impeding parenchyma independent 95 volumetric changes. Moreover, recent microCT studies, suggest that water released from 96 cavitating fibres and vessels may contribute meaningfully to capacitance at moderate water 97 potentials (Knipfer et al 2017(Knipfer et al , 2019. 98…”

Hydraulic acclimation in a Mediterranean oak subjected to permanent throughfall exclusion results in increased stem hydraulic capacitance

“…Further research in wood anatomy and tree water content regulation under drought stress (Knipfer et al, ; Martinez‐Vilalta et al, ) could help to more accurately discriminate how stem capacitive water sources are preferentially used during drought stress, and to better understand the underlying link between C S and the regulation of water potential and carbon and water exchange. More long‐term data on stem water pools, C S and allometric adjustments applying non‐destructive techniques across different species would be necessary to evaluate the generality of the pattern observed here and advance knowledge on hydraulic acclimation strategies across plant functional types.…”

“…The amount of water released at this point largely depends on the amount and lumen size of embolized conduits. Recent studies performed in vivo using X‐ray microtomography question, however, whether this sequential release of capacitive water sources along the desorption curve, which has been derived from excised branches, can be extrapolated to living plants (Knipfer et al, , ).…”

In vivo pressure gradient heterogeneity increases flow contribution of small diameter vessels in grapevine

“…The magnitude of storage pools in the xylem, however, is negligible compared to the flow rate during transpiration in many plants 44 , including first-year grapevine stems and thus is unlikely to shape pressure gradients within our model domain to any significant extent. Moreover, it has been shown that even storage pools theoretically available in the xylem can remain largely unused in vivo 45,46 , meaning that their effect on local pressure gradients is likely less pronounced than their total capacity suggests. Finally, while significant release of water from storage can temporarily affect transverse pressure gradient patterns, it is unclear why this mechanism should lead to a decreased overall contribution of widest vessels to flow.…”