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

Thorsten Knipfer,Clarissa Reyes,Craig R Brodersen,Daniel M Johnson,Andrew J Mcelrone,Z Carter Berry,J Mason Earles

doi:10.1104/pp.18.01303

Thorsten Knipfer, Clarissa Reyes + Show 5 more

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https://doi.org/10.1104/pp.18.01303

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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.

Highlights

Water discharge from stem internal storage compartments is thought to minimize the risk of vessel cavitation
In dead cell types with extremely rigid walls, such as dead fibers that provide for capillary water storage, a release of stored water will directly result in emptying of the lumen water, which has been shown using microCT imaging (Knipfer et al, 2017)
The spatiotemporal coupling of vessel cavitation and emptying of cells in the xylem matrix was investigated in three intact C. dentata saplings

Summary

Introduction

Water discharge from stem internal storage compartments is thought to minimize the risk of vessel cavitation. 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. According to published studies (as cited above), stem internal water storage under drought depends primarily on elastic water storage in living cells, but the contribution of tissue-specific storage of capillary water, under excised versus in vivo (intact plant) conditions, remains to be investigated. The goal of this study was to expand on our recent observations of tissue-specific refilling (Knipfer et al, 2017), and provide new insights into the spatiotemporal coupling between drought-induced vessel cavitation and release of stored xylem water under in vivo conditions and for different annual growth rings. Fluorescence light microscopy was used to detect the location of metabolically active cells in the stem

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