Storage compartments for capillary water refill in excised stems but rarely refill in intact woody plants (Laurus nobilis): Visualization of tissue-specific dynamics using microCT imaging

Authors: KNIPFER, THORSTEN - University Of California; CUNEO, ITALO - University Of California; EARLES, J. MASON - Yale University; REYES, CLARISSA - University Of California; BRODERSON, CRAIG - Yale University; McElrone, Andrew

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/17/2017
Publication Date: 12/5/2017
Citation: Knipfer, T., Cuneo, I., Earles, J., Reyes, C., Broderson, C., McElrone, A.J. 2017. Storage compartments for capillary water refill in excised stems but rarely refill in intact woody plants (Laurus nobilis): Visualization of tissue-specific dynamics using microCT imaging. Plant Physiology. 175(4):1649-1660. https://doi.org/10.1104/pp.17.01133.
DOI: https://doi.org/10.1104/pp.17.01133

Interpretive Summary: Stem water storage can prolong xylem hydraulic function and survival of woody plants under drought, but direct measurements of tissue-specific water storage remain elusive. Here, we imaged Laurus nobilis trees with X-ray computed micro-tomography (microCT) to investigate the time course and process of fiber and pith refilling in relation to vessel filling status. In intact saplings, refilling of air-filled fibers, pith tissue, and vessels was negligible over two timescales, a period of 24-h and 3-weeks, but data indicated that these capacitive tissues refill slowly when the shoot was covered in petroleum jelly and a humid plastic bag. In excised stems supplied with H2O, fibers and pith tissue refilled substantially in less than 8-h, while vessel filling status was variable. Initiation of vessel refilling (i.e. water droplets on wall, expanding water columns) was observed under both in-vivo and excised conditions, but this phenomenon was rare. Capillary forces predominantly drove the refilling of dead fibers and pith tissue as suggested by concave-shaped liquid/air menisci. Fiber-to-fiber, vessel-to-fiber, and vessel-to-vessel pitting was detected in stem xylem, as well as cell-to-cell connections in pith tissue, suggesting that water movement associated with capacitance and vessel refilling/emptying was associated with tissue network connectivity. Collectively, these data provide novel insights concerning tissue-specific dynamics of water storage under in-vivo and excised conditions, and suggest that water stored in dead fibers and pith tissue by capillarity may only be available for a single drought event, as these compartments do not refill on a diurnal basis in-vivo.

Technical Abstract: Water storage is thought to play an integral role in the maintenance of whole-plant water balance. The contribution of both living and dead cells to water storage can be derived from rehydration and water-release curves on excised plant material, but the underlying tissue-specific emptying/refilling dynamics remain unclear. Here, we used x-ray computed microtomography to characterize the refilling of xylem fibers, pith cells, and vessels under both excised and in vivo conditions in Laurus nobilis In excised stems supplied with water, water uptake exhibited a biphasic response curve, and x-ray computed microtomography images showed that high water storage capacitance was associated with fiber and pith refilling as driven by capillary forces: fibers refilled more rapidly than pith cells, while vessel refilling was minimal. In excised stems that were sealed, fiber and pith refilling was associated with vessel emptying, indicating a link between tissue connectivity and water storage. In contrast, refilling of fibers, pith cells, and vessels was negligible in intact saplings over two time scales, 24 h and 3 weeks. However, those compartments did refill slowly when the shoot was covered to prevent transpiration. Collectively, our data (1) provide direct evidence that storage compartments for capillary water refill in excised stems but rarely under in vivo conditions, (2) highlight that estimates of capacitance from excised samples should be interpreted with caution, as certain storage compartments may not be utilized in the intact plant, and (3) question the paradigm that fibers play a substantial role in daily discharge/recharge of stem capacitance in an intact tree.