Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation  

Abstract

We report a novel form of xylem dysfunction in angiosperms: reversible collapse of the xylem conduits of the smallest vein orders that demarcate and intrusively irrigate the areoles of red oak (Quercus rubra) leaves. Cryo-scanning electron microscopy revealed gradual increases in collapse from approximately 22 MPa down to 23 MPa, saturating thereafter (to 24 MPa). Over this range, cavitation remained negligible in these veins. Imaging of rehydration experiments showed spatially variable recovery from collapse within 20 s and complete recovery after 2 min. More broadly, the patterns of deformation induced by desiccation in both mesophyll and xylem suggest that cell wall collapse is unlikely to depend solely on individual wall properties, as mechanical constraints imposed by neighbors appear to be important. From the perspective of equilibrium leaf water potentials, petioles, whose vessels extend into the major veins, showed a vulnerability to cavitation that overlapped in the water potential domain with both minor vein collapse and buckling (turgor loss) of the living cells. However, models of transpiration transients showed that minor vein collapse and mesophyll capacitance could effectively buffer major veins from cavitation over time scales relevant to the rectification of stomatal wrong-way responses. We suggest that, for angiosperms, whose subsidiary cells give up large volumes to allow large stomatal apertures at the cost of potentially large wrong-way responses, vein collapse could make an important contribution to these plants' ability to transpire near the brink of cavitation-inducing water potentials.Terrestrial photosynthesis is inextricably linked with water loss. Plants expose hydrated cells to the atmosphere to obtain CO 2 , with evaporation an inevitable consequence. Vascular plants meet this challenge by replacing water lost via transpiration with water pulled from the soil. What allows this is the xylem: a system of stiff-walled conduits capable of remaining water filled at negative pressures low enough to extract water from micrometer-to nanometer-scale soil capillaries and to drive flow through the 10-to 100-mm-diameter xylem conduits that extend from the roots to the leaves (Tyree and Zimmermann, 2002). To deliver water at rates equal to transpiration, the pressure in the xylem must fall far below the vapor pressure of water, such that water transport through the xylem occurs in a metastable state (i.e. at kinetic, but not thermodynamic, equilibrium) and thus at risk of cavitation (Stroock et al., 2014). How many plants seemingly operate with little to no safety margin against cavitation Brodribb and Holbrook, 2004;Meinzer et al., 2009;Choat et al., 2012) remains an important and unsolved question.Cavitation occurs when metastable liquid water is replaced by water vapor due to the expansion of a gas bubble nucleus, forming an embolism or air blockage: embolism disrupts water transport because tensions cannot be transmitted through gas. The most probable origin of such nuclei is thought to be g...

Outside-Xylem Vulnerability, Not Xylem Embolism, Controls Leaf Hydraulic Decline during Dehydration

“…Such results are consistent with the hypothesis that strong K ox declines would act as a protective bottleneck, shielding the leaf and stem xylem under many scenarios of atmospheric and soil drought from tensions that would induce catastrophic embolisms (Scoffoni et al, 2014). Additional mechanisms for protection may operate; a recent study found that minor vein collapse in leaves of red oak (Quercus rubra) occurred under very strong tensions below the turgor loss point (more negative than 23 MPa) and, thus, could act as a further buffer against embolism under prolonged drought (Zhang et al, 2016). Notably, a similar protection occurs in roots, as cortical lacunae formation in fine roots induced strong declines in hydraulic conductance protecting root xylem conduits from embolism formation .…”

Neither xylem collapse, cavitation, or changing leaf conductance drive stomatal closure in wheat

“…Indeed, some vessels were non‐circular under well‐watered conditions, whereas others remained circular even under great water stress. Although a partial recovery of vessel shape after rehydration was observed in oak trees (Zhang et al, ), vessel deformation was found to be irreversible in wheat as neither xylem cavitation nor sample cutting caused a change in vessels shape, suggesting that flattening of hydraulic conduits might be caused by a force other than xylem pressure in wheat. Furthermore, the expected dichotomy in vessel shape characterizing vessel implosion (Brodribb & Holbrook, ) was not observed in wheat as vessels flattened slowly along the water stress gradient.…”

The Pneumatron: An automated pneumatic apparatus for estimating xylem vulnerability to embolism at high temporal resolution

“…Because the internal volume of the solenoid valve and connections determine V r , these components must be adapted to detect small amounts of gas extracted from leaf veins. It is currently unclear whether leaf morphology and conduit collapse in leaf veins affect gas extraction (Zhang, Rockwell, Graham, Alexander & Holbrook, ), which would make the pneumatic method problematic for some species.…”