Reversible Deformation of Transfusion Tracheids in Taxus baccata Is Associated with a Reversible Decrease in Leaf Hydraulic Conductance

Abstract

Declines in leaf hydraulic conductance (K leaf ) with increasing water stress have been attributed to cavitation of the leaf xylem. However, in the leaves of conifers, the reversible collapse of transfusion tracheids may provide an alternative explanation. Using Taxus baccata, a conifer species without resin, we developed a modified rehydration technique that allows the separation of declines in K leaf into two components: one reversible and one irreversible upon relaxation of water potential to 21 MPa. We surveyed leaves at a range of water potentials for evidence of cavitation using cryo-scanning electron microscopy and quantified dehydration-induced structural changes in transfusion tracheids by cryo-fluorescence microscopy. Irreversible declines in K leaf did not occur until leaf water potentials were more negative than 23 MPa. Declines in K leaf between 22 and 23 MPa were reversible and accompanied by the collapse of transfusion tracheids, as evidenced by cryo-fluorescence microscopy. Based on cryo-scanning electron microscopy, cavitation of either transfusion or xylem tracheids did not contribute to declines in K leaf in the reversible range. Moreover, the deformation of transfusion tracheids was quickly reversible, thus acting as a circuit breaker regulating the flux of water through the leaf vasculature. As transfusion tissue is present in all gymnosperms, the reversible collapse of transfusion tracheids may be a general mechanism in this group for the protection of leaf xylem from excessive loads generated in the living leaf tissue.

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

“…That the collapse of xylem conduits in the minor veins of red oak did not appear to affect measurements of K l requires comment, especially as the collapse of transfusion tracheids was closely associated with declines in K l in the conifers Podocarpus greyi and Taxus baccata (Brodribb and Holbrook, 2005;Zhang et al, 2014). The speed with which oak leaves rehydrate, coupled with the lack of any significant hysteresis in conduits returning to an unbuckled shape, means that much of the hydraulic effect of conduit collapse would have been lost early during the longer rehydration times required to measure K l on leaves initially below their turgor loss points (due to the increased capacitance).…”

“…If xylem conduits are unable to withstand the mechanical forces imposed by the negative pressure, they can deform or collapse inward, with the reduction in Poiseuille (or effective) radius markedly reducing the hydraulic conductance. Conduit deformation has been observed in tracheids of conifer leaves, most notably in transfusion tracheids, which supply water laterally from the vein to the photosynthetic cells (Cochard et al, 2004a;Brodribb and Holbrook, 2005;Zhang et al, 2014). In angiosperms, leaf xylem conduit thickness-to-span ratios (thought to be predictive of collapse) have been shown to correlate with resistance to the loss of hydraulic conductance as xylem tensions increase (Blackman et al, 2010), but no previous study has addressed whether xylem conduits in angiosperm leaves collapse as leaf water potentials (C L ) decline.…”

The Anatomical Determinants of Leaf Hydraulic Function

“…Additionally, along a height gradient in Douglas fi r, the hydraulic vulnerability of leafy shoots was lower for shoots with needles with narrower xylem conduits, fewer tracheids per cross-sectional leaf area, and fewer pits per tracheid (Woodruff et al 2008 ). In dicotyledons, narrower conduits in minor veins Brodribb et al 2007 Accessory transport elements might act as water storage to buffer cell water potentials from transiently high transpiration rates (Takeda 1913 ) Collapse of transfusion tracheids in conifers is associated with K leaf decline in dehydrating leaves (Brodribb and Holbrook 2005 ;Zhang et al 2014 ) may be protected during collapse under strong xylem tensions arising during drought. Thus, leaf minor vein conduit cell wall thickness to lumen breadth ratio ([ t / b ] 3 ) was positively related to leaf hydraulic vulnerability for 20 angiosperm species (Blackman et al 2010 ), and positively correlated with moisture availability in 67 species from the Proteaceae ).…”

Leaf Hydraulic Architecture and Stomatal Conductance: A Functional Perspective

“…Ginkgo tracheid diameters (10-15 mm; Leigh et al, 2011) overlap with midrib vessel diameter vessels in Viburnum spp. (9-18 mm; Scoffoni et al, 2016), and minor vein tracheary element diameters in red oak are in the range of tracheid diameters in Taxus baccata needles and Pseudotsuga menziesii fine branchlets (5-10 mm; Woodruff et al, 2008;Zhang et al, 2014Zhang et al, , 2016. While a more systematic analysis than these ad hoc comparisons is required to draw any firm conclusions, we can say, based on Pittermann et al (2005), that replacing the conduits in an oak minor vein with conifer-type tracheids of the same diameter would only increase the resistivity by about 20%, a loss that could be offset by an increase in tracheid diameter of only 5%.…”