The Plant Vascular System: Evolution, Development and FunctionsF

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There is abundant evidence that cavitation “pressures” in plants are negative enough for the cohesion-tension mechanism to operate. Such pressures are determined from a “vulnerability curve” which usually plots the hydraulic conductivity (reciprocal of resistivity) of the xylem (often as a percentage loss from maximum) as a function of the ψP value in the xylem sap. Curves are generated in several ways, but the centrifuge method is commonly used because of its rapidity (Alder et al. 1997; Cochard et al. 2005). Stems or roots are spun in a custom centrifuge rotor that places their xylem under a known tension at the center of rotation. The conductivity is measured either during or between spinning, and the experiment is continued until the conductivity has dropped to negligible values, thus indicating complete blockage of flow by cavitation. Typical species-specific variation is shown in Figure 17A, and Figure 17B compares the ψP value causing complete loss of xylem conductivity with the minimum ψP values measured in nature for 102 species (Sperry 2000). Clearly, the xylem of some species cavitates much more readily than others, but these vulnerable species also do not develop very negative ψP values in nature. Across the board, the minimum ψP is generally less negative than the value of ψP at zero conductivity, as is required by the cohesion-tension mechanism. Although the centrifuge method is widely accepted for conifers and for short-vesseled angiosperms, there is some controversy about its ability to measure the vulnerability of longvesseled taxa where many conduits can exceed the length of the spinning conductivity segment. Response curves in these taxa indicate that a significant number of these large vessels cavitate at very modest negative ψP values. This pattern is seen in two of the curves shown in Figure 17A (open symbols). Comparisons with other methods have verified this type of curve in many (Christman et al. 2012; Jacobson and Pratt 2012; Sperry et al. 2012), but not in all cases (Choat et al. 2010; Cochard et al. 2010a), and resolving the matter requires further research. A major cause of the cavitation in plant xylem is air-seeding through the inter-conduit pits that normally are responsible for confining gas embolism (Crombie et al. 1985; Sperry and Tyree 1988; Sperry and Tyree 1990; Jarbeau et al. 1995). The Pmin of inter-conduit connections is easily measured from the positively applied gas pressure that just breaches their seal (Christman et al. 2012). From a variety of techniques employed across a wide range of species, the Pmin range of inter-conduit pitting is generally indistinguishable from the range of ψP values that cause cavitation. In consequence, vulnerability curves can usually be reproduced using positive gas pressures rather than placing the xylem sap under tension (Cochard et al. 1992). The prevailing model of cavitation nucleation is that when the ψP in the transpiration stream drops to the Pmin of the inter-conduit seal against adjoining embolized vessels, a gas bubble is pulled into the transpi- Insights into Plant Vascular Biology 333 ration stream which then nucleates cavitation. The sap ψP in the cavitated conduit immediately rises to 0, and the sap is very quickly drained out of the conduit by the surrounding transpiration stream until the entire conduit becomes filled with water vapor and air, the exact composition of the embolism depending on diffusive exchange with the surrounding tissue (Tyree and Sperry 1989). According to this model, cavitation and embolism can propagate from conduit-to-conduit via pit failure. Considerable attention has been given to how the structure of inter-conduit pitting relates to its function in cavitation resistance. In conifer tracheids, where torus aspiration seals the pits, it has been proposed that air-seeding occurs when the pit membrane is stretched sufficiently to displace the torus from the aperture, exposing part of the margo through which air can readily pass (Figure 16D). Displacement has been observed microscopically, and conifers that are more resistant to cavitation generally have less flexible pit membranes, and can have a torus that covers the aperture with greater overlap (Sperry and Tyree 1990; Domec et al. 2006; Hacke and Jansen 2009). An alternative model is that air seeding occurs by displacement of the air-water-interface between the torus and the pit chamber wall. In some conifers, air-seeding could also occur through pores in the torus. In support of these mechanisms is a dependence of Pmin on the sap surface tension (Cochard et al. 2009; Holtta et al. 2012; Jansen et al. 2012). However, it is not clear whether sap solutions that lower the surface tension also alter pit membrane flexibility and, hence, the ease of torus displacement. It is also unclear whether the torus-margo membrane can de-aspirate to function a second time if the embolized tracheids refill. In angiosperm inter-vessel pits, air seeding probably occurs by displacement of the air-water meniscus from pores in their homogenously nano-porous pit membranes (Figure 16D), but beyond this, the details are surprisingly complex and ambiguous. Air seeding at pores is implied by the predicted sensitivity to surfactants and correspondence between pore dimensions, sized by particle penetration, and air-seeding pressures (Crombie et al. 1985; Sperry and Tyree 1988; Jarbeau et al. 1995). The pores may be pre-existing in the membrane, or perhaps created or enlarged by the partial or complete aspiration of the membrane that likely precedes the air-seeding (Thomas 1972). A major role of membrane strength is indicated by the effects of removing Ca 2+ from the membrane using various chelators such as oxalic acid. These treatments do not alter surface tension or hydraulic conductivity, but they can dramatically increase membrane flexibility and vulnerability to cavitation (Sperry and Tyree 1988; Sperry and Tyree 1990; Herbette and Cochard 2010). Further support for the importance of membrane mechanics is the cavitation “fatigue” phenomenon wherein xylem becomes more vulnerable to cavitation after having been cavitated and
334 Journal of Integrative Plant Biology Vol. 55 No. 4 2013 Figure 17. Vulnerability of xylem to cavitation by negative pressure. (A) Vulnerability curves for five species showing the drop in xylem hydraulic conductivity (normalized by stem cross-sectional area) as the xylem pressure becomes more negative. Curves were generated using the centrifugal force method. Species can differ considerably in their maximum hydraulic conductivity (x axis intercept) and how readily they lose it to cavitation (from Hacke et al. 2006). (B) Xylem pressure at zero hydraulic conductivity from cavitation (the y intercept of a, above) vs. the minimum pressure observed in nature for 102 species (from Sperry 2000). re-filled. The implication is that mechanical stress has plastically deformed the membrane to make it more porous. Cavitation fatigue is potentially reversible in vivo and with artificial xylem saps, suggesting the stressed and air-seeded pit membrane can be restored back to its normal form (Hacke et al. 2001b; Stiller and Sperry 2002). The possibility that pores are created by mechanical stress on the pit membrane is also consistent with the typical rarity of
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The Plant Vascular System: Evolution, Development and FunctionsF

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