The Plant Vascular System: Evolution, Development and FunctionsF

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Figure 15. Inter-vessel pit structure in angiosperm wood. Upper-right insert shows brightfield image of two overlapping vessels. Their common wall is studded with inter-vessel pits as shown in the main scanning electron microscopy (SEM) image where an intervessel wall has been sectioned to show individual pit structure. Pits consist of openings in the secondary wall (apertures) leading to pit chambers that are spanned by a pit membrane which is the modified primary cell wall and middle lamella of the adjacent vessel elements. The lower-right insert shows an SEM face view of the micro-porous pit membrane. Scale bars: 5 µm and 30 µm for the upper inset. Micrographs courtesy of Fredrick Lens, Jarmila Pittermann, and Brendan Choat. Inter-conduit pits add substantial flow resistance to the xylem conduit lumen. An unobstructed lumen conducts water as efficiently as an ideal cylindrical capillary tube of the same diameter (Zwieniecki et al. 2001a; Christman and Sperry 2010). The most extensive survey indicates that adding inter-conduit pits increases flow resistivity over that of an unobstructed lumen by an average factor of 2.8 in conifers with unicellular tracheids and 2.3 in angiosperms with multicellular vessels (Hacke et al. 2006; Pittermann et al. 2006a). The lower number for vessels is not surprising given that they are roughly 10 times longer than a tracheid of the same diameter (Pittermann et al. 2005), thereby spacing high resistance pits further apart and reducing the length-normalized resistance (resistivity). What is surprising is that the greater length of vessels does not have more of an effect: if inter-vessel pits have the same area-specific pit resistance as inter-tracheid pits, placing the end-walls 10 times further apart should increase lumen resistivity by less than a factor of 1.18. The higher observed factor of 2.3 indicates that inter-vessel pits have higher flow resistance than inter-tracheid ones, a difference consistent with anatomy and estimations based on modeling (Pittermann et al. 2005). Inter-vessel pits have nano-porous “homogeneous” pit membranes (pores usually < 100 nm) (Choat et al. 2008), or Insights into Plant Vascular Biology 331 Figure 16. Structure and function of inter-conduit pits in conifer tracheids (left) and angiosperm vessels (right). (A) Pit membranes, face view. (B) Side view schematic of membranes within the pit chamber formed by the secondary walls. Pits open and functioning in water transport. (C) Schematic of pit location within conduit network. (D) Side view of pits in sealed position showing proposed airseeding process (from Pittermann et al. 2005). often with no pores detectable, whereas inter-tracheid pits of conifers have a highly porous margo (pores ≫ 500 nm) (Petty and Preston 1969) peripheral to a central thickened torus (Figure 16A, left). The greater porosity of the margo decreases the area-specific pit resistance by an estimated 59-fold relative to inter-vessel pits of angiosperms (Pittermann et al. 2005). The homogenous-type pit membrane is presumably ancestral, and the implication is that the evolution of efficient torus-margo pitting, within in the gymnosperm lineage, was as hydraulically advantageous as the evolution of vessels in angiosperms.
332 Journal of Integrative Plant Biology Vol. 55 No. 4 2013 Pit membrane chemistry interacts with xylem sap chemistry to influence xylem flow resistance in a very complex and poorly understood manner. According to the “ionic effect”, increasing the concentration of KCl up to 50 mM (encompassing the physiological range) can decrease resistivity anywhere from 2% to 37% relative to pure water, depending on the angiosperm species and even the season (Nardini et al. 2011b). The KCl effect is much less or even negative in the already low-resistance torus-margo pits of conifer species (Cochard et al. 2010b). Furthermore, this KCl effect can be reduced or eliminated in the presence of as little as 1 mM Ca 2+ in some species and conditions (Van Iepeeren and Van Gelder 2006), but not in others (Nardini et al. 2011b). Skepticism about the importance of the phenomenon in planta (Van Iepeeren 2007) has been answered with observations indicating KCl-mediated decreases in resistivity associated with embolism and exposure of branches to sunlight (Nardini et al. 2011b). Interestingly, adaptive adjustments in KCl concentration may be mediated by xylem-phloem exchange (Zwieniecki et al. 2004). The ionic effect has been localized to the pit membranes, but the mechanism remains unknown. A “hydrogel” model implicates ionic shrinkage of pit membrane pectins or equivalent hydrogel polymers, and, hence, a widening of membrane pores (Zwieniecki et al. 2001b). However, recent observations with atomic force microscopy do not support a pore-widening effect. Although KCl was observed to thin the membrane, pores were not observed, suggesting that the decrease in resistance resulted from membrane thinning and perhaps increased permeability of non-porous gel material (Lee et al. 2012). The extent of pectins or similar gel materials in pit membranes appears to be highly variable across species, perhaps underlying the extreme variation in the ionic effect (Nardini et al. 2011b). Uncertainty about the extent of hydrogel components of pit membranes has led to an alternative (and perhaps complementary) hypothesis that ions increase permeability by reducing the diffuse-double layer of cations lining negatively charged nano-scale pores in the membrane (Van Doorn et al. 2011b). All of these hypotheses are consistent with a minor effect in torus-margo pit membranes, with their large micro-scale pores between cellulosic strands having presumably minimal pectin content. Although inter-conduit pits have the disadvantage of adding substantial flow resistance, they perform the highly advantageous function of trapping an air-water meniscus and minimizing the embolism event such that it does not compromise the conducting system (Figure 16B, C). The homogenous pits of angiosperm vessels have pores narrow enough to trap themeniscuswithaPmin negative enough to hold against a substantial range of negative ψP values (Figure 16D). The torusmargo pits function somewhat differently. The wider margo pores cannot sustain a very negative Pmin, but they can generate just enough pressure difference to aspirate the solid torus against the pit aperture on the water-filled side (Petty 1972). In this way, the torus can seal off the pit with a sufficiently negative Pmin to minimize air passage (Figure 16D). While inter-conduit pits minimize the propagation of embolism, as the next section indicates, they nevertheless play a major role in limiting the tensional gradient that can be generated by the cohesion-tension mechanism. Limits to negative ψ P values: the problem of cavitation Periodically, the cohesion-tension mechanism comes under question for its prediction of liquid pressures that fall below the vapor pressure of water, and also below pure vacuum for a gas (Canny 1998; Zimmermann et al. 2004). A tree 30 m tall requires a ψP of −0.3 MPa on its stationary water column just to balance the gravity component. To this we need to add, say, −0.3 MPa to balance a favorable soil water potential of −0.3 MPa. Finally, we need to add the typical ψP of −1 MPa needed to overcome frictional resistance under midday transpiration rates. The required ψP totals −1.6 MPa. At sea level and 20 ◦ C, a vapor pressure of only −0.098 MPa will bring water to its boiling point, and −0.1013 MPa corresponds to pure vacuum for a gas. Clearly, for the cohesion-tension mechanism to operate, transition from the liquid phase to the vapor phase must be suppressed, and the xylem sap must remain in a metastable liquid state. The xylem sap is in effect super-heated, although “super-tensioned” is more descriptive. The liquid water column becomes analogous to a solid whose strong atomic and intermolecular bonds allow it to be placed under tension; i.e., water is a tensile liquid! The concept of metastable water is foreign to the macroscopic world of normal human experience, hence the cohesiontension skeptics. Water boils at 100 ◦ C, and vacuum pumps become gas-locked at or above −0.098 MPa. But in these familiar cases, the phase change to vapor (cavitation) is nucleated by contact with foreign agents that destabilize the inter-molecular hydrogen-bonding of liquid water (Pickard 1981). Such “heterogeneous nucleation” of cavitation is typically triggered by minute and ubiquitous gas bubbles in the system. When care is taken to minimize such heterogeneous nucleation, liquid water can develop substantially metastable negative ψP values. Theoretical calculations, based on equations of state for water, put the limiting ψP at homogeneous cavitation (where energy of the water molecules themselves is sufficient to trigger the phase change) below −200 MPa at 20 ◦ C(Mercury and Tardy 2001). Experiments with a variety of systems ranging from centrifuged capillary tubes to water-filled quartz crystals have reached values well below −25 MPa, with some as low as −180 MPa and approaching the theoretical limit (Briggs 1950; Zheng et al. 1991). Such values dwarf even the most negative ψP in plants, which is about −13 MPa (Jacobson et al. 2007); more typical plant ψP values are less negative than −3 MPa.
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The Plant Vascular System: Evolution, Development and FunctionsF

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